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<!doctype html> <html data-n-head-ssr lang="en" data-n-head="%7B%22lang%22:%7B%22ssr%22:%22en%22%7D%7D"> <head > <link data-n-head="ssr" rel="icon" type="image/png" sizes="16x16" href="https://brand.frontiersin.org/m/ed3f9ce840a03d7/favicon_16-tenantFavicon-Frontiers.png"> <link data-n-head="ssr" rel="icon" type="image/png" sizes="32x32" href="https://brand.frontiersin.org/m/ed3f9ce840a03d7/favicon_32-tenantFavicon-Frontiers.png"> <link data-n-head="ssr" rel="apple-touch-icon" type="image/png" sizes="180x180" href="https://brand.frontiersin.org/m/ed3f9ce840a03d7/favicon_180-tenantFavicon-Frontiers.png"> <title>Frontiers | Transcriptional Response of Two Brassica napus Cultivars to Short-Term Hypoxia in the Root Zone</title><meta data-n-head="ssr" charset="utf-8"><meta data-n-head="ssr" name="viewport" content="width=device-width, initial-scale=1"><meta data-n-head="ssr" data-hid="charset" charset="utf-8"><meta data-n-head="ssr" data-hid="mobile-web-app-capable" name="mobile-web-app-capable" content="yes"><meta data-n-head="ssr" data-hid="apple-mobile-web-app-title" name="apple-mobile-web-app-title" content="Frontiers | Articles"><meta data-n-head="ssr" data-hid="theme-color" name="theme-color" content="#0C4DED"><meta data-n-head="ssr" data-hid="description" property="description" name="description" content="Waterlogging is one major stress for crops and causes multiple problems for plants, for example low gas diffusion, changes in redox potential and accumulatio..."><meta data-n-head="ssr" data-hid="og:title" property="og:title" name="title" content="Frontiers | Transcriptional Response of Two Brassica napus Cultivars to Short-Term Hypoxia in the Root Zone"><meta data-n-head="ssr" data-hid="og:description" property="og:description" name="description" content="Waterlogging is one major stress for crops and causes multiple problems for plants, for example low gas diffusion, changes in redox potential and accumulatio..."><meta data-n-head="ssr" data-hid="keywords" name="keywords" content="Brassica napus,waterlogging,root-zone hypoxia,fermenation,RNA sequencing"><meta data-n-head="ssr" data-hid="og:site_name" property="og:site_name" name="site_name" content="Frontiers"><meta data-n-head="ssr" data-hid="og:image" property="og:image" name="image" content="https://images-provider.frontiersin.org/api/ipx/w=1200&f=png/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g001.jpg"><meta data-n-head="ssr" data-hid="og:type" property="og:type" name="type" content="article"><meta data-n-head="ssr" data-hid="og:url" property="og:url" name="url" content="https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2022.897673/full"><meta data-n-head="ssr" data-hid="twitter:card" name="twitter:card" content="summary_large_image"><meta data-n-head="ssr" data-hid="citation_volume" name="citation_volume" content="13"><meta data-n-head="ssr" data-hid="citation_journal_title" name="citation_journal_title" content="Frontiers in Plant Science"><meta data-n-head="ssr" data-hid="citation_publisher" name="citation_publisher" content="Frontiers"><meta data-n-head="ssr" data-hid="citation_journal_abbrev" name="citation_journal_abbrev" content="Front. Plant Sci."><meta data-n-head="ssr" data-hid="citation_issn" name="citation_issn" content="1664-462X"><meta data-n-head="ssr" data-hid="citation_doi" name="citation_doi" content="10.3389/fpls.2022.897673"><meta data-n-head="ssr" data-hid="citation_firstpage" name="citation_firstpage" content="897673"><meta data-n-head="ssr" data-hid="citation_language" name="citation_language" content="English"><meta data-n-head="ssr" data-hid="citation_title" name="citation_title" content="Transcriptional Response of Two Brassica napus Cultivars to Short-Term Hypoxia in the Root Zone"><meta data-n-head="ssr" data-hid="citation_keywords" name="citation_keywords" content="Brassica napus; waterlogging; root-zone hypoxia; fermenation; RNA sequencing"><meta data-n-head="ssr" data-hid="citation_abstract" name="citation_abstract" content="<p>Waterlogging is one major stress for crops and causes multiple problems for plants, for example low gas diffusion, changes in redox potential and accumulation of toxic metabolites. <italic>Brassica napus</italic> is an important oil crop with high waterlogging sensitivity, which may cause severe yield losses. Its reactions to the stress are not fully understood. In this work the transcriptional response of rapeseed to one aspect of waterlogging, hypoxia in the root zone, was analyzed by RNAseq, including two rapeseed cultivars from different origin, Avatar from Europe and Zhongshuang 9 from Asia. Both cultivars showed a high number of differentially expressed genes in roots after 4 and 24 h of hypoxia. The response included many well-known hypoxia-induced genes such as genes coding for glycolytic and fermentative enzymes, and strongly resembled the hypoxia response of the model organism <italic>Arabidopsis thaliana</italic>. The carbohydrate status of roots, however, was minimally affected by root hypoxia, with a tendency of carbohydrate accumulation rather than a carbon starvation. Leaves did not respond to the root stress after a 24-h treatment. In agreement with the gene expression data, subsequent experiments with soil waterlogging for up to 14 days revealed no differences in response or tolerance to waterlogging between the two genotypes used in this study. Interestingly, using a 0.1% starch solution for waterlogging, which caused a lowered soil redox potential, resulted in much stronger effects of the stress treatment than using pure water suggesting a new screening method for rapeseed cultivars in future experiments.</p>"><meta data-n-head="ssr" data-hid="citation_pdf_url" name="citation_pdf_url" content="https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2022.897673/pdf"><meta data-n-head="ssr" data-hid="citation_online_date" name="citation_online_date" content="2022/04/11"><meta data-n-head="ssr" data-hid="citation_publication_date" name="citation_publication_date" content="2022/04/29"><meta data-n-head="ssr" data-hid="citation_author_0" name="citation_author" content="Ambros, Stefanie"><meta data-n-head="ssr" data-hid="citation_author_institution_0" name="citation_author_institution" content="Department of Plant Physiology, University of Bayreuth, Germany"><meta data-n-head="ssr" data-hid="citation_author_1" name="citation_author" content="Kotewitsch, Mona"><meta data-n-head="ssr" data-hid="citation_author_institution_1" name="citation_author_institution" content="Department of Plant Physiology, University of Bayreuth, Germany"><meta data-n-head="ssr" data-hid="citation_author_2" name="citation_author" content="Wittig, Philipp R."><meta data-n-head="ssr" data-hid="citation_author_institution_2" name="citation_author_institution" content="Department of Plant Physiology, University of Bayreuth, Germany"><meta data-n-head="ssr" data-hid="citation_author_3" name="citation_author" content="Bammer, Bettina"><meta data-n-head="ssr" data-hid="citation_author_institution_3" name="citation_author_institution" content="Department of Plant Physiology, University of Bayreuth, Germany"><meta data-n-head="ssr" data-hid="citation_author_4" name="citation_author" content="Mustroph, Angelika"><meta data-n-head="ssr" data-hid="citation_author_institution_4" name="citation_author_institution" content="Department of Plant Physiology, University of Bayreuth, Germany"><meta data-n-head="ssr" data-hid="dc.identifier" name="dc.identifier" content="doi:10.3389/fpls.2022.897673"><link data-n-head="ssr" rel="manifest" href="/article-pages/_nuxt/manifest.c499fc0a.json" data-hid="manifest"><link data-n-head="ssr" rel="canonical" href="https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2022.897673/full"><script data-n-head="ssr" data-hid="newrelic-browser-script" type="text/javascript">window.NREUM||(NREUM={});NREUM.info = {"agent":"","beacon":"bam.nr-data.net","errorBeacon":"bam.nr-data.net","licenseKey":"598a124f17","applicationID":"588603994","agentToken":null,"applicationTime":2.344063,"transactionName":"MQcDMkECCkNSW0YMWghNIgldDQFTRxd1IGFJTQ==","queueTime":0,"ttGuid":"0b8598a43eda193b"}; (window.NREUM||(NREUM={})).init={privacy:{cookies_enabled:true},ajax:{deny_list:["bam.nr-data.net"]},distributed_tracing:{enabled:true}};(window.NREUM||(NREUM={})).loader_config={agentID:"594400880",accountID:"230385",trustKey:"230385",xpid:"VgUHUl5WGwYIXFdSBAgOUg==",licenseKey:"598a124f17",applicationID:"588603994"};;/*! 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</div> <div class="ArticleDetailsEditors__ediorInfo__affiliation"> University of Pisa, Italy </div></div></a></div></div> <div class="ArticleDetailsEditors"><div class="ArticleDetailsEditors__editors"><div class="ArticleDetailsEditors__title">Reviewed by</div> <a href="https://loop.frontiersin.org/people/140716/overview" data-event="editorInfo-a-arunKShanker" class="ArticleDetailsEditors__ediorInfo"><figure class="Avatar Avatar--size-32"><img src="https://loop.frontiersin.org/images/profile/140716/32" alt="Arun K. 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Shanker </div> <div class="ArticleDetailsEditors__ediorInfo__affiliation"> Central Research Institute for Dryland Agriculture (ICAR), India </div></div></a><a href="https://loop.frontiersin.org/people/357256/overview" data-event="editorInfo-a-davidJespersen" class="ArticleDetailsEditors__ediorInfo"><figure class="Avatar Avatar--size-32"><img src="https://loop.frontiersin.org/images/profile/357256/32" alt="David Jespersen" class="Avatar__img is-inside-mask"></figure> <div class="ArticleDetailsEditors__ediorInfo__info"><div class="ArticleDetailsEditors__ediorInfo__name"> David Jespersen </div> <div class="ArticleDetailsEditors__ediorInfo__affiliation"> University of Georgia, United States </div></div></a><a href="https://loop.frontiersin.org/people/811663/overview" data-event="editorInfo-a-muhammadFarooq" class="ArticleDetailsEditors__ediorInfo"><figure class="Avatar Avatar--size-32"><img src="https://loop.frontiersin.org/images/profile/811663/32" alt="Muhammad Farooq" class="Avatar__img is-inside-mask"></figure> <div class="ArticleDetailsEditors__ediorInfo__info"><div class="ArticleDetailsEditors__ediorInfo__name"> Muhammad Farooq </div> <div class="ArticleDetailsEditors__ediorInfo__affiliation"> University of Teramo, Italy </div></div></a></div></div> <div class="ArticleDetailsGlossary ArticleDetailsGlossary--open"><button class="ArticleDetailsGlossary__header"><div class="ArticleDetailsGlossary__header__title">Table of contents</div> <div class="ArticleDetailsGlossary__header__arrow"></div></button> <div class="ArticleDetailsGlossary__content"><ul class="flyoutJournal"> <li><a href="#h1">Abstract</a></li> <li><a href="#h2">Introduction</a></li> <li><a href="#h3">Materials and Methods</a></li> <li><a href="#h4">Results</a></li> <li><a href="#h5">Discussion</a></li> <li><a href="#h6">Conclusion</a></li> <li><a href="#h7">Data Availability Statement</a></li> <li><a href="#h8">Author Contributions</a></li> <li><a href="#fun1">Funding</a></li> <li><a href="#conf1">Conflict of Interest</a></li> <li><a href="#disclaimer1">Publisher’s Note</a></li> <li><a href="#ack1">Acknowledgments</a></li> <li><a href="#S10">Supplementary Material</a></li> <li><a href="#abbr1">Abbreviations</a></li> <li><a href="#refer1">References</a></li> </ul> </div></div>  <div class="ActionsDropDown"><button aria-label="Open dropdown" data-event="actionsDropDown-button-toggle" class="ActionsDropDown__button ActionsDropDown__button--typeOutline ActionsDropDown__button--iconQuote"><span class="ActionsDropDown__button__label">Export citation</span></button> <div class="ActionsDropDown__menuWrapper"> <ul class="ActionsDropDown__menu"><li><a href="/journals/plant-science/articles/10.3389/fpls.2022.897673/endNote" target="_blank" rel="noopener noreferrer" data-event="actionsDropDown-a-endNote" class="ActionsDropDown__option"> EndNote </a></li><li><a href="/journals/plant-science/articles/10.3389/fpls.2022.897673/reference" target="_blank" rel="noopener noreferrer" 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Plant Sci.</span><span>, 29 April 2022</span></div> <div class="ArticleLayoutHeader__info__journalDate"> Sec. Plant Abiotic Stress </div> <div class="ArticleLayoutHeader__info__doiVolume"><span> Volume 13 - 2022 | </span> <a href="https://doi.org/10.3389/fpls.2022.897673" class="ArticleLayoutHeader__info__doi"> https://doi.org/10.3389/fpls.2022.897673 </a></div> </div>  <div class="ArticleLayoutHeader__isPartOfRT"><span class="ArticleLayoutHeader__isPartOfRT__label">This article is part of the Research Topic</span> <span class="ArticleLayoutHeader__isPartOfRT__title">Adaptation of Plants to Waterlogging and Hypoxia</span> <span class="Link__wrapper"><a aria-label="View all 15 articles" href="https://www.frontiersin.org/research-topics/27508/adaptation-of-plants-to-waterlogging-and-hypoxia/articles" target="_self" data-event="customLink-link-a_viewAll15Articles" class="Link Link--linkType Link--maincolor Link--medium Link--icon Link--chevronRight Link--right"><span>View all 15 articles</span></a></span></div></div> <div class="ArticleDetails__main__content"><div class="ArticleDetails__main__content__main ArticleDetails__main__content__main--fullArticle"><div class="JournalAbstract"><div class="JournalAbstract__titleWrapper"><h1>Transcriptional Response of Two <i>Brassica napus</i> Cultivars to Short-Term Hypoxia in the Root Zone</h1> </div> </div> <div class="JournalFullText"><div class="JournalAbstract"> <a id="h1" name="h1"></a> <div class="authors"><span class="author-wrapper"> <img class="pr5" src="https://loop.frontiersin.org/cdn/images/profile/default_32.jpg" alt="\r\nStefanie Ambros" onerror="this.onerror=null;this.src='https://loop.frontiersin.org/cdn/images/profile/default_32.jpg';">Stefanie Ambros</span><span class="author-wrapper"><img class="pr5" src="https://loop.frontiersin.org/cdn/images/profile/default_32.jpg" alt="Mona Kotewitsch" onerror="this.onerror=null;this.src='https://loop.frontiersin.org/cdn/images/profile/default_32.jpg';">Mona Kotewitsch</span><span class="author-wrapper"><img class="pr5" src="https://loop.frontiersin.org/cdn/images/profile/default_32.jpg" alt="Philipp R. Wittig" onerror="this.onerror=null;this.src='https://loop.frontiersin.org/cdn/images/profile/default_32.jpg';">Philipp R. Wittig</span><span class="author-wrapper"><img class="pr5" src="https://loop.frontiersin.org/cdn/images/profile/default_32.jpg" alt="Bettina Bammer" onerror="this.onerror=null;this.src='https://loop.frontiersin.org/cdn/images/profile/default_32.jpg';">Bettina Bammer</span><span class="author-wrapper"><a href="https://loop.frontiersin.org/people/27285" class="user-id-27285"><img class="pr5" src="https://loop.frontiersin.org/images/profile/27285/74" onerror="this.onerror=null;this.src='https://loop.frontiersin.org/cdn/images/profile/default_32.jpg';" alt="Angelika Mustroph*\r\n">Angelika Mustroph</a><sup>*</sup> </span></div> <ul class="notes"> <li class="pl0">Department of Plant Physiology, University of Bayreuth, Bayreuth, Germany</li> </ul> <p class="mb0">Waterlogging is one major stress for crops and causes multiple problems for plants, for example low gas diffusion, changes in redox potential and accumulation of toxic metabolites. <i>Brassica napus</i> is an important oil crop with high waterlogging sensitivity, which may cause severe yield losses. Its reactions to the stress are not fully understood. In this work the transcriptional response of rapeseed to one aspect of waterlogging, hypoxia in the root zone, was analyzed by RNAseq, including two rapeseed cultivars from different origin, Avatar from Europe and Zhongshuang 9 from Asia. Both cultivars showed a high number of differentially expressed genes in roots after 4 and 24 h of hypoxia. The response included many well-known hypoxia-induced genes such as genes coding for glycolytic and fermentative enzymes, and strongly resembled the hypoxia response of the model organism <i>Arabidopsis thaliana</i>. The carbohydrate status of roots, however, was minimally affected by root hypoxia, with a tendency of carbohydrate accumulation rather than a carbon starvation. Leaves did not respond to the root stress after a 24-h treatment. In agreement with the gene expression data, subsequent experiments with soil waterlogging for up to 14 days revealed no differences in response or tolerance to waterlogging between the two genotypes used in this study. Interestingly, using a 0.1% starch solution for waterlogging, which caused a lowered soil redox potential, resulted in much stronger effects of the stress treatment than using pure water suggesting a new screening method for rapeseed cultivars in future experiments.</p> <div class="clear"></div> </div> <div class="JournalFullText"> <a id="h2" name="h2"></a><h2>Introduction</h2> <p class="mb15">Many crop plants are very sensitive to flooding periods which may occur after heavy rainfall, rising sea water, or during fast snow melting in spring. Besides other effects, flooding severely restricts gas diffusion into and out of the plant tissues that are under water, leading to deficiency in oxygen and carbon dioxide. The increased frequency of extreme weather events due to climate change affects certain regions around the world, and these regions at risk might expand in the future even more (e.g., <a href="#B35">Kundzewicz et al., 2014</a>; <a href="#B67">Trenberth et al., 2014</a>; <a href="#B59">Pekel et al., 2016</a>; <a href="#B8">Blöschl et al., 2019</a>). Flooding events can be differentiated into two types that require different adaptations of plants, namely full submergence and root waterlogging (<a href="#B64">Sasidharan et al., 2017</a>).</p> <p class="mb15">Waterlogging is considered as the lesser problematic stress type. Many plants have developed adaptational mechanisms to cope with this type of stress, resulting in an avoidance or a tolerance strategy. One very important response to waterlogging is the formation of aerenchyma tissue within leaves, stems and roots, thus avoiding oxygen deficiency within plant organs that are under water (summarized in <a href="#B69">Voesenek and Bailey-Serres, 2015</a>; <a href="#B53">Mustroph et al., 2018</a>; <a href="#B77">Yamauchi et al., 2018</a>). Other mechanisms such as a barrier against radial oxygen loss in underwater organs and the formation of adventitious roots with high porosity also help to maintain a sufficient oxygen content within plant tissues.</p> <p class="mb15">Besides these avoidance mechanisms, there are also acclimation responses that enable tolerance to low oxygen concentrations within plant tissues at least for some time (summarized in <a href="#B5">Bailey-Serres et al., 2012</a>; <a href="#B69">Voesenek and Bailey-Serres, 2015</a>; <a href="#B53">Mustroph et al., 2018</a>). These mainly include biochemical modifications such as induction of glycolysis and fermentation in order to maintain energy production through periods with limited mitochondrial respiration. These responses also include specific enzymes or isoforms of starch and sucrose cleavage and glycolytic by-passes (summarized in <a href="#B27">Huang et al., 2008</a>; <a href="#B51">Mustroph et al., 2014</a>, <a href="#B53">2018</a>; <a href="#B4">Atwell et al., 2015</a>). Furthermore, growth and biosynthetic processes are strongly down-regulated under low-oxygen stress, including ribosomal activity on non-essential transcripts, since translation is an energy-consuming process (<a href="#B10">Branco-Price et al., 2008</a>; <a href="#B54">Mustroph et al., 2009</a>).</p> <p class="mb15">However, most crop species cannot tolerate longer periods of waterlogging since they only possess a limited acclimation potential. <i>Brassica napus</i> is an important oil crop plant and it is also used for animal feed. However, this plant species is very sensitive to soil flooding and waterlogging, since it is not able to form aerenchyma in the roots and exhibits a high radial oxygen loss under water (<a href="#B70">Voesenek et al., 1999</a>). Still, rapeseed is often used as a rotation crop on rice fields in Asia (<a href="#B78">Zou et al., 2013a</a>; <a href="#B38">Lee et al., 2014</a>), and therefore is often subjected to flooding conditions. Despite the importance and sensitivity of this crop, little is known about its molecular response to flooding conditions such as waterlogging and submergence. Such information could be vital to develop cultivars with enhanced flooding tolerance.</p> <p class="mb15">Indeed, several approaches have been used to identify rapeseed cultivars with higher waterlogging tolerance within the last years, mainly focusing on Asian cultivars (e.g., <a href="#B79">Zou et al., 2013b</a>,<a href="#B80">2014</a>; summarized in <a href="#B48">Mustroph, 2018</a>). However, the molecular bases for these tolerance traits are still not known, despite efforts to study the response of different cultivars at the level of transcriptome (<a href="#B78">Zou et al., 2013a</a>,<a href="#B81">2015</a>) and proteome (<a href="#B75">Xu et al., 2018</a>). Mapping processes of these cultivars with contrasting responses are ongoing, with no clear results so far (<a href="#B16">Ding et al., 2020</a>). There could be several reasons for it. For example, the molecular analyses were performed at specific developmental stages or with a stress duration that did not reveal differences between the cultivars. The other possibility would be that little genetic differences in waterlogging tolerance exist between genotypes studied so far, despite interesting observations in the field. We therefore raised the following hypothesis: if differences in waterlogging tolerance between contrasting rapeseed cultivars exist, those should emerge through a comparison of an Asian cultivar with observed waterlogging tolerance, Zhongshuang 9 (<a href="#B79">Zou et al., 2013b</a>,<a href="#B80">2014</a>), and a European cultivar not bred for flooding tolerance.</p> <p class="mb15">There is evidence that <i>Brassica napus</i> roots can respond to waterlogging and the associated hypoxia at the transcriptional level, for example by induction of genes coding for fermentative enzymes (<a href="#B78">Zou et al., 2013a</a>,<a href="#B81">2015</a>), while leaves above air responded in a different way (<a href="#B38">Lee et al., 2014</a>). On the other hand, avoidance mechanisms such as the formation of aerenchyma are not present in this species (<a href="#B70">Voesenek et al., 1999</a>; <a href="#B60">Ploschuk et al., 2018</a>). However, the existing transcriptome analyses were performed without the full genome information on <i>Brassica napus</i>, which was only published later (<a href="#B13">Chalhoub et al., 2014</a>). It is therefore not known whether all or only a few gene copies for one gene function of the tetraploid species are hypoxia responsive. We hypothesize that most or all gene copies of a hypoxia-induced gene in the rapeseed genome are responsive to the stress treatment, which would require modification of not only one but multiple target genes by breeders.</p> <p class="mb0">The aim of our work was to (1) compare the transcriptional responses of two different <i>Brassica napus</i> cultivars to one aspect of waterlogging, hypoxic conditions in the root zone, including the analysis of roots and leaves at two different time points and (2) to evaluate with different growth conditions whether a difference in waterlogging tolerance exists between the two cultivars. In our previous analysis utilizing the same two cultivars (<a href="#B73">Wittig et al., 2021</a>), we could not identify significant differences in submergence tolerance, but a strong transcriptional response to submergence in leaves of both genotypes. Here, we also identified a large number of transcripts induced by hypoxia in roots, which were mainly similar between the cultivars and also similar to the transcriptional response of <i>Arabidopsis thaliana</i> to hypoxia (<a href="#B54">Mustroph et al., 2009</a>, <a href="#B52">2010</a>; <a href="#B37">Lee and Bailey-Serres, 2019</a>). However, the response of hypoxic roots was very different from submerged rapeseed leaves. In addition, and in accordance with our analysis under submergence, we could not identify differences in waterlogging tolerance between the two cultivars, despite the application of several growth conditions and stress treatment methods.</p> <a id="h3" name="h3"></a><h2>Materials and Methods</h2> <h3 class="pt0">Plant Material and Growth Conditions</h3> <p class="mb15">Seeds of two rapeseed cultivars were used, the hybrid winter cultivar Avatar (<a href="#B74">Wollmer et al., 2018</a>; <a href="#B73">Wittig et al., 2021</a>) as well as the semi-winter cultivar Zhongshuang 9 (<a href="#B78">Zou et al., 2013a</a>; <a href="#B73">Wittig et al., 2021</a>).</p> <p class="mb15">For the experiments with plants in hydroponics, dry seeds were sterilized in a chlorine gas atmosphere for 45 min. After removal of the gas, the sterilized seeds were germinated in small tubes containing 1:10 Hoagland solution (0.28 mM Ca(NO<sub>3</sub>)<sub>2</sub>, 0.1 mM (NH<sub>4</sub>)H<sub>2</sub>PO<sub>4</sub>, 0.2 mM MgSO<sub>4</sub>, 0.6 mM KNO<sub>3</sub>, 5 μM of a complex of Fe(III) and N,N′-di-(2-hydroxybenzoyl)-ethylenediamine-N,N′-diacetate (ABCR, Karlsruhe, Germany), pH 5.7). Plants were grown in a short-day chamber (8 h illumination with ca. 100 μmol photons * m<sup>–2</sup> * s<sup>–1</sup>) at 23°C. After 4 days, the tubes were transferred into large buckets (4.5 l of volume) by use of a perforated plate. The buckets were filled with KNOP nutrient solution (<a href="#B50">Mustroph et al., 2006</a>), which was continuously bubbled with air. The nutrient solution was replaced twice a week. When plants were 15 days old, the stress treatment was applied to half of the plants by bubbling the nutrient solution with nitrogen gas for the time indicated. The shoot tissues remained in air.</p> <p class="mb0">For the experiments with plants on soil, seeds were pre-germinated in the dark at 30°C for 24 h on moist filter paper. Subsequently, germinating seeds were transferred into pots (5.3 × 5.3 cm) filled with a soil-sand mixture. The soil used was standard potting soil type GS90 coarse: potting soil (Ökohum GmbH): vermiculite in a ratio of 3:3:1. The potting soil was mixed with sand in a ratio of 3:1. Plants were grown in a short-day chamber (8 h illumination with ca. 100 μmol photons * m<sup>–2</sup> * s<sup>–1</sup>) at 23°C. 15-day-old plants were used for the experiments. For stress treatment of soil-grown plants, two waterlogging variants were used. In a first set, pots were placed in a box, which was subsequently filled with tap water up to the soil surface. In a second set, one portion of the pots were placed into boxes and filled with a 0.1% starch solution in deionized water (<a href="#B44">Mano and Takeda, 2012</a>; <a href="#B46">Miricescu et al., 2021</a>), while another portion of the pots were waterlogged with deionized water only. Control pots were watered regularly as needed. Both treatments lasted for two weeks. The number of plants per replicate is specified in the respective figure part.</p> <h3>RNA Extraction, RNA Sequencing and Bioinformatics</h3> <p class="mb15">For transcriptome analyses, root and leaf tissue from plants grown in hydroponics were used. Plants were stressed with 4 and 24 h of nitrogen flushing of the medium in the root zone. Subsequently, the entire root system and the first true leaf was harvested together with air-gassed controls and immediately frozen in liquid nitrogen. The frozen tissue was ground in liquid nitrogen. RNA extraction, quality control, processing of the RNA for sequencing, and the subsequent bioinformatics analyses were carried out exactly as previously described (<a href="#B73">Wittig et al., 2021</a>). Briefly, RNA was extracted by use of the ISOLATE II RNA plant kit (Bioline, Luckenwalde, Germany). After quality controls through gel electrophoresis and fluorimeter measurements, RNA was further processed by Eurofins Genomics Europe Shared Services GmbH (Ebersberg, Germany). Sequencing was done with the 150 bp paired-end mode on the Illumina HiSeq 4000 platform.</p> <p class="mb0">Three replicates per time point and genotype were done, resulting in a total of 36 libraries, with 30 Mio to 50 Mio reads per library (<a href="#S10">Supplementary Table 1</a>). Transcript quantification was done by use of the Kallisto software (<a href="#B11">Bray et al., 2016</a>). About 76 to 80% of the reads from the cultivar Avatar aligned to the reference genome of Darmor (<a href="#B13">Chalhoub et al., 2014</a>). Reads from the cultivar Zhongshuang 9 had a mapping rate of 67 to 75% (<a href="#S10">Supplementary Table 1</a>). Mapping rates for leaves were generally higher than for roots and were similar to the mapping rates in our previous study (<a href="#B73">Wittig et al., 2021</a>). DEG analysis was carried out with the edgeR and limma Bioconductor packages in R (<a href="#B45">McCarthy et al., 2012</a>) as previously described (<a href="#B47">Müller et al., 2021</a>). RNA sequencing raw and processed data have been deposited at the Gene Expression Omnibus database under the accession GSE180262.</p> <h3>Enzyme Extraction and ADH Activity</h3> <p class="mb0">Frozen root material from plants grown in hydroponics was ground to a fine powder. Enzymes were extracted in 50 mM Hepes-KOH, pH 6.8 containing 5 mM Mg acetate, 5 mM β-mercaptoethanol, 15% (v/v) glycerin, 1 mM EDTA, 1 mM EGTA, and 0.1 mM Pefabloc proteinase inhibitor (Sigma-Aldrich, Germany). The samples were then centrifuged at 13,000 g at 4°C for 15 min. The resulting supernatant was used for spectrophotometric determination of ADH activity at 340 nm (SPECORD 200 PLUS, Analytic Jena, Germany). The ADH activity was measured in 50 mM TES buffer, pH 7.5 including 0.17 mM NADH (<a href="#B72">Waters et al., 1991</a>). The reaction was started by adding 10 mM acetaldehyde. The protein content as determined by the Bradford reagent and by use of a BSA standard curve (<a href="#B9">Bradford, 1976</a>). The number of biological replicates is specified in the respective figure part.</p> <h3>Carbohydrate Extraction and Measurement of Sugar Content</h3> <p class="mb15">One leaf of each plant (from hydroponics or soil-grown plants) was frozen in liquid nitrogen and the fresh weight of the samples was determined. The frozen plant samples were ground to a fine powder. To extract soluble sugars, 1 ml of 0.83 N perchloric acid was added, mixed well, and then stored on ice until all samples were processed. The samples were then centrifuged for 15 min at 13,000 g and 4°C, and the supernatant was transferred to a new 1.5 ml Eppendorf reaction tube. The pellet was overlaid with 600 μl of 80% ethanol for subsequent starch extraction and temporarily stored at 4°C. The supernatant was mixed with 200 μl of 1 M Bicine and quickly neutralized with 100 μl of 4 M KOH. The samples were then centrifuged for 10 min at 13,200 rpm and 4°C and the supernatant was transferred to a new reaction tube. The supernatant was either frozen at −20°C or used directly for the measurement of the sugar content.</p> <p class="mb15">For starch extraction, the pellet from sugar extraction was mixed with 600 μl of 80% ethanol and centrifuged at 13,000 g and 4°C for 5 min. The supernatant was then removed, and the procedure was repeated once. After removal of the ethanol, 400 μl of 0.2 M KOH was added to the pellet and the samples were homogenized. This was placed on a heating block at 95°C for 1 h. After incubation, the samples were centrifuged for 5 min at 10,000 rpm and 4°C, and the supernatant was transferred to a new 1.5 ml reaction tube. The supernatant was neutralized with 80 μl of 1 N acetic acid. From the extract, 50 μl was then mixed with 100 μl amyloglucosidase (2 mg/ml enzyme in 50 mM sodium acetate pH 5.0) and incubated overnight at 55°C on the heating block.</p> <p class="mb0">Both sugar and starch content were measured spectrophotometrically (SPECORD 200 PLUS, Analytic Jena, Germany). For this, 780 μl of 0.1 M imidazole buffer containing 1 mM ATP and 2 mM NAD in a semi-micro cuvette was mixed with 20 μl of each sample and 1 u glucose-6-phosphate dehydrogenase was added. Then, the measurement was started at a wavelength of 340 nm. For both the sugar and the starch measurement 0.5 u of hexokinase in 5 μl of imidazole buffer was added after 10 min to measure glucose. Starch measurement was stopped 20 min after addition of the enzyme. For soluble sugars, 0.2 u phosphoglucose isomerase in 5 μl buffer was pipetted to the samples after a plateau was reached, to measure fructose. After constant values had again been established, 60 u invertase in 5 μl buffer was added and mixed well to determine the sucrose content. The number of biological replicates is specified in the respective figure part.</p> <h3>Chlorophyll Fluorescence and Chlorophyll Content</h3> <p class="mb15">To determine the chlorophyll fluorescence, the quantum yield of photosystem II of the plants grown on soil was measured under constant conditions using a Junior-PAM (Walz, Effeltrich, Germany). This PAM measurement (pulse-amplitude-modulated fluorescence measurement) was performed using a saturating pulse method (SAT pulses). A large adult light-adapted leaf of each plant was clamped between two magnets and irradiated for 10 seconds with ambient light of about 100 μmol photons * m<sup>–2</sup> * s<sup>–1</sup>, and subsequently a saturation pulse was applied. The ΦPSII value was calculated and used for further evaluation.</p> <p class="mb15">Determination of chlorophyll content in an invasive way was done as follows. Extraction of chlorophyll was performed according to the protocol of <a href="#B57">Park et al. (2018)</a>. In this process, 1.4 ml of 80% aqueous acetone was added to frozen and ground leaf samples and mixed well. Then, the samples were stored overnight at 4°C. The next day, the leaf samples were centrifuged at 13,000 g for 5 min at 4°C and the supernatant was pipetted into a new tube. For measurement of chlorophyll content, the supernatant was diluted 1:10 with acetone in a semi-micro cuvette and absorbance was measured at 645 nm and 663 nm. Chlorophyll content was calculated by use of the formula developed by <a href="#B2">Arnon (1949)</a>.</p> <p class="mb0">Determination of chlorophyll content in a non-invasive way was done by use of the chlorophyll concentration meter MC-100 (Apogee Instruments, Logan, United States) using the settings for kohlrabi.</p> <h3>Chemical Parameters of the Waterlogging Solution</h3> <p class="mb0">Oxygen content, oxidation-reduction potential (ORP), pH and conductivity of the waterlogging solution of soil-grown plants was determined by use of the multimeter PCE-PHD 1 (PCE instruments, Meschede, Germany) and the following electrodes: OXPB-11, ORP-14, PE-03, CDPB-03. Measurements were done about 2 to 3 h after start of illumination. The temperature of the waterlogging solution ranged between 19 and 23°C at the time of the measurements.</p> <a id="h4" name="h4"></a><h2>Results</h2> <h3 class="pt0">Transcriptome Analysis Under Root Hypoxia</h3> <p class="mb15">Waterlogging is a complex stress in nature, including limited gas diffusion, microbial activities, changes in redox chemistry and accumulation of toxic metabolites. In a simplified approach we initially focused on the low-oxygen component of waterlogging and therefore performed an RNAseq analysis of plants in hydroponics with their roots exposed to nitrogen gassing causing hypoxia (<a href="#S10">Supplementary Table 1</a>). This experimental set-up also allowed for controlled aeration of the root system and allowed a direct comparison to the hypoxia response of the model species <i>Arabidopsis thaliana</i> (<a href="#B54">Mustroph et al., 2009</a>).</p> <p class="mb0">Treating plant roots with hypoxia caused a strong transcriptional response in roots of both genotypes. After 4 h, 5,736 and 3,948 transcripts were significantly up-regulated compared to air-treated controls (log2FC > 1, FDR < 0.01) in Avatar and Zhongshuang 9, respectively, with an overlap of 3,145 transcripts (<a href="#F1">Figure 1</a> and <a href="#S10">Supplementary Table 2</a>, columns R to AD). After 24 h, 2,550 and 3,061 transcripts were induced, with an overlap of 1,729 transcripts. The overlap between 4 h and 24 h was 1,897 and 1,844 transcripts for Avatar and Zhongshuang 9, respectively (<a href="#S10">Supplementary Figure 1</a>). The number of down-regulated genes in roots was even higher. 8,983 and 7,010 transcripts were down-regulated after 4 h, and 4,415 and 5,619 transcripts were down-regulated after 24 h in Avatar and Zhongshuang 9, respectively. Again, there was a high similarity between the time points with 2,952 and 3,237 transcripts commonly downregulated in Avatar and Zhongshuang 9, respectively (<a href="#S10">Supplementary Figure 1</a>). The response of the leaves to hypoxia in the root zone was only analyzed after 24 h and was much lower, with 341 and 112 transcripts significantly induced in Avatar and Zhongshuang 9, with an overlap of only 12 transcripts. 564 and 418 transcripts were significantly down-regulated in leaves, with an overlap of 88 transcripts (<a href="#F1">Figure 1</a> and <a href="#S10">Supplementary Table 2</a>, columns R to AD).</p> <div class="DottedLine"></div> <div class="Imageheaders">FIGURE 1</div> <div class="FigureDesc"> <a href="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g001.jpg" name="figure1" target="_blank"> <picture> <source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=480&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g001.jpg" media="(max-width: 563px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=370&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g001.jpg" media="(max-width: 1024px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=290&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g001.jpg" media="(max-width: 1441px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=410&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g001.jpg" media=""><source type="image/jpg" srcset="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g001.jpg" media=""> <img src="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g001.jpg" alt="www.frontiersin.org" id="F1" loading="lazy"> </picture> </a> <p><strong>Figure 1.</strong> Venn diagrams showing overlaps of induced <b>(A,C,E)</b> or repressed <b>(B,D,F)</b> genes between two <i>Brassica napus</i> cultivars (Avatar, Zhongshuang 9) in hydroponics after 4 and 24 h of root hypoxia, compared with aerated controls. <b>(A,B)</b> Roots were treated with 4 h of hypoxia; <b>(C,D)</b> Roots were treated with 24 h of hypoxia; <b>(E,F)</b> Leaves of plants treated with root hypoxia for 24 h.</p> </div> <div class="clear"></div> <div class="DottedLine"></div> <h3>Roots Induce a Typical and Strong Hypoxia Response</h3> <p class="mb15">A functional gene ontology (GO) analysis of the transcripts of roots responding to nitrogen-gassing revealed many GO categories to be significantly enriched (<a href="#S10">Supplementary Table 3</a>). After 4 h, many categories involved in stress response were enriched, for example “response to chitin,” “heat acclimation,” “respiratory burst involved in defense response,” and “intracellular signal transduction”. Furthermore, hormonal responses were induced, such as “response to ethylene,” “response to jasmonic acid,” and “salicylic acid mediated signaling pathway.” The hypoxia-related terms “response to hypoxia” and “anaerobic respiration” were enriched, and this enrichment was even higher after 24 h. Comparison of genotypes revealed a very similar response, but surprisingly, a few chloroplast-related GOs were enriched only in Avatar roots after 4 h (<a href="#S10">Supplementary Table 3</a>).</p> <p class="mb15">In general, the response in roots after 24 h was very similar to the response after 4 h, but fewer genes remained induced (<a href="#S10">Supplementary Figure 1</a>). The functional categories “jasmonic acid biosynthetic process,” “response to water deprivation,” and “endoplasmic reticulum unfolded protein response” were less enriched after 24 than after 4 h (<a href="#S10">Supplementary Table 3</a>).</p> <p class="mb15">Among down-regulated genes after 4 h, we observed the functional categories “extracellular region,” “anchored component of membrane,” “cell proliferation,” “histone H3-K9 methylation,” “plant-type cell wall,” and categories associated with DNA replication. DNA replication was still enriched in Zhongshuang 9 after 24 h, but much less affected in Avatar after 24 h. In contrast, some categories, for example “trichoblast differentiation”, were more enriched in Avatar after 4 and 24 h than in the other genotype. Furthermore, “Casparian strip” was more enriched after 24 than 4 h in both genotypes. Among enriched GO terms of down-regulated genes, many were associated with biosynthetic processes (<a href="#S10">Supplementary Table 3</a>).</p> <p class="mb0">The enrichment of hypoxia-related categories in this dataset let us to compare the rapeseed hypoxia response to the previously defined hypoxia core response genes (HRGs) of Arabidopsis (<a href="#B54">Mustroph et al., 2009</a>). Indeed, of the 49 HRGs from Arabidopsis (<a href="#F2">Figure 2</a>), which correspond to 161 expressed transcripts in rapeseed (<a href="#S10">Supplementary Figure 2</a>), 118 to 127 transcripts responded to hypoxia in roots after 4 and 24 h, and therefore showed a highly significant enrichment (<a href="#S10">Supplementary Table 2</a>, column Q; <a href="#S10">Supplementary Table 4</a>). In many cases, most or all isogenes of one HRG in Arabidopsis responded in a similar manner to the stress in rapeseed, but with some exceptions, for example <i>ACT DOMAIN REPEAT</i> 7 (<i>ACR7</i>), <i>ALANINE AMINTRANSFERASE 1</i> (<i>AlaAT1</i>), <i>FCS-LIKE ZINC FINGER PROTEINS with DUF581</i> (<i>FLZ1</i>, <i>FLZ2</i> and <i>FLZ13</i>), <i>AT4G39675</i> (hypothetical protein), <i>PHLOEM PROTEIN 2-A FAMILY</i> (<i>PP2-A11</i> and <i>PP2-A13</i>), and <i>RESPIRATORY BURST OXIDASE HOMOLOGUE D</i> (<i>RBOHD</i>) (<a href="#S10">Supplementary Figure 2</a>). Both genotypes responded in a very similar way, and only one HRG, <i>AT5G10040</i>, was induced by hypoxia in Avatar, but not in Zhongshuang 9 (<a href="#F2">Figure 2</a> and <a href="#S10">Supplementary Figure 2</a>).</p> <div class="DottedLine"></div> <div class="Imageheaders">FIGURE 2</div> <div class="FigureDesc"> <a href="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g002.jpg" name="figure2" target="_blank"> <picture> <source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=480&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g002.jpg" media="(max-width: 563px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=370&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g002.jpg" media="(max-width: 1024px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=290&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g002.jpg" media="(max-width: 1441px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=410&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g002.jpg" media=""><source type="image/jpg" srcset="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g002.jpg" media=""> <img src="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g002.jpg" alt="www.frontiersin.org" id="F2" loading="lazy"> </picture> </a> <p><strong>Figure 2.</strong> Heatmap of hypoxia core-response genes (<a href="#B54">Mustroph et al., 2009</a>) from the <i>Brassica napus</i> expression data. A summary of up to six rapeseed gene IDs for one Arabidopsis gene ID is shown. For expression of all rapeseed genes, please see <a href="#S10">Supplementary Figure 2</a>. Values are signal-log ratios (SLR) of summed counts of root-zone hypoxia vs. aerated control. AV, Avatar; ZS, Zhongshuang 9. The color intensity reflects the SLR values (blue, –3; yellow, + 3). Crossed cells represent values that are not significant (FDR > 0.01).</p> </div> <div class="clear"></div> <div class="DottedLine"></div> <p class="mb15 w100pc float_left mt15">Of the genes highly expressed in hypoxic rapeseed roots, several have a known function under hypoxia, for example primary metabolism and glycolysis (<i>PYRUVATE DECARBOXYLASE</i>, <i>PDC1</i> and <i>PDC3</i>; <i>ALCOHOL DEHYDROGENASE 1</i>, <i>ADH1</i>; <i>AlaAT1</i>; <i>SUCROSE SYNTHASE 1</i>, <i>SUS1</i>; <i>FRUCTOKINASE 2</i>, <i>FRK2</i>; <i>PHOSPHOFRUCTOKINASE</i>, <i>PFK3</i> and <i>PFK6</i>; <i>FRUCTOSE-BISPHOSPHATE ALDOLASE 6</i>, <i>FBA6</i>), or signal transduction (<i>HYPOXIA-RESPONSIVE ERF</i>, <i>HRE1</i> and <i>HRE2</i>; <i>HYPOXIA RESPONSE ATTENUATOR 1</i>, <i>HRA1</i>; <i>LOB DOMAIN CONTAINING PROTEIN 41</i>, <i>LBD41</i>). A few HRGs were not induced by hypoxia in rapeseed, but in Arabidopsis (<i>ATYPICAL CYS HIS RICH THIOREDOXIN</i>, <i>ACHT5</i>; <i>ABSCISIC ACID 8’-HYDROXYLASE</i>, <i>CYP707A3</i>; <i>FAR-RED-ELONGATED HYPOCOTYL1-LIKE PROTEIN</i>, <i>FHL</i>, and a RING/U-box superfamily protein, <i>AT5G42200</i>).</p> <p class="mb0">Interestingly, there was also an overlap of hypoxia-down-regulated genes between Arabidopsis and rapeseed (<a href="#S10">Supplementary Table 2</a>, column P; <a href="#S10">Supplementary Table 4</a>), for example several genes coding for invertase/pectin methylesterase inhibitor superfamily proteins, nodulin MtN21/EamA-like transporter family proteins (<i>UMAMIT12</i>, <i>UMAMIT17</i>), as well as several genes coding for biosynthesis enzymes (e.g., 3-ketoacyl-CoA synthase 20, <i>KCS20</i>; cytochrome P450 family proteins <i>CYP83B1</i>, <i>CYP82F1</i>, <i>CYP79B2</i>; Galactose mutarotase-like superfamily protein).</p> <h3>Transcriptional Changes of Roots in Primary Metabolism, Plant Hormones and Starvation-Responses</h3> <p class="mb15">The functional categorization by use of GO terms (<a href="#S10">Supplementary Table 3</a>) suggested a transcriptional response of several pathways to root-zone hypoxia, including primary metabolism and hormone-associated pathways. This let us to have a deeper look into specific pathways. In primary metabolism, the expression of many genes coding for enzymes in glycolysis and fermentation were up-regulated, including hexokinase, phosphofructokinase and aldolase (<a href="#S10">Supplementary Table 5</a>). For sucrolysis, sucrose-synthase-coding genes were induced, while invertase-like genes were reduced in their expression. Pyruvate dehydrogenase, TCA-cycle enzymes and enzymes for the pentose-phosphate cycle were not modified in expression or even down-regulated. Interestingly, some alternative enzymes were significantly induced in Avatar at the transcript level after 4 h of hypoxia, namely <i>ISOCITRATE LYASE</i> from the glyoxylate cycle, and <i>PYRUVATE ORTHOPHOSPHATE DIKINASE</i> (<i>PPDK</i>) from gluconeogenesis. Among genes coding for nitrogen metabolism, several aminotransferases were induced in both cultivars, for example isoforms for <i>AlaAT1</i> and <i>ASPARTATE AMINOTRANSFERASE 2</i> (<i>AspAT2</i>) (<a href="#S10">Supplementary Table 5</a>).</p> <p class="mb15">Plant hormone biosynthesis and signaling were also among the enriched GO categories within the differentially expressed genes in roots under hypoxia (<a href="#S10">Supplementary Table 3</a>). While auxin biosynthesis was not clearly modified, several polar auxin transporters were negatively affected after 4 h of hypoxia. Despite this, several members of the SAUR-like auxin-responsive protein family were differentially expressed, but with no clear trend (<a href="#S10">Supplementary Table 6</a>). Cytokinin biosynthesis and signaling were in tendency negatively affected by root hypoxia (<a href="#S10">Supplementary Tables 3</a>, <a href="#S10">6</a>), with the exception of the HPt factor gene <i>HPT PHOSPHOTRANSMITTER 4</i> (<i>AHP4</i>), whose expression was strongly induced after 4 and 24 h of hypoxia. In gibberellin metabolism, some genes coding for enzymes involved in biosynthesis and degradation were differentially expressed, but the respective GO terms were not enriched. Signaling related to this group of plant hormones was not affected by hypoxia (<a href="#S10">Supplementary Tables 3</a>, <a href="#S10">6</a>). Brassinosteroid biosynthesis, on the other hand, was negatively regulated by hypoxia.</p> <p class="mb15">Among the stress-related hormones, there was a strong enrichment of genes responding to either ethylene or abscisic acid (<a href="#S10">Supplementary Table 3</a>). However, while neither abscisic acid biosynthesis nor degradation was strongly affected by the stress, genes coding for biosynthetic enzymes in ethylene production were induced upon hypoxia (<i>1-AMINO-CYCLOPROPANE-1-CARBOXYLATE SYNTHASE 2</i> and <i>1-AMINO-CYCLOPROPANE-1-CARBOXYLATE OXIDASE 1</i>, <a href="#S10">Supplementary Table 6</a>). Several genes coding for different steps of jasmonic acid biosynthesis and signal transduction were induced especially after 4 h of root hypoxia, and parts of the salicylic acid signal transduction were induced after 4 and 24 h of hypoxia (<a href="#S10">Supplementary Table 3</a>).</p> <p class="mb0">Previously we have shown that submerged leaves of <i>Brassica napus</i> showed a strong starvation response (<a href="#B73">Wittig et al., 2021</a>). We therefore compared the present dataset to the starvation-responsive genes of Arabidopsis (<a href="#B68">Usadel et al., 2008</a>; <a href="#B15">Cookson et al., 2016</a>). Indeed, there was an enrichment of starvation-induced genes (<a href="#S10">Supplementary Table 4</a>), although less pronounced than under submergence, and affecting different genes. Among starvation-responsive genes in roots under hypoxia, the following transcripts were found: <i>CHY-type/CTCHY-type/RING-type ZINC FINGER PROTEIN</i> (<i>AT5G22920</i>), Eukaryotic aspartyl protease family protein (<i>AT5G19120</i>), <i>GLUTAMINE-DEPENDENT ASPARAGINE SYNTHASE 1</i> (<i>ASN1</i>), and <i>MATERNAL EFFECT EMBRYO ARREST 14</i> (<i>MEE14</i>) (<a href="#S10">Supplementary Table 2</a>, columns R to AD).</p> <h3>Biochemical Modifications in Response to Root-Zone Hypoxia</h3> <p class="mb0">The transcriptional data suggest an induction of transcripts coding for fermentative enzymes (<a href="#S10">Supplementary Table 2</a>, columns R to AD, <a href="#S10">Supplementary Table 3</a>). In order to analyze whether these transcriptional changes translate into an enhanced activity of fermentative enzymes, we measured the activity of ADH after hypoxic treatment in the root zone. After 4 and 24 h we did not observe any significant increase in ADH activity (<a href="#S10">Supplementary Figure 3</a>). However, after 3 days of stress, a strong and significant induction of ADH activity was observed in roots of both cultivars, Avatar and Zhongshuang 9, although no differences were detected between the genotypes (<a href="#F3">Figure 3</a>). This indicates a strong hypoxia response also at the protein level, albeit with a delay in comparison to the transcriptional changes.</p> <div class="DottedLine"></div> <div class="Imageheaders">FIGURE 3</div> <div class="FigureDesc"> <a href="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g003.jpg" name="figure3" target="_blank"> <picture> <source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=480&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g003.jpg" media="(max-width: 563px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=370&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g003.jpg" media="(max-width: 1024px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=290&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g003.jpg" media="(max-width: 1441px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=410&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g003.jpg" media=""><source type="image/jpg" srcset="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g003.jpg" media=""> <img src="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g003.jpg" alt="www.frontiersin.org" id="F3" loading="lazy"> </picture> </a> <p><strong>Figure 3.</strong> ADH activity [nmol * mg prot<sup>–1</sup> * min<sup>–1</sup>] in roots of two <i>Brassica napus</i> cultivars (Avatar, Zhongshuang 9) in hydroponics after 3 days of root hypoxia, compared with aerated controls. At time of harvest, plants were 18 days old. Data are means ± SD of 4 to 5 replicates. Different letters indicate significant differences (ANOVA and Tukey <i>post hoc</i> test, <i>p</i> < 0.05).</p> </div> <div class="clear"></div> <div class="DottedLine"></div> <p class="mb15 w100pc float_left mt15">Several starvation-responsive genes were among the hypoxia-induced genes in roots after 4 and 24 h (<a href="#S10">Supplementary Table 2, columns M and N</a>), but the enrichment was much lower (<a href="#S10">Supplementary Table 4</a>) than in our previous study on complete submergence. Therefore, the carbohydrate content in roots and leaves was measured after both time points. Interestingly, leaf sugar content did not significantly differ between aeration and root hypoxia, and between genotypes (<a href="#F4">Figure 4A</a>). There was a slightly lower level of carbohydrates at the 24-h-time point for stress and control samples, since these plants had only 2 h of light after the 16-h-night, while the plants from the 4-h-time point had 6 h of light.</p> <div class="DottedLine"></div> <div class="Imageheaders">FIGURE 4</div> <div class="FigureDesc"> <a href="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g004.jpg" name="figure4" target="_blank"> <picture> <source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=480&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g004.jpg" media="(max-width: 563px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=370&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g004.jpg" media="(max-width: 1024px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=290&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g004.jpg" media="(max-width: 1441px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=410&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g004.jpg" media=""><source type="image/jpg" srcset="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g004.jpg" media=""> <img src="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g004.jpg" alt="www.frontiersin.org" id="F4" loading="lazy"> </picture> </a> <p><strong>Figure 4.</strong> Content of carbohydrates [μmol * g FW<sup>–1</sup>] in leaves <b>(A)</b> and roots <b>(B)</b> of two <i>Brassica napus</i> cultivars (Avatar, Zhongshuang 9) in hydroponics after 4 and 24 h of root hypoxia, compared with aerated controls. At time of start of stress, plants were 15 days old. Data are means ± SD of 5 replicates. Different letters indicate significant differences for the sum of sugars (ANOVA and Tukey <i>post hoc</i> test, <i>p</i> < 0.05). n.s., ANOVA was not significant; *, significant compared with respective control (<i>T</i>-Test, <i>p</i> < 0.05).</p> </div> <div class="clear"></div> <div class="DottedLine"></div> <p class="mb15 w100pc float_left mt15">In roots, carbohydrate levels, especially starch, were lower than in leaves under both control and stressed conditions (<a href="#F4">Figure 4B</a>). In this case, a tendency of higher sugar contents after stress treatment was observed, which was only significant for sucrose. Again, there was no difference between the genotypes. Sugar starvation due to lower sugar content can therefore be excluded. However, the transcriptomic data still suggest a starvation response (<a href="#S10">Supplementary Table 2</a>, columns M and N). This could be a hint that carbohydrates were not fully available for the plant cells and their metabolism. This assumed lower consumption rate could be an explanation for the observed slight rise in sugar levels in roots.</p> <h3>Comparison to Previous Rapeseed Transcriptome Analyses Under Flooding-Related Stress Treatments</h3> <p class="mb15">Two datasets from roots of <i>Brassica napus</i> plants stressed with waterlogging for 12 h have been published already (<a href="#B78">Zou et al., 2013a</a>,<a href="#B81">2015</a>). In contrast to our study, the plants were grown in pots with sand and treated with waterlogging. Although this dataset is somewhat incomplete due to the missing reference genome at the time of publication, there is a good agreement with our dataset (<a href="#S10">Supplementary Figure 4</a> and <a href="#S10">Supplementary Table 2</a>, columns AZ to BL). About 636 and 234 transcripts were hypoxia-responsive after 4 and 24 h in the present study and were also responsive to 6 and 12 h of waterlogging. The overlap with down-regulated genes was 222 and 89 transcripts for 4 and 24 h of hypoxia. The high number of genes only found in our dataset might be due to the different mapping basis, and probably not due to strong differences in expression (<a href="#S10">Supplementary Figure 4</a> compared with <a href="#S10">Supplementary Figure 5</a>). Indeed, 45 and 42 HRG homologs were also induced by waterlogging of Zhongshuang 9 and GH01, respectively (<a href="#S10">Supplementary Table 2</a>, column Q).</p> <p class="mb0">Another two rapeseed datasets have been obtained from about 2- to 3-day-old seedlings that were fully submerged for 12 or 6 h (<a href="#B24">Guo et al., 2020</a>; <a href="#B41">Li et al., 2021</a>), whose gene expression was based on the reference genome sequence Darmor (<a href="#B13">Chalhoub et al., 2014</a>). Again, there was a good agreement of gene expression data in comparison with the expression data from roots from our dataset, despite of the different developmental stages and treatment conditions (<a href="#S10">Supplementary Table 2</a>, columns BM to BT, <a href="#S10">Supplementary Table 7A</a>). This similarity in gene expression was observed for up- and down-regulated genes and allowed for the definition of a <i>Brassica napus</i> hypoxic core response gene set (BnHRGs) containing 131 commonly up-regulated genes (<a href="#S10">Supplementary Table 7B</a>) and 163 commonly down-regulated genes (<a href="#S10">Supplementary Table 7C</a>).</p> <h3>The Leaf Response Is Less Pronounced If Only Roots Are Affected by Hypoxia</h3> <p class="mb15">In leaves, only a small number of genes was induced by root hypoxia, with little overlap between the two cultivars (<a href="#F1">Figure 1</a>). The most enriched GO terms for Avatar were “2-(2′-methylthio)ethylmalate synthase activity” and “response to insect”, while for Zhongshuang 9 the categories “cation transmembrane transporter activity” (including zinc and iron) and “cellular response to heat” were enriched. Among the down-regulated genes, there was more functional overlap, including the categories “RNA methylation” and further ribosome-related categories as well as “cell wall” (<a href="#S10">Supplementary Table 3</a>).</p> <p class="mb15">In leaves, there was no induction of HRGs (<a href="#S10">Supplementary Figure 2</a> and <a href="#S10">Supplementary Table 4</a>) and no enrichment of GO categories associated with hypoxia (<a href="#S10">Supplementary Table 3</a>). This does not come as a surprise, since the leaves were still in an aerobic atmosphere and with ongoing photosynthesis. The overlap with the starvation response of Arabidopsis (<a href="#B68">Usadel et al., 2008</a>; <a href="#B15">Cookson et al., 2016</a>), as previously observed in submerged rapeseed leaves (<a href="#B73">Wittig et al., 2021</a>), was much lower in this dataset (<a href="#S10">Supplementary Table 4</a>). There was also no indication for a modification of primary metabolism or photosynthesis due to root hypoxia (<a href="#S10">Supplementary Table 5</a>), with the exception of one gene, PAD4, coding for an <i>ALANINE:GLYOXYLATE AMINOTRANSFERASE</i> (<a href="#B58">Parthasarathy et al., 2019</a>), which was induced in leaves of the cultivar Avatar. At the 24-h-time point, there was no clear evidence for a drought response in leaves as a consequence of root damages under the stress (<a href="#S10">Supplementary Table 3</a>). Besides the enhanced expression of the cytokinin signaling component <i>AHP4</i>, no hormone-related transcripts were differentially expressed in leaves of plants with hypoxic roots (<a href="#S10">Supplementary Table 6</a>).</p> <p class="mb0">When we compared the new data to our previous analysis under submergence (<a href="#B73">Wittig et al., 2021</a>), there was hardly any overlap between submerged leaves and leaves from plants with hypoxic roots (<a href="#S10">Supplementary Figure 6</a>). Interestingly, the stressed roots after 24 h shared more induced or reduced transcripts with submerged leaves than the leaves from the two experiments (<a href="#S10">Supplementary Figure 6</a>).</p> <h3>Are There Differences in Gene Expression Between the Two Genotypes?</h3> <p class="mb15">This analysis was done with two genotypes of <i>Brassica napus</i>, one European winter type (Avatar) and one Asian semi-winter type with a previously described high flooding tolerance (Zhongshuang 9, e.g., <a href="#B79">Zou et al., 2013b</a>,<a href="#B80">2014</a>). As mentioned above, the general response of roots to hypoxia was very similar between the two genotypes (<a href="#S10">Supplementary Table 2</a>, columns R to AD, <a href="#S10">Supplementary Table 4</a> and <a href="#F1">Figure 1</a>). There were only small differences at certain time points, and a statistical analysis using a complex comparison revealed no clear signatures (<a href="#S10">Supplementary Table 2</a>, columns AR to AX). Also, the GO analysis of these complex comparisons did only show small differences, for example a stronger reduction of “xylosyltransferase activity” in Avatar (<a href="#S10">Supplementary Table 3</a>). The observed differences might rather be due to differential expression of certain isoforms, while the overall transcript levels of a gene function were rather similar. Indeed, due to genome triplication and its tetraploid status (<a href="#B55">Nikolov and Tsiantis, 2017</a>), rapeseed may contain up to 6 genes for a gene from Arabidopsis.</p> <p class="mb0">However, there were general differences in expression between both genotypes, independent of the stress treatment (<a href="#S10">Supplementary Table 2</a>, columns AE to AQ, <a href="#S10">Supplementary Figure 7</a>). These genotype-specific differences were similar to those observed before for submerged leaves (<a href="#B73">Wittig et al., 2021</a>). In all root samples, about 2,900 transcripts were higher expressed in Avatar, while about 1,000 transcripts were higher in Zhongshuang 9. The difference in numbers might be partially caused by the difference in mapping rates between the two genotypes (<a href="#S10">Supplementary Table 1</a>). A functional analysis classified the differentially expressed genes into certain categories, but there were only a few GOs enriched in our dataset (<a href="#S10">Supplementary Table 3</a>). This suggests that gene copies, but not gene functions are differentially expressed between genotypes. Functional categories with higher expression levels in Avatar were enriched in ribosome function and translation, while in Zhongshuang 9 a few transport categories were enriched. Similar observations were made for leaves.</p> <h3>Is There a Difference in Waterlogging Tolerance Between Both Cultivars?</h3> <p class="mb0">The transcriptional and biochemical analysis did not reveal obvious differences between the two rapeseed cultivars upon treatment with hypoxia in the root zone. We therefore asked whether differences exist in long-term response to hypoxia and waterlogging. First, we used the hydroponics system for a long-term gassing of plants with nitrogen in the root zone. After 7 days of treatment, plants were harvested, and fresh weight was determined (<a href="#F5">Figure 5</a>). The treatment caused growth retardation of the plants, resulting in significantly lowered root and shoot fresh weights. Interestingly, there was also a slight decrease in the ratio of fresh weight to dry weight (<a href="#S10">Supplementary Figure 8A</a>) indicating a slight drought due to root damages under prolonged root hypoxia. However, there were no differences between the two cultivars. Potentially, the treatment duration was too short, but the hydroponic system was not suitable for longer stress treatments. Furthermore, it might not perfectly mimic the situation in soil, or in agriculture.</p> <div class="DottedLine"></div> <div class="Imageheaders">FIGURE 5</div> <div class="FigureDesc"> <a href="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g005.jpg" name="figure5" target="_blank"> <picture> <source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=480&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g005.jpg" media="(max-width: 563px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=370&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g005.jpg" media="(max-width: 1024px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=290&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g005.jpg" media="(max-width: 1441px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=410&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g005.jpg" media=""><source type="image/jpg" srcset="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g005.jpg" media=""> <img src="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g005.jpg" alt="www.frontiersin.org" id="F5" loading="lazy"> </picture> </a> <p><strong>Figure 5.</strong> Fresh weight of shoots <b>(A)</b> and roots <b>(B)</b> of two <i>Brassica napus</i> cultivars (Avatar, Zhongshuang 9) in hydroponics after 7 days of root hypoxia, compared with aerated controls. At time of harvest, plants were 22 days old. Data are means ± SD of 4 experiments with 7-10 plants per experiment (<i>n</i> = 34 – 40). Different letters indicate significant differences (ANOVA and Tukey <i>post hoc</i> test, <i>p</i> < 0.05).</p> </div> <div class="clear"></div> <div class="DottedLine"></div> <p class="mb15 w100pc float_left mt15">Therefore, a more natural system was used, rapeseed plants grown on soil. After 15 days of growth on normoxic soil, plants were treated with waterlogging in the root zone. This treatment was done for 14 days. To evaluate fitness at an early timepoint in a non-invasive manner, a chlorophyll fluorescence parameter, the effective quantum yield of PSII (ΦPSII), was determined. This value slightly increased after 6 days of waterlogging in both genotypes (<a href="#F6">Figure 6B</a>). Overall, the ΦPSII values for Zhongshuang 9 were slightly smaller than the values for Avatar, but the trend between control and stress treatment was the same. After 14 days of stress, the differences in ΦPSII between control and stress were no longer significant. The fresh weight in this experimental set-up significantly decreased under waterlogging, as shown in the hydroponic system (<a href="#F6">Figure 6A</a>), but the changes were not as severe as expected. Again, no differences between the genotypes were found.</p> <div class="DottedLine"></div> <div class="Imageheaders">FIGURE 6</div> <div class="FigureDesc"> <a href="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g006.jpg" name="figure6" target="_blank"> <picture> <source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=480&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g006.jpg" media="(max-width: 563px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=370&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g006.jpg" media="(max-width: 1024px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=290&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g006.jpg" media="(max-width: 1441px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=410&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g006.jpg" media=""><source type="image/jpg" srcset="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g006.jpg" media=""> <img src="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g006.jpg" alt="www.frontiersin.org" id="F6" loading="lazy"> </picture> </a> <p><strong>Figure 6.</strong> Performance of two <i>Brassica napus</i> cultivars (Avatar, Zhongshuang 9) on soil under waterlogging with tap water (“WL”) for up to 14 days. At time of harvest, plants were 29 days old. <b>(A)</b> Fresh weight of shoots after 14 days of stress treatment compared with controls. Data are means ± SD of 3 experiments with 10 plants per experiment (n = 30). <b>(B)</b> chlorophyll fluorescence (ΦPSII) after 6 and 14 days of stress treatment compared with controls. Data are means ± SD of 3 experiments with 10 plants per experiment (<i>n</i> = 30). <b>(C)</b> Content of carbohydrates [μmol * g FW<sup>–1</sup>] in leaves of after 14 days of stress. Data are means ± SD of 2 experiments with 6 plants per experiment (<i>n</i> = 12). <b>(D)</b> Chlorophyll content [mg * g FW<sup>–1</sup>] in leaves of after 14 days of stress. Data are means ± SD of 2 experiments with 8 plants per experiment (n = 16). Different letters indicate significant differences (ANOVA and Tukey <i>post hoc</i> test, <i>p</i> < 0.05). n.s., not significant.</p> </div> <div class="clear"></div> <div class="DottedLine"></div> <p class="mb15 w100pc float_left mt15">Two additional parameters were analyzed in this system, in order to reveal any effect of the modified stress system on the plant carbohydrate and pigment system. As shown for the short-term hydroponics system (<a href="#F4">Figure 4</a>), the carbohydrate content of leaves from plants under waterlogging in soil did not respond to the stress treatment, even after 14 days of stress (<a href="#F6">Figure 6C</a>). The chlorophyll content showed a tendency to decrease after stress treatment, but no significant differences between the two genotypes were observed (<a href="#F6">Figure 6D</a>). These results suggest that waterlogging on soil in a controlled growth chamber might not be as severe as natural waterlogging in agriculture.</p> <p class="mb0">In order to establish a more natural system, we came across a waterlogging system with a starch solution that may cause a lower soil redox potential for plants grown in pots in climate chambers, which was successfully used for barley (<a href="#B44">Mano and Takeda, 2012</a>; <a href="#B46">Miricescu et al., 2021</a>). Strikingly, the waterlogging with a 0.1% starch solution strongly enhanced the severity of the stress treatment in comparison to waterlogging in distilled water (<a href="#F7">Figure 7</a> and <a href="#S10">Supplementary Figure 9</a>) or in tap water (<a href="#F6">Figure 6</a>). Here, the fresh weight of aboveground organs of stressed plants was reduced to 30% of the control plants, while in distilled water it was only reduced to 90% (<a href="#F7">Figure 7A</a>), and in tap water to about 70% (<a href="#F6">Figure 6A</a>). There were also indications for a stronger drought stress when waterlogging was done in starch solution since the ratio of fresh weight to dry weight was severely reduced (<a href="#S10">Supplementary Figure 8B</a>). The analysis of chlorophyll fluorescence (ΦPSII) showed little changes after 7 days of stress, but a significant decrease after 14 days of waterlogging in a starch solution (<a href="#F7">Figure 7C</a>). For chlorophyll, estimated here with a non-invasive method, we did not observe clear differences after 14 days of stress (<a href="#F7">Figure 7D</a>).</p> <div class="DottedLine"></div> <div class="Imageheaders">FIGURE 7</div> <div class="FigureDesc"> <a href="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g007.jpg" name="figure7" target="_blank"> <picture> <source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=480&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g007.jpg" media="(max-width: 563px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=370&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g007.jpg" media="(max-width: 1024px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=290&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g007.jpg" media="(max-width: 1441px)"><source type="image/webp" srcset="https://images-provider.frontiersin.org/api/ipx/w=410&f=webp/https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g007.jpg" media=""><source type="image/jpg" srcset="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g007.jpg" media=""> <img src="https://www.frontiersin.org/files/Articles/897673/fpls-13-897673-HTML/image_m/fpls-13-897673-g007.jpg" alt="www.frontiersin.org" id="F7" loading="lazy"> </picture> </a> <p><strong>Figure 7.</strong> Performance of two <i>Brassica napus</i> cultivars (Avatar, Zhongshuang 9) on soil under waterlogging with a 0.1% starch solution (“starch”) or with distilled water (“WL”) for up to 14 days. At time of harvest, plants were 29 days old. <b>(A)</b> Fresh weight of shoots after 14 days of stress treatment compared with controls. <b>(B)</b> Chlorophyll fluorescence (ΦPSII) after 7 and 14 days of stress treatment compared with controls. <b>(C)</b> Chlorophyll content [μmol * m<sup>–2</sup>] in leaves of after 7 and 14 days of stress. Data are means ± SD of 3 experiments with 6 plants per experiment (<i>n</i> = 18). Different letters indicate significant differences (ANOVA and Tukey <i>post hoc</i> test, <i>p</i> < 0.05).</p> </div> <div class="clear"></div> <div class="DottedLine"></div> <p class="mb15 w100pc float_left mt15">In order to determine the causal reasons for these strong differences in plant growth, we also obtained chemical parameters of the waterlogging solutions in the two variants. While waterlogging with distilled water only resulted in mild decreases in oxygen content, starting at day 9, the oxygen content strongly decreased within the first 24 h of waterlogging in the starch solution, and remained at this low level for at least 10 days (<a href="#S10">Supplementary Figure 10A</a>). Subsequently, the oxidation-reduction potential (ORP) decreased after 2 and 3 days of waterlogging with starch solution, but it remained relatively high in distilled water (<a href="#S10">Supplementary Figure 10B</a>). The increase in both oxygen and ORP after 10 days of waterlogging might suggest a partial recovery of the system due to exhaustion of starch. The pH value temporarily decreased in the waterlogging treatment with starch (<a href="#S10">Supplementary Figure 10C</a>), while the conductivity increased with time in both variants, with a slightly stronger increase in starch solution (<a href="#S10">Supplementary Figure 10D</a>). The latter could be due to enhanced root death and subsequent release of ions into the solution.</p> <a id="h5" name="h5"></a><h2>Discussion</h2> <h3 class="pt0"><i>Brassica napus</i> Roots Strongly Respond to Hypoxia</h3> <p class="mb15">The oil crop plant <i>Brassica napus</i> is described to be very sensitive to soil waterlogging (<a href="#B80">Zou et al., 2014</a>). It is not able to form aerenchyma in its roots as part of an avoidance strategy (<a href="#B70">Voesenek et al., 1999</a>; <a href="#B60">Ploschuk et al., 2018</a>), and will therefore experience hypoxia inside root tissues under waterlogging. We were therefore interested in its transcriptional response to this aspect of waterlogging stress to estimate whether rapeseed was able to induce biochemical acclimations as part of the tolerance strategy. After 4 and 24 h of root hypoxia, a high number of genes was differentially expressed in both cultivars compared to aerated controls (<a href="#S10">Supplementary Table 2</a>, columns R to AD and <a href="#F1">Figure 1</a>). More transcripts were down-regulated than up-regulated.</p> <p class="mb15">The functional analysis of up-regulated genes revealed the induction of a strong hypoxia response, as indicated by the enrichment of hypoxia-associated GO terms (<a href="#S10">Supplementary Table 3</a>). Furthermore, there was a significant overlap with hypoxia-induced genes in Arabidopsis in general as well as with the hypoxia core response genes (HRGs, <a href="#B54">Mustroph et al., 2009</a>; <a href="#F2">Figure 2</a> and <a href="#S10">Supplementary Figure 2</a>, <a href="#S10">Supplementary Table 4</a>). Among the hypoxia-induced genes were transcripts coding for fermentative enzymes (<i>ADH1</i>, <i>PDC1</i>, <i>PDC3</i>), glycolytic enzymes (<i>SUS1</i>, <i>FRK2</i>, <i>PFK3</i>, <i>PFK6</i>, <i>FBA6</i>) as well as transcriptional regulators (<i>HRE1</i>, <i>HRE2</i>, <i>HRA1</i>, <i>LBD41</i>). Both plant species are rather sensitive to waterlogging stress, and it remains to be evaluated whether differences in tolerance exist between the two species.</p> <p class="mb15">Glycolysis and fermentation are important processes to maintain energy balance under hypoxia since mitochondrial respiration is strongly inhibited. Their induction is therefore an essential component of the tolerance to low-oxygen stress. As Arabidopsis, also rapeseed was able to induce the expression of the associated genes under root hypoxia (<a href="#S10">Supplementary Table 2</a>, columns R to AD), which may also result in higher enzyme activities as shown here for the ADH activity during prolonged stress treatment (<a href="#F3">Figure 3</a>), and therefore might hint at an acclimation response of rapeseed plants. Mutants with a defect in fermentative enzymes indeed showed a lower tolerance to flooding-related stresses, for example in rice (<a href="#B63">Saika et al., 2006</a>; <a href="#B66">Takahashi et al., 2014</a>), maize (<a href="#B65">Schwartz, 1969</a>; <a href="#B30">Johnson et al., 1994</a>) or Arabidopsis (<a href="#B29">Jacobs et al., 1988</a>; <a href="#B28">Ismond et al., 2003</a>). Interestingly, the proposed enhancement of glycolysis and fermentation does not cause a carbohydrate limitation in our system (<a href="#F4">Figure 4</a>), most likely due to ongoing photosynthesis in the leaves.</p> <p class="mb15">In addition, many plant species induced enzymes with alternative energy requirements upon hypoxia treatment, mainly sucrose synthase, the pyrophosphate-dependent phosphofructokinases (PFP) as well as PPDK (<a href="#B27">Huang et al., 2008</a>; <a href="#B51">Mustroph et al., 2014</a>, <a href="#B53">2018</a>; <a href="#B4">Atwell et al., 2015</a>). Interestingly and unlike Arabidopsis (<a href="#B54">Mustroph et al., 2009</a>), rapeseed induced two genes coding for the PFP alpha subunit in hypoxic roots, and this induction was stronger after 4 than after 24 h. This might be a hint for an alternative energy usage in <i>Brassica napus</i>. Several transcripts coding for PPDK and SUS are also among the hypoxia-induced genes in rapeseed (<a href="#S10">Supplementary Table 2</a>, columns R to AD, <a href="#S10">Supplementary Table 5</a>).</p> <p class="mb15">Among transcriptional regulators, the function of LBD41 is still unclear, but it is commonly induced by hypoxia in many plant species (<a href="#B52">Mustroph et al., 2010</a>; <a href="#B18">Gasch et al., 2016</a>). HRE1 and HRE2 are members of the group VII ERFs, which are important regulators of the hypoxia-specific transcription (<a href="#B21">Gibbs et al., 2011</a>; <a href="#B42">Licausi et al., 2011</a>). Both proteins are probably not involved in the initial response to hypoxia (<a href="#B18">Gasch et al., 2016</a>), but most likely in the later stages of hypoxia (<a href="#B43">Licausi et al., 2010</a>). HRA1 has been described as a negative regulator of hypoxia-specific transcription (<a href="#B22">Giuntoli et al., 2014</a>, <a href="#B23">2017</a>). The transcriptional regulation of the hypoxic response in rapeseed might therefore be very similar to Arabidopsis.</p> <p class="mb15">Among the genes with reduced expression under hypoxia there are many whose products are involved in biosynthetic processes such as sterol, xylan and suberin biosynthesis, and in growth-related GO terms such as DNA replication, cell wall and cell proliferation (<a href="#S10">Supplementary Table 3</a>). This is not surprising since it has been previously suggested that the hypoxia acclimation strategy includes down-regulation of growth and biosynthesis in Arabidopsis (<a href="#B10">Branco-Price et al., 2008</a>; <a href="#B54">Mustroph et al., 2009</a>). In accordance, growth of rapeseed plants is reduced under root hypoxia (<a href="#F5">Figure 5</a>). Moreover, the low-oxygen quiescence strategy is a response of certain rice cultivars that show enhanced survival under relatively deep floods (<a href="#B76">Xu et al., 2006</a>; <a href="#B17">Fukao and Bailey-Serres, 2008</a>). Therefore, growth reduction of rapeseed plants could be a positive acclimation strategy under waterlogging (this work) as well as under submergence (<a href="#B73">Wittig et al., 2021</a>).</p> <p class="mb15">Whether the down-regulation of growth and biosynthesis is an active process in <i>Brassica napus</i> remains to be elucidated. However, the fast down-regulation of many growth-related genes might suggest a controlled response. It is unlikely that the growth regulation is caused by sugar starvation since there is no indication for a carbohydrate starvation in rapeseed plants under root-zone hypoxia, and sugar content is rather higher than lower under stress (<a href="#F4">Figure 4</a>). This phenomenon has been previously observed in waterlogged plants of many species, for example in wheat and maize (e.g., <a href="#B26">Huang and Johnson, 1995</a>; <a href="#B49">Mustroph and Albrecht, 2003</a>; <a href="#B1">Albrecht et al., 2004</a>), tomato (<a href="#B20">Gharbi et al., 2009</a>), potato (<a href="#B7">Biemelt et al., 1999</a>), and rapeseed (<a href="#B40">Leul and Zhou, 1999</a>). It might either be explained by a higher transport rate from the shoot, a reduced growth rate of roots, a limited sugar usage capacity in root cells, or a controlled down-regulation of root metabolism (<a href="#B19">Geigenberger et al., 2000</a>; <a href="#B1">Albrecht et al., 2004</a>; <a href="#B20">Gharbi et al., 2009</a>).</p> <p class="mb15">The underlying factors for the observed growth reduction, however, are not known yet. Hormones known to play a role under flooding-related stresses are abscisic acid (ABA) and gibberellic acid (GA) (summarized in <a href="#B5">Bailey-Serres et al., 2012</a>; <a href="#B69">Voesenek and Bailey-Serres, 2015</a>). The GA-sensing DELLA proteins, who are responsible for growth reduction in rice under submergence (<a href="#B17">Fukao and Bailey-Serres, 2008</a>), are not modified in their expression in rapeseed (<a href="#S10">Supplementary Table 2</a>, columns R to AD; <a href="#S10">Supplementary Table 6</a>). However, a transcript coding for the GA degradation enzyme <i>GIBBERELLIN 2-OXIDASE 3</i> (<i>GA2OX3</i>, <a href="#B61">Rieu et al., 2008</a>) is strongly induced in hypoxic rapeseed roots (<i>BnaA05g09290D</i>), which might play a role in reduction of growth in this species, while its homolog <i>GA2OX2</i> is seldomly induced by hypoxia in Arabidopsis (<a href="#B52">Mustroph et al., 2010</a>). An involvement of the stress hormone ABA in growth reduction is also possible since several genes coding for the biosynthesis enzyme 9-cis-epoxycarotenoid dioxygenase (<i>NCED</i>) are reduced in their expression (<a href="#S10">Supplementary Table 2</a>, columns R to AD; <a href="#S10">Table 6</a>). However, the HRG from Arabidopsis, <i>CYP707A3</i>, which is involved in the degradation of ABA (<a href="#B56">Okamoto et al., 2011</a>), is not induced by hypoxia in rapeseed roots (<a href="#F2">Figure 2</a>). In addition, other hormone pathways are differentially expressed and might be involved in the growth reduction, for example brassinosteroids, whose biosynthesis enzymes are strongly reduced in hypoxic roots (<a href="#S10">Supplementary Table 6</a>).</p> <p class="mb15">The transcriptional response in this work was compared to other published data of rapeseed as well as to Arabidopsis. In two publications, young rapeseed seedlings (about 3 days old) were subjected to full submergence (<a href="#B24">Guo et al., 2020</a>; <a href="#B41">Li et al., 2021</a>). Despite the different systems, there was a substantial and significant overlap between the different treatments and developmental stages (<a href="#S10">Supplementary Table 2</a>, columns BM to BT, <a href="#S10">Supplementary Table 7A</a>). Many HRGs were among the induced genes under diverse flooding-related conditions. The direct comparison of our and earlier studies allowed us to define a set of hypoxia core response genes for <i>Brassica napus</i> (BnHRGs, <a href="#S10">Supplementary Tables 7B,C</a>). 131 up-regulated and 163 down-regulated genes were in this dataset. While a large number of the up-regulated genes was also among HRGs in Arabidopsis (27), or was also hypoxia-responsive in Arabidopsis (90), a few genes seemed to be specific for rapeseed (14). Surprisingly, we found two transcription factors that are not yet described as HRGs in Arabidopsis, and that are rather linked to ABA, drought or wounding, namely <i>ETHYLENE RESPONSE FACTOR #111</i> (<i>ERF#111</i>, <i>ABR1</i>) and <i>DEHYDRATION-RESPONSIVE ELEMENT BINDING PROTEIN 2C</i> (<i>DREB2C</i>) (e.g., <a href="#B36">Lee et al., 2010</a>; <a href="#B31">Kim et al., 2011</a>; <a href="#B6">Bäumler et al., 2019</a>). The importance of these transcription factors under waterlogging and hypoxia in rapeseed remains to be elucidated.</p> <p class="mb15">Comparing our expression data to the expression of Arabidopsis under hypoxia (e.g., <a href="#B10">Branco-Price et al., 2008</a>; <a href="#B54">Mustroph et al., 2009</a>, <a href="#B52">2010</a> and references therein; <a href="#B25">Hsu et al., 2011</a>) revealed a strong overlap (<a href="#S10">Supplementary Table 4</a>). This included many, but not all HRGs. For example, the genes coding for <i>ACHT5</i>, <i>CYP707A3</i>, and <i>FHL</i> were not induced by hypoxia in <i>Brassica napus</i>. On the other hand, several genes were strongly induced in rapeseed by hypoxia, but not in Arabidopsis, for example <i>PEPTIDEMETHIONINE SULFOXIDE REDUCTASE 3</i> (<i>PMSR3</i>), ATP-dependent Clp protease (<i>AT1G33360</i>), <i>EXPANSIN-LIKE B1</i> (<i>EXLB1</i>), and two genes involved in hormone pathways already mentioned above (<i>AHP4</i>, <i>GA2OX3</i>). The function of these proteins in the context of hypoxic acclimation of rapeseed remains to be examined. A possible function of <i>PMSR3</i> could be the protection of proteins against oxidation of methionine residues (<a href="#B62">Sadanandom et al., 2000</a>), but its induction in rapeseed seems to be only temporary.</p> <p class="mb15">There was also some overlap with genes commonly reduced by hypoxia in Arabidopsis. Although a previous work could not define a general set of down-regulated HRGs, there were seven genes that displayed a common root-specific down-regulation under hypoxia (<a href="#B54">Mustroph et al., 2009</a>). Of those seven genes, three were also commonly reduced in hypoxic rapeseed roots, namely <i>CYP83B1</i>, <i>MYB DOMAIN PROTEIN 34</i> (<i>MYB34</i>) and <i>SLAC1 HOMOLOG 3</i> (<i>SLAH3</i>). The first two gene products are involved in tryptophan biosynthesis and its regulation, and thereby might affect glucosinolate biosynthesis (<a href="#B12">Celenza et al., 2005</a>). Their common down-regulation supports our hypothesis that biosynthetic processes are mainly reduced under hypoxic conditions. The third gene codes for an anion channel, which recently has been described to be involved in depolarization of membranes due to cytoplasmic acidosis, for example caused by flooding and hypoxia (<a href="#B39">Lehmann et al., 2021</a>). Indeed, Arabidopsis plants with a defect in <i>SLAH3</i> were more resistant to full submergence in darkness, and the down-regulation of its expression in Arabidopsis as well as rapeseed might be an advantage for survival.</p> <p class="mb0">Our experiments allow the conclusion that rapeseed roots can strongly respond to hypoxia in a coordinated way, and that this response is similar, but not identical to the response of Arabidopsis. Knowledge from the model plant <i>Arabidopsis thaliana</i>, for example about the transcriptional regulation of the hypoxia response and mechanisms of metabolic acclimation, might therefore be reasonably transferrable to the crop <i>Brassica napus</i>, in order to improve its tolerance against flooding. However, rapeseed has a much higher gene number due to whole-genome triplication and the tetraploid status (<a href="#B55">Nikolov and Tsiantis, 2017</a>), making it a difficult species for genetic analyses. Indeed, most Arabidopsis genes have 2 to 8 isogenes in <i>Brassica napus</i>, which is also true for many HRGs. Most, but not all isogenes for one Arabidopsis HRG are regulated in a similar way in rapeseed (<a href="#S10">Supplementary Table 2</a>, column Q; <a href="#S10">Supplementary Figure 2</a>). It remains to be determined how the differential expression among isogenes is regulated, and whether previously defined promoter elements such as the HRPE (<a href="#B18">Gasch et al., 2016</a>) are mutated or modified in some isogenes.</p> <h3><i>Brassica napus</i> Leaves Show Only a Minor Response to Root Hypoxia</h3> <p class="mb15">Previously we have identified a set of genes that is strongly induced under submergence in leaves of two <i>Brassica napus</i> cultivars (<a href="#B73">Wittig et al., 2021</a>). This analysis revealed a signature for carbohydrate starvation, which was in line with a severe decline in carbohydrate levels under water within a few hours, but hardly any induction of hypoxia-responsive genes. In the present work, leaves of <i>Brassica napus</i> plants with root hypoxia showed little changes in gene expression (<a href="#S10">Supplementary Table 2</a>, columns R to AD) indicating that the shoot was not yet affected by the stress of the root system, including the carbohydrate levels (<a href="#F4">Figure 4</a>). Previous analyses, however, have observed different responses in shoots of plants under root hypoxia or waterlogging. In Arabidopsis (<a href="#B25">Hsu et al., 2011</a>) and cotton (<a href="#B14">Christianson et al., 2010</a>), many transcripts in the shoot responded to the root stress after 12 and 24 h, respectively. An analysis of rapeseed under root waterlogging also revealed massive transcriptional changes in leaves after 36 and 72 h of stress (<a href="#B38">Lee et al., 2014</a>). Only in poplar, a waterlogging treatment did not result in significant expression differences in leaves, as determined after 7 days of stress (<a href="#B32">Kreuzwieser et al., 2009</a>). Possible explanations for such a small response in our system could be that (1) the timepoint was too early to observe transcriptional changes, (2) the stress treatment was not severe enough to induce changes in the shoot system, or (3) changes occurred mainly in other parts of the shoots, for example the meristem or the stem. Indeed, the work on Arabidopsis harvested whole shoots (<a href="#B25">Hsu et al., 2011</a>), and this was also the case for the previous work on rapeseed (<a href="#B38">Lee et al., 2014</a>).</p> <p class="mb15">Surprisingly, the low number of transcripts in leaves responding to root hypoxia are hardly related to any specific GO term, and almost no modifications were observed for photosynthesis-related genes, as it has been previously observed (<a href="#B38">Lee et al., 2014</a>). Also, no modification of ROS metabolism and no induction of ABA biosynthesis genes that might indicate problems with water uptake were observed in our experiment. This is in accordance with the small changes within the physiological data, i.e., the sugar content in leaves (<a href="#F4">Figure 4</a>), and no symptoms of wilting. Only after 7 days of stress treatment, the fresh weight in the hydroponic system was negatively affected (<a href="#F5">Figure 5</a>), and a slightly lower water content was observed (<a href="#S10">Supplementary Figure 8A</a>).</p> <p class="mb15">After longer durations of the stress in the soil waterlogging system, a decrease in chlorophyll content was detected, but only with the invasive method (Figjure 6D). Decreases in chlorophyll content in rapeseed under root waterlogging have been found before (<a href="#B3">Ashraf and Mehmood, 1990</a>; <a href="#B40">Leul and Zhou, 1999</a>; <a href="#B38">Lee et al., 2014</a>), but they were more pronounced in the recovery phase. Surprisingly, the photosynthetic efficiency around PSII was only marginally affected under root waterlogging, as measured in the soil system (<a href="#F6">Figures 6B</a>, 7C). These results suggest that photosynthesis was only mildly affected in our stress treatment, thus explaining little changes in gene expression or sugar status (<a href="#S10">Supplementary Table 2</a> and <a href="#F4">Figure 4</a>). Therefore, a later timepoint might reveal more changes in gene expression in shoots, and potentially also a more severe treatment variant (<a href="#F7">Figure 7</a>).</p> <p class="mb0">A common response of leaves in both genotypes was observed among down-regulated genes. Here, many genes associated with ribosomes and translation were lower expressed in leaves when roots were treated with hypoxia (<a href="#S10">Supplementary Table 3</a>). This is a hint that there is indeed some regulation of gene expression in leaves of plants with roots under stress. The down-regulation of ribosomal proteins suggests a down-regulation of translation in general, as it has been observed before for Arabidopsis seedlings (<a href="#B10">Branco-Price et al., 2008</a>; <a href="#B54">Mustroph et al., 2009</a>). The signal that transmits the root stress to the shoots is, however, still unclear and remains to be solved.</p> <h3>No Difference in the Response to Hypoxia and Waterlogging Between the Two Cultivars</h3> <p class="mb15">One goal of this experimental set-up was to identify potential differences between two rapeseed cultivars, of which one had been described as tolerant toward waterlogging (e.g., <a href="#B79">Zou et al., 2013b</a>,<a href="#B80">2014</a>). However, in none of our experimental set-ups, root-zone hypoxia in hydroponics (<a href="#F3">Figures 3-5</a>), waterlogging on soil (<a href="#F6">Figure 6</a>), and waterlogging with a starch solution (<a href="#F7">Figure 7</a>), we observed significant differences between the cultivars. Also, the gene expression analysis did not reveal clear differences in stress response between the genotypes (<a href="#S10">Supplementary Table 2</a>, columns AR to AX). This might lead to the conclusion that the cultivars do not differ in their tolerance to waterlogging and root hypoxia, as previously demonstrated for treatment with submergence using the same two cultivars (<a href="#B73">Wittig et al., 2021</a>). However, we cannot exclude a difference in tolerance at other developmental stages, in the recovery phase, or in field trials. It is also important to note that other rapeseed cultivars with contrasting response to waterlogging might exist. Furthermore, we have not evaluated whether differences in the genomic sequence of hypoxia-regulated genes exist between Avatar and Zhongshuang 9, and whether such differences might modify waterlogging and hypoxia tolerance. Indeed, certain single nucleotide polymorphisms (SNPs) that might be associated with submergence tolerance have been detected in a panel of rapeseed cultivars (<a href="#B71">Wang et al., 2020</a>), but genome-wide association studies under waterlogging are still missing.</p> <p class="mb15">There are overall differences in gene expression between genotypes (<a href="#S10">Supplementary Figure 7</a> and <a href="#S10">Supplementary Table 2</a>, columns AE to AQ), but they were seldomly related with a specific gene function (<a href="#S10">Supplementary Table 3</a>). Ribosomal proteins are generally more expressed in Avatar than in Zhongshuang 9, and especially leaves show a slight enrichment of photosynthesis-associated genes, which might correlate with a slightly higher chlorophyll content (<a href="#F6">Figure 6D</a>). Zhongshuang 9 showed even less functional categories with differential expression, which could be also due to a slightly lower mapping rate in comparison to the cultivar Avatar (<a href="#S10">Supplementary Table 1</a>).</p> <p class="mb15">Previous analyses have suggested that Zhongshuang 9 is more tolerant to waterlogging than GH01 due to expression differences for several genes (<a href="#B78">Zou et al., 2013a</a>,<a href="#B81">2015</a>). However, the overall expression changes in response to the stress treatment in both cultivars were surprisingly similar (<a href="#S10">Supplementary Table 2</a>, columns AZ to BL). In order to evaluate the previously observed expression differences, we extracted the respective <i>Brassica napus</i> gene IDs and looked for differential expression between our genotypes in the current genome assembly. However, none of the suggested candidates was differentially expressed between genotypes in our dataset (<a href="#S10">Supplementary Table 8A</a>). Moreover, our overview reveals multiple genes coding for one gene function, and the sum over all transcripts might be more similar than single gene copies suggest, for example the nine transcripts coding for glyceraldehyde-3-phosphate dehydrogenase C subunit 1 (<i>GAPC1</i>, <a href="#S10">Supplementary Table 8A</a>). In addition, a recent quantitative trait locus (QTL) analysis of the same two genotypes suggested another set of genes to be differentially expressed (<a href="#B16">Ding et al., 2020</a>). However, there was no overlap of gene IDs between the two studies (<a href="#B81">Zou et al., 2015</a>; <a href="#B16">Ding et al., 2020</a>), and we could observe similar transcriptional changes for only a few transcripts in Zhongshuang 9 (<a href="#S10">Supplementary Table 8B</a>). This suggests that (1) the candidate genes from both studies are not differentially expressed at all developmental stages or stress variants, (2) other genes might be responsible for the QTLs defined in <a href="#B16">Ding et al. (2020)</a>, or (3) the genotype Avatar does not differ as much from Zhongshuang 9 as GH01. In fact, most differences between the cultivars might occur only at the recovery phase after stress, as it has been recently demonstrated (<a href="#B33">Kuai et al., 2020a</a>,<a href="#B34">b</a>). Interestingly, the impact of nitrogen fertilizer on growth after flooding was as high or even higher than the impact of the genotype in these two publications.</p> <p class="mb0">More work is therefore needed, with the inclusion of more and diverse genotypes, in order to find and develop flooding-tolerant rapeseed genotypes. One improvement to previous waterlogging treatments could be the addition of 0.1% starch to the solution. The addition of starch strongly decreased the oxygen content and increased the reduction potential (<a href="#S10">Supplementary Figure 10</a>), and therefore resembles more natural conditions than waterlogging with pure water, as previously demonstrated in barley (<a href="#B44">Mano and Takeda, 2012</a>; <a href="#B46">Miricescu et al., 2021</a>). In our hands, the stress treatment with a starch solution was more severe compared with waterlogging with tap water (<a href="#F7">Figure 7</a> and <a href="#S10">Supplementary Figure 9</a>), and subsequent screening methods should consider this modified type of waterlogging stress, together with the addition of a recovery phase.</p> <a id="h6" name="h6"></a><h2>Conclusion</h2> <p class="mb0">This work demonstrates that rapeseed is indeed able to strongly respond to waterlogging-associated hypoxia in the root zone at the transcriptional level. These responses might indicate an acclimation response to the stress, but they could also include responses to stress damage. A core hypoxia response for rapeseed plants could be defined, which can be used for future studies. However, a genotype-specific response to hypoxia and waterlogging between cultivars from different origin (Europe and Asia) could not be detected. However, we cannot exclude that SNPs related to tolerance are more important than overall transcriptional levels. In future, differences in gene sequences should be analyzed as well, for example by using a genome-wide association mapping approach, potentially together with QTL analyses. So far, only very few studies on rapeseed under flooding stress contain sufficient data for such an approach (<a href="#B16">Ding et al., 2020</a>; <a href="#B71">Wang et al., 2020</a>), and more work is required in this direction. The present dataset and a modified waterlogging treatment of plants grown in pots by use of a starch solution might help to identify potential tolerance-related genes in certain QTL regions, which ultimately could result in waterlogging-tolerant rapeseed genotypes.</p> <a id="h7" name="h7"></a><h2>Data Availability Statement</h2> <p class="mb0">The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: National Center for Biotechnology Information (NCBI) BioProject database under accession number GSE180262.</p> <a id="h8" name="h8"></a><h2>Author Contributions</h2> <p class="mb0">AM designed the experiments, analyzed the data and wrote the manuscripts. BB developed the methods. SA, MK, PW, and AM performed the experiments. All authors contributed to the article and approved the submitted version.</p> <a id="fun1" name="fun1"></a><h2>Funding</h2> <p class="mb0">This study was supported by the Bavarian State Ministry of the Environment and Consumer Protection, project network BayKlimaFit [grant number TGC01GCUFuE69742]. This study was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) [491183248] and by the Open Access Publishing Fund of the University of Bayreuth.</p> <a id="conf1" name="conf1"></a><h2>Conflict of Interest</h2> <p class="mb0">The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p> <a id="disclaimer1" name="disclaimer1"></a><h2>Publisher’s Note</h2> <p class="mb0">All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.</p> <a id="ack1" name="ack1"></a><h2>Acknowledgments</h2> <p class="mb0">We thank Alois Aigner and Xi-Ling Zou for providing <i>Brassica napus</i> seeds. Maria Klecker is acknowledged for critical reading of the manuscript, and the students Verena Geiger and Jonas Freiberg are acknowledged for help with the experiments.</p> <a id="S10" name="S10"></a><h2>Supplementary Material</h2> <p class="mb0">The Supplementary Material for this article can be found online at: <a href="https://www.frontiersin.org/articles/10.3389/fpls.2022.897673/full#supplementary-material">https://www.frontiersin.org/articles/10.3389/fpls.2022.897673/full#supplementary-material</a></p> <a id="abbr1" name="abbr1"></a><h2>Abbreviations</h2> <p class="mb0">ADH, alcohol dehydrogenase; ERF, ethylene response factor; FDR, false discovery rate; GO, gene ontology; HRG, hypoxia core-response gene; PDC, pyruvate decarboxylase; SNP, single nucleotide polymorphism; QTL, quantitative trail locus.</p> <a id="refer1" name="refer1"></a><h2>References</h2> <div class="References" style="margin-bottom:0.5em;"> <p class="ReferencesCopy1"><a name="B1" id="B1"></a>Albrecht, G., Mustroph, A., and Fox, T. 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Plant Sci.</i> 13:897673. doi: 10.3389/fpls.2022.897673</p> <p id="timestamps"> <span>Received:</span> 16 March 2022; <span>Accepted:</span> 11 April 2022;<br><span>Published:</span> 29 April 2022.</p> <div> <p>Edited by:</p> <a href="https://loop.frontiersin.org/people/698294/overview">Silvia Pampana</a>, University of Pisa, Italy</div> <div> <p>Reviewed by:</p> <a href="https://loop.frontiersin.org/people/357256/overview">David Jespersen</a>, University of Georgia, United States<br> <a href="https://loop.frontiersin.org/people/811663/overview">Muhammad Farooq</a>, University of Teramo, Italy<br> <a href="https://loop.frontiersin.org/people/140716/overview">Arun K. Shanker</a>, Central Research Institute for Dryland Agriculture (ICAR), India</div> <p><span>Copyright</span> © 2022 Ambros, Kotewitsch, Wittig, Bammer and Mustroph. This is an open-access article distributed under the terms of the <a rel="license" href="http://creativecommons.org/licenses/by/4.0/" target="_blank">Creative Commons Attribution License (CC BY)</a>. The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</p> <p><span>*Correspondence:</span> Angelika Mustroph, <a href="mailto:angelika.mustroph@uni-bayreuth.de">angelika.mustroph@uni-bayreuth.de</a></p> <div class="clear"></div> </div></div></div> <p class="AbstractSummary__disclaimer"><span>Disclaimer: </span> All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. 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The journal has the long-term goal of supporting sustainable development, food security, functional ecosystems, biotechnology (including biofuels and biomaterials), and human health.\u003C\u002Fp\u003E\n\u003Cp\u003EFrontiers in Plant Science welcomes Original Research, Review, Opinion, and Perspective articles, among other submission types, covering the journal’s specialty sections:\u003C\u002Fp\u003E\n\n\u003Cdiv\u003E • aquatic photosynthetic organisms\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • crop and product physiology\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • functional plant ecology\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • functional and applied plant genomics\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • photosynthesis and photobiology\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant abiotic stress\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant bioinformatics\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant biophysics and modeling\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant biotechnology\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant breeding\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant cell biology\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant development and EvoDevo\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant genetics, epigenetics and chromosome biology\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant membrane traffic and transport\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant metabolism and chemodiversity\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant nutrition\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant pathogen interactions\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant physiology\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant proteomics and protein structural biology\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant symbiotic interactions\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant systematics and evolution\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • plant systems and synthetic biology\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • sustainable and intelligent phytoprotection\u003C\u002Fdiv\u003E\n\u003Cdiv\u003E • technical advances in plant science.\u003C\u002Fdiv\u003E\n\u003Cbr\u003E\n\u003Cp\u003EFurthermore, the journal welcomes submissions that support and advance the UN's Sustainable Development Goals (SDGs), notably SDG 13: climate action and SDG 15: life on land.\u003C\u002Fp\u003E  \n\n\u003Cp\u003EFrontiers in Plant Science is committed to advancing developments in the field of plant biology by allowing unrestricted access to articles and communicating scientific knowledge to researchers and the public alike, to enable the scientific breakthroughs of the future.\u003C\u002Fp\u003E \n \n\u003Cp\u003ERequirements\u003Cp\u003E\n\u003Cp\u003EManuscripts that focus on non-plant-related microbiology, human or animal genetics, and medical and pharmacological research are not suitable for publication in this journal. Pure field agriculture studies such as those focusing on fertilizer application or yield optimization, without relevance to plant science, are also not within the scope of this journal.\u003C\u002Fp\u003E\nStudies falling into the categories below will not be considered for review in this journal unless they are expanded and provide insight into the biological process being studied:\u003C\u002Fp\u003E\n\n\u003Cp\u003Ei) Descriptive collections of transcripts, proteins, or metabolites, including comparative sets as a result of different conditions or treatments;\u003C\u002Fp\u003E\n\u003Cp\u003Eii) Descriptive studies that define gene families using pure phylogenetics and the assignment of cursory functional attributions (e.g. expression profiles, promoter analysis, and bioinformatic parameters).\u003C\u002Fp\u003E\n\n\u003Cp\u003EQuantitative analysis needs to be performed on a minimum of three biological replicates in order to enable an assessment of significance. This includes quantitative omics studies (transcriptomics, proteomics, metabolomics) as well as phenotypic measurements, quantitative assays, and qPCR expression analysis. Studies that do not comply with these replication requirements will not be considered for review.\u003Cp\u003E\n\n\u003Cp\u003EStudies using transgenic or mutant lines (plants and algae), for example, T-DNA, transposon, RNAi, CRISPR\u002FCas9, chemically induced, overexpressors and reporter fusions (GUS, GFPs, LUC), should be based on data from multiple alleles (minimum of two) displaying a common and stable phenotype. Qualitative data can be presented from a single allele but should be indicative of observations from multiple alleles which should be explicitly stated in the text. Quantitative data should be derived from multiple alleles (at least two) and should be displayed separately for each allele (with at least three independent replications for each allele). Studies reporting single alleles may be considered acceptable when:\u003C\u002Fp\u003E\n\n\u003Cp\u003Ei) Complementation via transformation is used for confirmation;\u003C\u002Fp\u003E \n\u003Cp\u003Eii) The allele has been previously characterized and published, and is representative of multiple independent lines;\u003C\u002Fp\u003E\n\u003Cp\u003Eiii) In situations where genetic transformation is difficult or not yet possible, alternative evidence should be presented\u003C\u002Fp\u003E\n\n",palette:"green",impactFactor:"5.6",citeScore:"7.1",citations:"616000",showTagline:e,twitter:"@FrontPlantSci",__typename:"Journal"},currentFrontiersJournal:{id:q,name:n,slug:r,printISSN:e,shortName:H,electronicISSN:I,abbreviation:W,specialtyId:e,publicationDate:e,isOnline:h,isOpenForSubmissions:h,spaceId:c,field:{id:X,domainId:c,__typename:Y},__typename:a},articleHubSlug:g,articleHubPage:J,currentArticle:{id:897673,doi:Z,title:_,acceptanceDate:new Date(1649670608000),receptionDate:new Date(1647427812000),publicationDate:new Date(1651190400000),isPublished:h,abstract:$,researchTopic:{id:27508,title:"Adaptation of Plants to Waterlogging and Hypoxia",articlesCount:aa,isMagazinePage:k,slug:"adaptation-of-plants-to-waterlogging-and-hypoxia",isOpenForSubmission:k},articleType:{id:24,name:"Original Research"},stage:{id:K,name:g},keywords:["Brassica napus","waterlogging","root-zone hypoxia","fermenation","RNA sequencing"],authors:[{id:m,firstName:ab,lastName:"Ambros",givenNames:ab,isCorresponding:k,isProfilePublic:k,userId:m,affiliations:[{organizationName:s,countryName:t,cityName:g,stateName:g,zipCode:g}]},{id:m,firstName:ac,lastName:"Kotewitsch",givenNames:ac,isCorresponding:k,isProfilePublic:k,userId:m,affiliations:[{organizationName:s,countryName:t,cityName:g,stateName:g,zipCode:g}]},{id:m,firstName:ad,lastName:"Wittig",givenNames:ad,isCorresponding:k,isProfilePublic:k,userId:m,affiliations:[{organizationName:s,countryName:t,cityName:g,stateName:g,zipCode:g}]},{id:m,firstName:ae,lastName:"Bammer",givenNames:ae,isCorresponding:k,isProfilePublic:k,userId:m,affiliations:[{organizationName:s,countryName:t,cityName:g,stateName:g,zipCode:g}]},{id:af,firstName:ag,lastName:"Mustroph",givenNames:ag,isCorresponding:k,isProfilePublic:h,userId:af,affiliations:[{organizationName:s,countryName:t,cityName:g,stateName:g,zipCode:g}]}],editors:[{id:ah,firstName:ai,lastName:"Pampana",givenNames:ai,isCorresponding:k,isProfilePublic:h,userId:ah,affiliations:[{organizationName:"University of Pisa",countryName:aj,cityName:g,stateName:g,zipCode:g}]}],reviewers:[{id:ak,firstName:"Arun",lastName:"Shanker",givenNames:"Arun K.",isCorresponding:k,isProfilePublic:h,userId:ak,affiliations:[{organizationName:"Central Research Institute for Dryland Agriculture (ICAR)",countryName:"India",cityName:g,stateName:g,zipCode:g}]},{id:al,firstName:am,lastName:"Jespersen",givenNames:am,isCorresponding:k,isProfilePublic:h,userId:al,affiliations:[{organizationName:"University of Georgia",countryName:"United States",cityName:g,stateName:g,zipCode:g}]},{id:an,firstName:ao,lastName:"Farooq",givenNames:ao,isCorresponding:k,isProfilePublic:h,userId:an,affiliations:[{organizationName:"University of Teramo",countryName:aj,cityName:g,stateName:g,zipCode:g}]}],journal:{id:q,slug:r,name:n,shortName:H,electronicISSN:I,field:{id:X,domainId:c,__typename:Y},specialtyId:e,journalSectionPaths:[{section:ap,__typename:"journal_journalSectionPath"}],__typename:a},section:ap,impactMetrics:{views:1900,downloads:718,citations:L},volume:M,articleVolume:"Volume 13 - 2022",relatedArticles:[],isPublishedV2:k,contents:{fullTextHtml:"\u003Cdiv class=\"JournalAbstract\"\u003E\r\n\u003Ca id=\"h1\" name=\"h1\"\u003E\u003C\u002Fa\u003E\r\n\u003Ch1\u003ETranscriptional Response of Two \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E Cultivars to Short-Term Hypoxia in the Root Zone\u003C\u002Fh1\u003E\r\n\u003Cdiv class=\"authors\"\u003E\r\n\u003Cimg class=\"pr5\" src=\"http:\u002F\u002F3b76aaf63d1816bb57bf-a34624e694c43cdf8b40aa048a644ca4.r96.cf2.rackcdn.com\u002FDesign\u002FImages\u002Fnewprofile_default_profileimage_new.jpg\" alt=\"\"\u002F\u003EStefanie Ambros, \u003Cimg class=\"pr5\" src=\"http:\u002F\u002F3b76aaf63d1816bb57bf-a34624e694c43cdf8b40aa048a644ca4.r96.cf2.rackcdn.com\u002FDesign\u002FImages\u002Fnewprofile_default_profileimage_new.jpg\" alt=\"\"\u002F\u003EMona Kotewitsch, \u003Cimg class=\"pr5\" src=\"http:\u002F\u002F3b76aaf63d1816bb57bf-a34624e694c43cdf8b40aa048a644ca4.r96.cf2.rackcdn.com\u002FDesign\u002FImages\u002Fnewprofile_default_profileimage_new.jpg\" alt=\"\"\u002F\u003EPhilipp R. Wittig, \u003Cimg class=\"pr5\" src=\"http:\u002F\u002F3b76aaf63d1816bb57bf-a34624e694c43cdf8b40aa048a644ca4.r96.cf2.rackcdn.com\u002FDesign\u002FImages\u002Fnewprofile_default_profileimage_new.jpg\" alt=\"\"\u002F\u003EBettina Bammer and \u003Ca href=\"https:\u002F\u002Fwww.frontiersin.org\u002Fpeople\u002Fu\u002F27285\" class=\"user-id-27285\"\u003E\u003Cimg class=\"pr5\" src=\"https:\u002F\u002Floop.frontiersin.org\u002Fimages\u002Fprofile\u002F27285\u002F24\" onerror=\"this.src='http:\u002F\u002F3b76aaf63d1816bb57bf-a34624e694c43cdf8b40aa048a644ca4.r96.cf2.rackcdn.com\u002FDesign\u002FImages\u002Fnewprofile_default_profileimage_new.jpg'\" alt=\"\"\u002F\u003EAngelika Mustroph\u003C\u002Fa\u003E\u003Csup\u003E*\u003C\u002Fsup\u003E\r\n\u003C\u002Fdiv\u003E\r\n\u003Cul class=\"notes\"\u003E\r\n\u003Cli class=\"pl0\"\u003EDepartment of Plant Physiology, University of Bayreuth, Bayreuth, Germany\u003C\u002Fli\u003E\r\n\u003C\u002Ful\u003E\r\n\u003Cp class=\"mb0\"\u003EWaterlogging is one major stress for crops and causes multiple problems for plants, for example low gas diffusion, changes in redox potential and accumulation of toxic metabolites. \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E is an important oil crop with high waterlogging sensitivity, which may cause severe yield losses. Its reactions to the stress are not fully understood. In this work the transcriptional response of rapeseed to one aspect of waterlogging, hypoxia in the root zone, was analyzed by RNAseq, including two rapeseed cultivars from different origin, Avatar from Europe and Zhongshuang 9 from Asia. Both cultivars showed a high number of differentially expressed genes in roots after 4 and 24 h of hypoxia. The response included many well-known hypoxia-induced genes such as genes coding for glycolytic and fermentative enzymes, and strongly resembled the hypoxia response of the model organism \u003Ci\u003EArabidopsis thaliana\u003C\u002Fi\u003E. The carbohydrate status of roots, however, was minimally affected by root hypoxia, with a tendency of carbohydrate accumulation rather than a carbon starvation. Leaves did not respond to the root stress after a 24-h treatment. In agreement with the gene expression data, subsequent experiments with soil waterlogging for up to 14 days revealed no differences in response or tolerance to waterlogging between the two genotypes used in this study. Interestingly, using a 0.1% starch solution for waterlogging, which caused a lowered soil redox potential, resulted in much stronger effects of the stress treatment than using pure water suggesting a new screening method for rapeseed cultivars in future experiments.\u003C\u002Fp\u003E\r\n\u003Cdiv class=\"clear\"\u003E\u003C\u002Fdiv\u003E\r\n\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"JournalFullText\"\u003E\r\n\u003Ca id=\"h2\" name=\"h2\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003EIntroduction\u003C\u002Fh2\u003E\r\n\u003Cp class=\"mb15\"\u003EMany crop plants are very sensitive to flooding periods which may occur after heavy rainfall, rising sea water, or during fast snow melting in spring. Besides other effects, flooding severely restricts gas diffusion into and out of the plant tissues that are under water, leading to deficiency in oxygen and carbon dioxide. The increased frequency of extreme weather events due to climate change affects certain regions around the world, and these regions at risk might expand in the future even more (e.g., \u003Ca href=\"#B35\"\u003EKundzewicz et al., 2014\u003C\u002Fa\u003E; \u003Ca href=\"#B67\"\u003ETrenberth et al., 2014\u003C\u002Fa\u003E; \u003Ca href=\"#B59\"\u003EPekel et al., 2016\u003C\u002Fa\u003E; \u003Ca href=\"#B8\"\u003EBlöschl et al., 2019\u003C\u002Fa\u003E). Flooding events can be differentiated into two types that require different adaptations of plants, namely full submergence and root waterlogging (\u003Ca href=\"#B64\"\u003ESasidharan et al., 2017\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EWaterlogging is considered as the lesser problematic stress type. Many plants have developed adaptational mechanisms to cope with this type of stress, resulting in an avoidance or a tolerance strategy. One very important response to waterlogging is the formation of aerenchyma tissue within leaves, stems and roots, thus avoiding oxygen deficiency within plant organs that are under water (summarized in \u003Ca href=\"#B69\"\u003EVoesenek and Bailey-Serres, 2015\u003C\u002Fa\u003E; \u003Ca href=\"#B53\"\u003EMustroph et al., 2018\u003C\u002Fa\u003E; \u003Ca href=\"#B77\"\u003EYamauchi et al., 2018\u003C\u002Fa\u003E). Other mechanisms such as a barrier against radial oxygen loss in underwater organs and the formation of adventitious roots with high porosity also help to maintain a sufficient oxygen content within plant tissues.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EBesides these avoidance mechanisms, there are also acclimation responses that enable tolerance to low oxygen concentrations within plant tissues at least for some time (summarized in \u003Ca href=\"#B5\"\u003EBailey-Serres et al., 2012\u003C\u002Fa\u003E; \u003Ca href=\"#B69\"\u003EVoesenek and Bailey-Serres, 2015\u003C\u002Fa\u003E; \u003Ca href=\"#B53\"\u003EMustroph et al., 2018\u003C\u002Fa\u003E). These mainly include biochemical modifications such as induction of glycolysis and fermentation in order to maintain energy production through periods with limited mitochondrial respiration. These responses also include specific enzymes or isoforms of starch and sucrose cleavage and glycolytic by-passes (summarized in \u003Ca href=\"#B27\"\u003EHuang et al., 2008\u003C\u002Fa\u003E; \u003Ca href=\"#B51\"\u003EMustroph et al., 2014\u003C\u002Fa\u003E, \u003Ca href=\"#B53\"\u003E2018\u003C\u002Fa\u003E; \u003Ca href=\"#B4\"\u003EAtwell et al., 2015\u003C\u002Fa\u003E). Furthermore, growth and biosynthetic processes are strongly down-regulated under low-oxygen stress, including ribosomal activity on non-essential transcripts, since translation is an energy-consuming process (\u003Ca href=\"#B10\"\u003EBranco-Price et al., 2008\u003C\u002Fa\u003E; \u003Ca href=\"#B54\"\u003EMustroph et al., 2009\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EHowever, most crop species cannot tolerate longer periods of waterlogging since they only possess a limited acclimation potential. \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E is an important oil crop plant and it is also used for animal feed. However, this plant species is very sensitive to soil flooding and waterlogging, since it is not able to form aerenchyma in the roots and exhibits a high radial oxygen loss under water (\u003Ca href=\"#B70\"\u003EVoesenek et al., 1999\u003C\u002Fa\u003E). Still, rapeseed is often used as a rotation crop on rice fields in Asia (\u003Ca href=\"#B78\"\u003EZou et al., 2013a\u003C\u002Fa\u003E; \u003Ca href=\"#B38\"\u003ELee et al., 2014\u003C\u002Fa\u003E), and therefore is often subjected to flooding conditions. Despite the importance and sensitivity of this crop, little is known about its molecular response to flooding conditions such as waterlogging and submergence. Such information could be vital to develop cultivars with enhanced flooding tolerance.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EIndeed, several approaches have been used to identify rapeseed cultivars with higher waterlogging tolerance within the last years, mainly focusing on Asian cultivars (e.g., \u003Ca href=\"#B79\"\u003EZou et al., 2013b\u003C\u002Fa\u003E,\u003Ca href=\"#B80\"\u003E2014\u003C\u002Fa\u003E; summarized in \u003Ca href=\"#B48\"\u003EMustroph, 2018\u003C\u002Fa\u003E). However, the molecular bases for these tolerance traits are still not known, despite efforts to study the response of different cultivars at the level of transcriptome (\u003Ca href=\"#B78\"\u003EZou et al., 2013a\u003C\u002Fa\u003E,\u003Ca href=\"#B81\"\u003E2015\u003C\u002Fa\u003E) and proteome (\u003Ca href=\"#B75\"\u003EXu et al., 2018\u003C\u002Fa\u003E). Mapping processes of these cultivars with contrasting responses are ongoing, with no clear results so far (\u003Ca href=\"#B16\"\u003EDing et al., 2020\u003C\u002Fa\u003E). There could be several reasons for it. For example, the molecular analyses were performed at specific developmental stages or with a stress duration that did not reveal differences between the cultivars. The other possibility would be that little genetic differences in waterlogging tolerance exist between genotypes studied so far, despite interesting observations in the field. We therefore raised the following hypothesis: if differences in waterlogging tolerance between contrasting rapeseed cultivars exist, those should emerge through a comparison of an Asian cultivar with observed waterlogging tolerance, Zhongshuang 9 (\u003Ca href=\"#B79\"\u003EZou et al., 2013b\u003C\u002Fa\u003E,\u003Ca href=\"#B80\"\u003E2014\u003C\u002Fa\u003E), and a European cultivar not bred for flooding tolerance.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EThere is evidence that \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E roots can respond to waterlogging and the associated hypoxia at the transcriptional level, for example by induction of genes coding for fermentative enzymes (\u003Ca href=\"#B78\"\u003EZou et al., 2013a\u003C\u002Fa\u003E,\u003Ca href=\"#B81\"\u003E2015\u003C\u002Fa\u003E), while leaves above air responded in a different way (\u003Ca href=\"#B38\"\u003ELee et al., 2014\u003C\u002Fa\u003E). On the other hand, avoidance mechanisms such as the formation of aerenchyma are not present in this species (\u003Ca href=\"#B70\"\u003EVoesenek et al., 1999\u003C\u002Fa\u003E; \u003Ca href=\"#B60\"\u003EPloschuk et al., 2018\u003C\u002Fa\u003E). However, the existing transcriptome analyses were performed without the full genome information on \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E, which was only published later (\u003Ca href=\"#B13\"\u003EChalhoub et al., 2014\u003C\u002Fa\u003E). It is therefore not known whether all or only a few gene copies for one gene function of the tetraploid species are hypoxia responsive. We hypothesize that most or all gene copies of a hypoxia-induced gene in the rapeseed genome are responsive to the stress treatment, which would require modification of not only one but multiple target genes by breeders.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EThe aim of our work was to (1) compare the transcriptional responses of two different \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E cultivars to one aspect of waterlogging, hypoxic conditions in the root zone, including the analysis of roots and leaves at two different time points and (2) to evaluate with different growth conditions whether a difference in waterlogging tolerance exists between the two cultivars. In our previous analysis utilizing the same two cultivars (\u003Ca href=\"#B73\"\u003EWittig et al., 2021\u003C\u002Fa\u003E), we could not identify significant differences in submergence tolerance, but a strong transcriptional response to submergence in leaves of both genotypes. Here, we also identified a large number of transcripts induced by hypoxia in roots, which were mainly similar between the cultivars and also similar to the transcriptional response of \u003Ci\u003EArabidopsis thaliana\u003C\u002Fi\u003E to hypoxia (\u003Ca href=\"#B54\"\u003EMustroph et al., 2009\u003C\u002Fa\u003E, \u003Ca href=\"#B52\"\u003E2010\u003C\u002Fa\u003E; \u003Ca href=\"#B37\"\u003ELee and Bailey-Serres, 2019\u003C\u002Fa\u003E). However, the response of hypoxic roots was very different from submerged rapeseed leaves. In addition, and in accordance with our analysis under submergence, we could not identify differences in waterlogging tolerance between the two cultivars, despite the application of several growth conditions and stress treatment methods.\u003C\u002Fp\u003E\r\n\u003Ca id=\"h3\" name=\"h3\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003EMaterials and Methods\u003C\u002Fh2\u003E\r\n\u003Ch3 class=\"pt0\"\u003EPlant Material and Growth Conditions\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb15\"\u003ESeeds of two rapeseed cultivars were used, the hybrid winter cultivar Avatar (\u003Ca href=\"#B74\"\u003EWollmer et al., 2018\u003C\u002Fa\u003E; \u003Ca href=\"#B73\"\u003EWittig et al., 2021\u003C\u002Fa\u003E) as well as the semi-winter cultivar Zhongshuang 9 (\u003Ca href=\"#B78\"\u003EZou et al., 2013a\u003C\u002Fa\u003E; \u003Ca href=\"#B73\"\u003EWittig et al., 2021\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EFor the experiments with plants in hydroponics, dry seeds were sterilized in a chlorine gas atmosphere for 45 min. After removal of the gas, the sterilized seeds were germinated in small tubes containing 1:10 Hoagland solution (0.28 mM Ca(NO\u003Csub\u003E3\u003C\u002Fsub\u003E)\u003Csub\u003E2\u003C\u002Fsub\u003E, 0.1 mM (NH\u003Csub\u003E4\u003C\u002Fsub\u003E)H\u003Csub\u003E2\u003C\u002Fsub\u003EPO\u003Csub\u003E4\u003C\u002Fsub\u003E, 0.2 mM MgSO\u003Csub\u003E4\u003C\u002Fsub\u003E, 0.6 mM KNO\u003Csub\u003E3\u003C\u002Fsub\u003E, 5 μM of a complex of Fe(III) and N,N′-di-(2-hydroxybenzoyl)-ethylenediamine-N,N′-diacetate (ABCR, Karlsruhe, Germany), pH 5.7). Plants were grown in a short-day chamber (8 h illumination with ca. 100 μmol photons * m\u003Csup\u003E–2\u003C\u002Fsup\u003E * s\u003Csup\u003E–1\u003C\u002Fsup\u003E) at 23°C. After 4 days, the tubes were transferred into large buckets (4.5 l of volume) by use of a perforated plate. The buckets were filled with KNOP nutrient solution (\u003Ca href=\"#B50\"\u003EMustroph et al., 2006\u003C\u002Fa\u003E), which was continuously bubbled with air. The nutrient solution was replaced twice a week. When plants were 15 days old, the stress treatment was applied to half of the plants by bubbling the nutrient solution with nitrogen gas for the time indicated. The shoot tissues remained in air.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EFor the experiments with plants on soil, seeds were pre-germinated in the dark at 30°C for 24 h on moist filter paper. Subsequently, germinating seeds were transferred into pots (5.3 × 5.3 cm) filled with a soil-sand mixture. The soil used was standard potting soil type GS90 coarse: potting soil (Ökohum GmbH): vermiculite in a ratio of 3:3:1. The potting soil was mixed with sand in a ratio of 3:1. Plants were grown in a short-day chamber (8 h illumination with ca. 100 μmol photons * m\u003Csup\u003E–2\u003C\u002Fsup\u003E * s\u003Csup\u003E–1\u003C\u002Fsup\u003E) at 23°C. 15-day-old plants were used for the experiments. For stress treatment of soil-grown plants, two waterlogging variants were used. In a first set, pots were placed in a box, which was subsequently filled with tap water up to the soil surface. In a second set, one portion of the pots were placed into boxes and filled with a 0.1% starch solution in deionized water (\u003Ca href=\"#B44\"\u003EMano and Takeda, 2012\u003C\u002Fa\u003E; \u003Ca href=\"#B46\"\u003EMiricescu et al., 2021\u003C\u002Fa\u003E), while another portion of the pots were waterlogged with deionized water only. Control pots were watered regularly as needed. Both treatments lasted for two weeks. The number of plants per replicate is specified in the respective figure part.\u003C\u002Fp\u003E\r\n\u003Ch3\u003ERNA Extraction, RNA Sequencing and Bioinformatics\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb15\"\u003EFor transcriptome analyses, root and leaf tissue from plants grown in hydroponics were used. Plants were stressed with 4 and 24 h of nitrogen flushing of the medium in the root zone. Subsequently, the entire root system and the first true leaf was harvested together with air-gassed controls and immediately frozen in liquid nitrogen. The frozen tissue was ground in liquid nitrogen. RNA extraction, quality control, processing of the RNA for sequencing, and the subsequent bioinformatics analyses were carried out exactly as previously described (\u003Ca href=\"#B73\"\u003EWittig et al., 2021\u003C\u002Fa\u003E). Briefly, RNA was extracted by use of the ISOLATE II RNA plant kit (Bioline, Luckenwalde, Germany). After quality controls through gel electrophoresis and fluorimeter measurements, RNA was further processed by Eurofins Genomics Europe Shared Services GmbH (Ebersberg, Germany). Sequencing was done with the 150 bp paired-end mode on the Illumina HiSeq 4000 platform.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EThree replicates per time point and genotype were done, resulting in a total of 36 libraries, with 30 Mio to 50 Mio reads per library (\u003Ca href=\"#S10\"\u003ESupplementary Table 1\u003C\u002Fa\u003E). Transcript quantification was done by use of the Kallisto software (\u003Ca href=\"#B11\"\u003EBray et al., 2016\u003C\u002Fa\u003E). About 76 to 80% of the reads from the cultivar Avatar aligned to the reference genome of Darmor (\u003Ca href=\"#B13\"\u003EChalhoub et al., 2014\u003C\u002Fa\u003E). Reads from the cultivar Zhongshuang 9 had a mapping rate of 67 to 75% (\u003Ca href=\"#S10\"\u003ESupplementary Table 1\u003C\u002Fa\u003E). Mapping rates for leaves were generally higher than for roots and were similar to the mapping rates in our previous study (\u003Ca href=\"#B73\"\u003EWittig et al., 2021\u003C\u002Fa\u003E). DEG analysis was carried out with the edgeR and limma Bioconductor packages in R (\u003Ca href=\"#B45\"\u003EMcCarthy et al., 2012\u003C\u002Fa\u003E) as previously described (\u003Ca href=\"#B47\"\u003EMüller et al., 2021\u003C\u002Fa\u003E). RNA sequencing raw and processed data have been deposited at the Gene Expression Omnibus database under the accession GSE180262.\u003C\u002Fp\u003E\r\n\u003Ch3\u003EEnzyme Extraction and ADH Activity\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb0\"\u003EFrozen root material from plants grown in hydroponics was ground to a fine powder. Enzymes were extracted in 50 mM Hepes-KOH, pH 6.8 containing 5 mM Mg acetate, 5 mM β-mercaptoethanol, 15% (v\u002Fv) glycerin, 1 mM EDTA, 1 mM EGTA, and 0.1 mM Pefabloc proteinase inhibitor (Sigma-Aldrich, Germany). The samples were then centrifuged at 13,000 g at 4°C for 15 min. The resulting supernatant was used for spectrophotometric determination of ADH activity at 340 nm (SPECORD 200 PLUS, Analytic Jena, Germany). The ADH activity was measured in 50 mM TES buffer, pH 7.5 including 0.17 mM NADH (\u003Ca href=\"#B72\"\u003EWaters et al., 1991\u003C\u002Fa\u003E). The reaction was started by adding 10 mM acetaldehyde. The protein content as determined by the Bradford reagent and by use of a BSA standard curve (\u003Ca href=\"#B9\"\u003EBradford, 1976\u003C\u002Fa\u003E). The number of biological replicates is specified in the respective figure part.\u003C\u002Fp\u003E\r\n\u003Ch3\u003ECarbohydrate Extraction and Measurement of Sugar Content\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb15\"\u003EOne leaf of each plant (from hydroponics or soil-grown plants) was frozen in liquid nitrogen and the fresh weight of the samples was determined. The frozen plant samples were ground to a fine powder. To extract soluble sugars, 1 ml of 0.83 N perchloric acid was added, mixed well, and then stored on ice until all samples were processed. The samples were then centrifuged for 15 min at 13,000 g and 4°C, and the supernatant was transferred to a new 1.5 ml Eppendorf reaction tube. The pellet was overlaid with 600 μl of 80% ethanol for subsequent starch extraction and temporarily stored at 4°C. The supernatant was mixed with 200 μl of 1 M Bicine and quickly neutralized with 100 μl of 4 M KOH. The samples were then centrifuged for 10 min at 13,200 rpm and 4°C and the supernatant was transferred to a new reaction tube. The supernatant was either frozen at −20°C or used directly for the measurement of the sugar content.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EFor starch extraction, the pellet from sugar extraction was mixed with 600 μl of 80% ethanol and centrifuged at 13,000 g and 4°C for 5 min. The supernatant was then removed, and the procedure was repeated once. After removal of the ethanol, 400 μl of 0.2 M KOH was added to the pellet and the samples were homogenized. This was placed on a heating block at 95°C for 1 h. After incubation, the samples were centrifuged for 5 min at 10,000 rpm and 4°C, and the supernatant was transferred to a new 1.5 ml reaction tube. The supernatant was neutralized with 80 μl of 1 N acetic acid. From the extract, 50 μl was then mixed with 100 μl amyloglucosidase (2 mg\u002Fml enzyme in 50 mM sodium acetate pH 5.0) and incubated overnight at 55°C on the heating block.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EBoth sugar and starch content were measured spectrophotometrically (SPECORD 200 PLUS, Analytic Jena, Germany). For this, 780 μl of 0.1 M imidazole buffer containing 1 mM ATP and 2 mM NAD in a semi-micro cuvette was mixed with 20 μl of each sample and 1 u glucose-6-phosphate dehydrogenase was added. Then, the measurement was started at a wavelength of 340 nm. For both the sugar and the starch measurement 0.5 u of hexokinase in 5 μl of imidazole buffer was added after 10 min to measure glucose. Starch measurement was stopped 20 min after addition of the enzyme. For soluble sugars, 0.2 u phosphoglucose isomerase in 5 μl buffer was pipetted to the samples after a plateau was reached, to measure fructose. After constant values had again been established, 60 u invertase in 5 μl buffer was added and mixed well to determine the sucrose content. The number of biological replicates is specified in the respective figure part.\u003C\u002Fp\u003E\r\n\u003Ch3\u003EChlorophyll Fluorescence and Chlorophyll Content\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb15\"\u003ETo determine the chlorophyll fluorescence, the quantum yield of photosystem II of the plants grown on soil was measured under constant conditions using a Junior-PAM (Walz, Effeltrich, Germany). This PAM measurement (pulse-amplitude-modulated fluorescence measurement) was performed using a saturating pulse method (SAT pulses). A large adult light-adapted leaf of each plant was clamped between two magnets and irradiated for 10 seconds with ambient light of about 100 μmol photons * m\u003Csup\u003E–2\u003C\u002Fsup\u003E * s\u003Csup\u003E–1\u003C\u002Fsup\u003E, and subsequently a saturation pulse was applied. The ΦPSII value was calculated and used for further evaluation.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EDetermination of chlorophyll content in an invasive way was done as follows. Extraction of chlorophyll was performed according to the protocol of \u003Ca href=\"#B57\"\u003EPark et al. (2018)\u003C\u002Fa\u003E. In this process, 1.4 ml of 80% aqueous acetone was added to frozen and ground leaf samples and mixed well. Then, the samples were stored overnight at 4°C. The next day, the leaf samples were centrifuged at 13,000 g for 5 min at 4°C and the supernatant was pipetted into a new tube. For measurement of chlorophyll content, the supernatant was diluted 1:10 with acetone in a semi-micro cuvette and absorbance was measured at 645 nm and 663 nm. Chlorophyll content was calculated by use of the formula developed by \u003Ca href=\"#B2\"\u003EArnon (1949)\u003C\u002Fa\u003E.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EDetermination of chlorophyll content in a non-invasive way was done by use of the chlorophyll concentration meter MC-100 (Apogee Instruments, Logan, United States) using the settings for kohlrabi.\u003C\u002Fp\u003E\r\n\u003Ch3\u003EChemical Parameters of the Waterlogging Solution\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb0\"\u003EOxygen content, oxidation-reduction potential (ORP), pH and conductivity of the waterlogging solution of soil-grown plants was determined by use of the multimeter PCE-PHD 1 (PCE instruments, Meschede, Germany) and the following electrodes: OXPB-11, ORP-14, PE-03, CDPB-03. Measurements were done about 2 to 3 h after start of illumination. The temperature of the waterlogging solution ranged between 19 and 23°C at the time of the measurements.\u003C\u002Fp\u003E\r\n\u003Ca id=\"h4\" name=\"h4\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003EResults\u003C\u002Fh2\u003E\r\n\u003Ch3 class=\"pt0\"\u003ETranscriptome Analysis Under Root Hypoxia\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb15\"\u003EWaterlogging is a complex stress in nature, including limited gas diffusion, microbial activities, changes in redox chemistry and accumulation of toxic metabolites. In a simplified approach we initially focused on the low-oxygen component of waterlogging and therefore performed an RNAseq analysis of plants in hydroponics with their roots exposed to nitrogen gassing causing hypoxia (\u003Ca href=\"#S10\"\u003ESupplementary Table 1\u003C\u002Fa\u003E). This experimental set-up also allowed for controlled aeration of the root system and allowed a direct comparison to the hypoxia response of the model species \u003Ci\u003EArabidopsis thaliana\u003C\u002Fi\u003E (\u003Ca href=\"#B54\"\u003EMustroph et al., 2009\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003ETreating plant roots with hypoxia caused a strong transcriptional response in roots of both genotypes. After 4 h, 5,736 and 3,948 transcripts were significantly up-regulated compared to air-treated controls (log2FC > 1, FDR < 0.01) in Avatar and Zhongshuang 9, respectively, with an overlap of 3,145 transcripts (\u003Ca href=\"#F1\"\u003EFigure 1\u003C\u002Fa\u003E and \u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns R to AD). After 24 h, 2,550 and 3,061 transcripts were induced, with an overlap of 1,729 transcripts. The overlap between 4 h and 24 h was 1,897 and 1,844 transcripts for Avatar and Zhongshuang 9, respectively (\u003Ca href=\"#S10\"\u003ESupplementary Figure 1\u003C\u002Fa\u003E). The number of down-regulated genes in roots was even higher. 8,983 and 7,010 transcripts were down-regulated after 4 h, and 4,415 and 5,619 transcripts were down-regulated after 24 h in Avatar and Zhongshuang 9, respectively. Again, there was a high similarity between the time points with 2,952 and 3,237 transcripts commonly downregulated in Avatar and Zhongshuang 9, respectively (\u003Ca href=\"#S10\"\u003ESupplementary Figure 1\u003C\u002Fa\u003E). The response of the leaves to hypoxia in the root zone was only analyzed after 24 h and was much lower, with 341 and 112 transcripts significantly induced in Avatar and Zhongshuang 9, with an overlap of only 12 transcripts. 564 and 418 transcripts were significantly down-regulated in leaves, with an overlap of 88 transcripts (\u003Ca href=\"#F1\"\u003EFigure 1\u003C\u002Fa\u003E and \u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns R to AD).\u003C\u002Fp\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"Imageheaders\"\u003EFIGURE 1\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"FigureDesc\"\u003E\r\n\u003Ca href=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_m\u002Ffpls-13-897673-g001.jpg\" name=\"figure1\" target=\"_blank\"\u003E\r\n\u003Cimg src=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_t\u002Ffpls-13-897673-g001.gif\" id=\"F1\" alt=\"www.frontiersin.org\" \u002F\u003E\u003C\u002Fa\u003E\r\n\u003Cp\u003E\u003Cstrong\u003EFigure 1.\u003C\u002Fstrong\u003E Venn diagrams showing overlaps of induced \u003Cb\u003E(A,C,E)\u003C\u002Fb\u003E or repressed \u003Cb\u003E(B,D,F)\u003C\u002Fb\u003E genes between two \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E cultivars (Avatar, Zhongshuang 9) in hydroponics after 4 and 24 h of root hypoxia, compared with aerated controls. \u003Cb\u003E(A,B)\u003C\u002Fb\u003E Roots were treated with 4 h of hypoxia; \u003Cb\u003E(C,D)\u003C\u002Fb\u003E Roots were treated with 24 h of hypoxia; \u003Cb\u003E(E,F)\u003C\u002Fb\u003E Leaves of plants treated with root hypoxia for 24 h.\u003C\u002Fp\u003E\r\n\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"clear\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Ch3\u003ERoots Induce a Typical and Strong Hypoxia Response\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb15\"\u003EA functional gene ontology (GO) analysis of the transcripts of roots responding to nitrogen-gassing revealed many GO categories to be significantly enriched (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E). After 4 h, many categories involved in stress response were enriched, for example “response to chitin,” “heat acclimation,” “respiratory burst involved in defense response,” and “intracellular signal transduction”. Furthermore, hormonal responses were induced, such as “response to ethylene,” “response to jasmonic acid,” and “salicylic acid mediated signaling pathway.” The hypoxia-related terms “response to hypoxia” and “anaerobic respiration” were enriched, and this enrichment was even higher after 24 h. Comparison of genotypes revealed a very similar response, but surprisingly, a few chloroplast-related GOs were enriched only in Avatar roots after 4 h (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EIn general, the response in roots after 24 h was very similar to the response after 4 h, but fewer genes remained induced (\u003Ca href=\"#S10\"\u003ESupplementary Figure 1\u003C\u002Fa\u003E). The functional categories “jasmonic acid biosynthetic process,” “response to water deprivation,” and “endoplasmic reticulum unfolded protein response” were less enriched after 24 than after 4 h (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EAmong down-regulated genes after 4 h, we observed the functional categories “extracellular region,” “anchored component of membrane,” “cell proliferation,” “histone H3-K9 methylation,” “plant-type cell wall,” and categories associated with DNA replication. DNA replication was still enriched in Zhongshuang 9 after 24 h, but much less affected in Avatar after 24 h. In contrast, some categories, for example “trichoblast differentiation”, were more enriched in Avatar after 4 and 24 h than in the other genotype. Furthermore, “Casparian strip” was more enriched after 24 than 4 h in both genotypes. Among enriched GO terms of down-regulated genes, many were associated with biosynthetic processes (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EThe enrichment of hypoxia-related categories in this dataset let us to compare the rapeseed hypoxia response to the previously defined hypoxia core response genes (HRGs) of Arabidopsis (\u003Ca href=\"#B54\"\u003EMustroph et al., 2009\u003C\u002Fa\u003E). Indeed, of the 49 HRGs from Arabidopsis (\u003Ca href=\"#F2\"\u003EFigure 2\u003C\u002Fa\u003E), which correspond to 161 expressed transcripts in rapeseed (\u003Ca href=\"#S10\"\u003ESupplementary Figure 2\u003C\u002Fa\u003E), 118 to 127 transcripts responded to hypoxia in roots after 4 and 24 h, and therefore showed a highly significant enrichment (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, column Q; \u003Ca href=\"#S10\"\u003ESupplementary Table 4\u003C\u002Fa\u003E). In many cases, most or all isogenes of one HRG in Arabidopsis responded in a similar manner to the stress in rapeseed, but with some exceptions, for example \u003Ci\u003EACT DOMAIN REPEAT\u003C\u002Fi\u003E 7 (\u003Ci\u003EACR7\u003C\u002Fi\u003E), \u003Ci\u003EALANINE AMINTRANSFERASE 1\u003C\u002Fi\u003E (\u003Ci\u003EAlaAT1\u003C\u002Fi\u003E), \u003Ci\u003EFCS-LIKE ZINC FINGER PROTEINS with DUF581\u003C\u002Fi\u003E (\u003Ci\u003EFLZ1\u003C\u002Fi\u003E, \u003Ci\u003EFLZ2\u003C\u002Fi\u003E and \u003Ci\u003EFLZ13\u003C\u002Fi\u003E), \u003Ci\u003EAT4G39675\u003C\u002Fi\u003E (hypothetical protein), \u003Ci\u003EPHLOEM PROTEIN 2-A FAMILY\u003C\u002Fi\u003E (\u003Ci\u003EPP2-A11\u003C\u002Fi\u003E and \u003Ci\u003EPP2-A13\u003C\u002Fi\u003E), and \u003Ci\u003ERESPIRATORY BURST OXIDASE HOMOLOGUE D\u003C\u002Fi\u003E (\u003Ci\u003ERBOHD\u003C\u002Fi\u003E) (\u003Ca href=\"#S10\"\u003ESupplementary Figure 2\u003C\u002Fa\u003E). Both genotypes responded in a very similar way, and only one HRG, \u003Ci\u003EAT5G10040\u003C\u002Fi\u003E, was induced by hypoxia in Avatar, but not in Zhongshuang 9 (\u003Ca href=\"#F2\"\u003EFigure 2\u003C\u002Fa\u003E and \u003Ca href=\"#S10\"\u003ESupplementary Figure 2\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"Imageheaders\"\u003EFIGURE 2\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"FigureDesc\"\u003E\r\n\u003Ca href=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_m\u002Ffpls-13-897673-g002.jpg\" name=\"figure2\" target=\"_blank\"\u003E\r\n\u003Cimg src=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_t\u002Ffpls-13-897673-g002.gif\" id=\"F2\" alt=\"www.frontiersin.org\" \u002F\u003E\u003C\u002Fa\u003E\r\n\u003Cp\u003E\u003Cstrong\u003EFigure 2.\u003C\u002Fstrong\u003E Heatmap of hypoxia core-response genes (\u003Ca href=\"#B54\"\u003EMustroph et al., 2009\u003C\u002Fa\u003E) from the \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E expression data. A summary of up to six rapeseed gene IDs for one Arabidopsis gene ID is shown. For expression of all rapeseed genes, please see \u003Ca href=\"#S10\"\u003ESupplementary Figure 2\u003C\u002Fa\u003E. Values are signal-log ratios (SLR) of summed counts of root-zone hypoxia vs. aerated control. AV, Avatar; ZS, Zhongshuang 9. The color intensity reflects the SLR values (blue, –3; yellow, + 3). Crossed cells represent values that are not significant (FDR > 0.01).\u003C\u002Fp\u003E\r\n\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"clear\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cp class=\"mb15 w100pc float_left mt15\"\u003EOf the genes highly expressed in hypoxic rapeseed roots, several have a known function under hypoxia, for example primary metabolism and glycolysis (\u003Ci\u003EPYRUVATE DECARBOXYLASE\u003C\u002Fi\u003E, \u003Ci\u003EPDC1\u003C\u002Fi\u003E and \u003Ci\u003EPDC3\u003C\u002Fi\u003E; \u003Ci\u003EALCOHOL DEHYDROGENASE 1\u003C\u002Fi\u003E, \u003Ci\u003EADH1\u003C\u002Fi\u003E; \u003Ci\u003EAlaAT1\u003C\u002Fi\u003E; \u003Ci\u003ESUCROSE SYNTHASE 1\u003C\u002Fi\u003E, \u003Ci\u003ESUS1\u003C\u002Fi\u003E; \u003Ci\u003EFRUCTOKINASE 2\u003C\u002Fi\u003E, \u003Ci\u003EFRK2\u003C\u002Fi\u003E; \u003Ci\u003EPHOSPHOFRUCTOKINASE\u003C\u002Fi\u003E, \u003Ci\u003EPFK3\u003C\u002Fi\u003E and \u003Ci\u003EPFK6\u003C\u002Fi\u003E; \u003Ci\u003EFRUCTOSE-BISPHOSPHATE ALDOLASE 6\u003C\u002Fi\u003E, \u003Ci\u003EFBA6\u003C\u002Fi\u003E), or signal transduction (\u003Ci\u003EHYPOXIA-RESPONSIVE ERF\u003C\u002Fi\u003E, \u003Ci\u003EHRE1\u003C\u002Fi\u003E and \u003Ci\u003EHRE2\u003C\u002Fi\u003E; \u003Ci\u003EHYPOXIA RESPONSE ATTENUATOR 1\u003C\u002Fi\u003E, \u003Ci\u003EHRA1\u003C\u002Fi\u003E; \u003Ci\u003ELOB DOMAIN CONTAINING PROTEIN 41\u003C\u002Fi\u003E, \u003Ci\u003ELBD41\u003C\u002Fi\u003E). A few HRGs were not induced by hypoxia in rapeseed, but in Arabidopsis (\u003Ci\u003EATYPICAL CYS HIS RICH THIOREDOXIN\u003C\u002Fi\u003E, \u003Ci\u003EACHT5\u003C\u002Fi\u003E; \u003Ci\u003EABSCISIC ACID 8’-HYDROXYLASE\u003C\u002Fi\u003E, \u003Ci\u003ECYP707A3\u003C\u002Fi\u003E; \u003Ci\u003EFAR-RED-ELONGATED HYPOCOTYL1-LIKE PROTEIN\u003C\u002Fi\u003E, \u003Ci\u003EFHL\u003C\u002Fi\u003E, and a RING\u002FU-box superfamily protein, \u003Ci\u003EAT5G42200\u003C\u002Fi\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EInterestingly, there was also an overlap of hypoxia-down-regulated genes between Arabidopsis and rapeseed (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, column P; \u003Ca href=\"#S10\"\u003ESupplementary Table 4\u003C\u002Fa\u003E), for example several genes coding for invertase\u002Fpectin methylesterase inhibitor superfamily proteins, nodulin MtN21\u002FEamA-like transporter family proteins (\u003Ci\u003EUMAMIT12\u003C\u002Fi\u003E, \u003Ci\u003EUMAMIT17\u003C\u002Fi\u003E), as well as several genes coding for biosynthesis enzymes (e.g., 3-ketoacyl-CoA synthase 20, \u003Ci\u003EKCS20\u003C\u002Fi\u003E; cytochrome P450 family proteins \u003Ci\u003ECYP83B1\u003C\u002Fi\u003E, \u003Ci\u003ECYP82F1\u003C\u002Fi\u003E, \u003Ci\u003ECYP79B2\u003C\u002Fi\u003E; Galactose mutarotase-like superfamily protein).\u003C\u002Fp\u003E\r\n\u003Ch3\u003ETranscriptional Changes of Roots in Primary Metabolism, Plant Hormones and Starvation-Responses\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb15\"\u003EThe functional categorization by use of GO terms (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E) suggested a transcriptional response of several pathways to root-zone hypoxia, including primary metabolism and hormone-associated pathways. This let us to have a deeper look into specific pathways. In primary metabolism, the expression of many genes coding for enzymes in glycolysis and fermentation were up-regulated, including hexokinase, phosphofructokinase and aldolase (\u003Ca href=\"#S10\"\u003ESupplementary Table 5\u003C\u002Fa\u003E). For sucrolysis, sucrose-synthase-coding genes were induced, while invertase-like genes were reduced in their expression. Pyruvate dehydrogenase, TCA-cycle enzymes and enzymes for the pentose-phosphate cycle were not modified in expression or even down-regulated. Interestingly, some alternative enzymes were significantly induced in Avatar at the transcript level after 4 h of hypoxia, namely \u003Ci\u003EISOCITRATE LYASE\u003C\u002Fi\u003E from the glyoxylate cycle, and \u003Ci\u003EPYRUVATE ORTHOPHOSPHATE DIKINASE\u003C\u002Fi\u003E (\u003Ci\u003EPPDK\u003C\u002Fi\u003E) from gluconeogenesis. Among genes coding for nitrogen metabolism, several aminotransferases were induced in both cultivars, for example isoforms for \u003Ci\u003EAlaAT1\u003C\u002Fi\u003E and \u003Ci\u003EASPARTATE AMINOTRANSFERASE 2\u003C\u002Fi\u003E (\u003Ci\u003EAspAT2\u003C\u002Fi\u003E) (\u003Ca href=\"#S10\"\u003ESupplementary Table 5\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EPlant hormone biosynthesis and signaling were also among the enriched GO categories within the differentially expressed genes in roots under hypoxia (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E). While auxin biosynthesis was not clearly modified, several polar auxin transporters were negatively affected after 4 h of hypoxia. Despite this, several members of the SAUR-like auxin-responsive protein family were differentially expressed, but with no clear trend (\u003Ca href=\"#S10\"\u003ESupplementary Table 6\u003C\u002Fa\u003E). Cytokinin biosynthesis and signaling were in tendency negatively affected by root hypoxia (\u003Ca href=\"#S10\"\u003ESupplementary Tables 3\u003C\u002Fa\u003E, \u003Ca href=\"#S10\"\u003E6\u003C\u002Fa\u003E), with the exception of the HPt factor gene \u003Ci\u003EHPT PHOSPHOTRANSMITTER 4\u003C\u002Fi\u003E (\u003Ci\u003EAHP4\u003C\u002Fi\u003E), whose expression was strongly induced after 4 and 24 h of hypoxia. In gibberellin metabolism, some genes coding for enzymes involved in biosynthesis and degradation were differentially expressed, but the respective GO terms were not enriched. Signaling related to this group of plant hormones was not affected by hypoxia (\u003Ca href=\"#S10\"\u003ESupplementary Tables 3\u003C\u002Fa\u003E, \u003Ca href=\"#S10\"\u003E6\u003C\u002Fa\u003E). Brassinosteroid biosynthesis, on the other hand, was negatively regulated by hypoxia.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EAmong the stress-related hormones, there was a strong enrichment of genes responding to either ethylene or abscisic acid (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E). However, while neither abscisic acid biosynthesis nor degradation was strongly affected by the stress, genes coding for biosynthetic enzymes in ethylene production were induced upon hypoxia (\u003Ci\u003E1-AMINO-CYCLOPROPANE-1-CARBOXYLATE SYNTHASE 2\u003C\u002Fi\u003E and \u003Ci\u003E1-AMINO-CYCLOPROPANE-1-CARBOXYLATE OXIDASE 1\u003C\u002Fi\u003E, \u003Ca href=\"#S10\"\u003ESupplementary Table 6\u003C\u002Fa\u003E). Several genes coding for different steps of jasmonic acid biosynthesis and signal transduction were induced especially after 4 h of root hypoxia, and parts of the salicylic acid signal transduction were induced after 4 and 24 h of hypoxia (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EPreviously we have shown that submerged leaves of \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E showed a strong starvation response (\u003Ca href=\"#B73\"\u003EWittig et al., 2021\u003C\u002Fa\u003E). We therefore compared the present dataset to the starvation-responsive genes of Arabidopsis (\u003Ca href=\"#B68\"\u003EUsadel et al., 2008\u003C\u002Fa\u003E; \u003Ca href=\"#B15\"\u003ECookson et al., 2016\u003C\u002Fa\u003E). Indeed, there was an enrichment of starvation-induced genes (\u003Ca href=\"#S10\"\u003ESupplementary Table 4\u003C\u002Fa\u003E), although less pronounced than under submergence, and affecting different genes. Among starvation-responsive genes in roots under hypoxia, the following transcripts were found: \u003Ci\u003ECHY-type\u002FCTCHY-type\u002FRING-type ZINC FINGER PROTEIN\u003C\u002Fi\u003E (\u003Ci\u003EAT5G22920\u003C\u002Fi\u003E), Eukaryotic aspartyl protease family protein (\u003Ci\u003EAT5G19120\u003C\u002Fi\u003E), \u003Ci\u003EGLUTAMINE-DEPENDENT ASPARAGINE SYNTHASE 1\u003C\u002Fi\u003E (\u003Ci\u003EASN1\u003C\u002Fi\u003E), and \u003Ci\u003EMATERNAL EFFECT EMBRYO ARREST 14\u003C\u002Fi\u003E (\u003Ci\u003EMEE14\u003C\u002Fi\u003E) (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns R to AD).\u003C\u002Fp\u003E\r\n\u003Ch3\u003EBiochemical Modifications in Response to Root-Zone Hypoxia\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb0\"\u003EThe transcriptional data suggest an induction of transcripts coding for fermentative enzymes (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns R to AD, \u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E). In order to analyze whether these transcriptional changes translate into an enhanced activity of fermentative enzymes, we measured the activity of ADH after hypoxic treatment in the root zone. After 4 and 24 h we did not observe any significant increase in ADH activity (\u003Ca href=\"#S10\"\u003ESupplementary Figure 3\u003C\u002Fa\u003E). However, after 3 days of stress, a strong and significant induction of ADH activity was observed in roots of both cultivars, Avatar and Zhongshuang 9, although no differences were detected between the genotypes (\u003Ca href=\"#F3\"\u003EFigure 3\u003C\u002Fa\u003E). This indicates a strong hypoxia response also at the protein level, albeit with a delay in comparison to the transcriptional changes.\u003C\u002Fp\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"Imageheaders\"\u003EFIGURE 3\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"FigureDesc\"\u003E\r\n\u003Ca href=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_m\u002Ffpls-13-897673-g003.jpg\" name=\"figure3\" target=\"_blank\"\u003E\r\n\u003Cimg src=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_t\u002Ffpls-13-897673-g003.gif\" id=\"F3\" alt=\"www.frontiersin.org\" \u002F\u003E\u003C\u002Fa\u003E\r\n\u003Cp\u003E\u003Cstrong\u003EFigure 3.\u003C\u002Fstrong\u003E ADH activity [nmol * mg prot\u003Csup\u003E–1\u003C\u002Fsup\u003E * min\u003Csup\u003E–1\u003C\u002Fsup\u003E] in roots of two \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E cultivars (Avatar, Zhongshuang 9) in hydroponics after 3 days of root hypoxia, compared with aerated controls. At time of harvest, plants were 18 days old. Data are means ± SD of 4 to 5 replicates. Different letters indicate significant differences (ANOVA and Tukey \u003Ci\u003Epost hoc\u003C\u002Fi\u003E test, \u003Ci\u003Ep\u003C\u002Fi\u003E < 0.05).\u003C\u002Fp\u003E\r\n\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"clear\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cp class=\"mb15 w100pc float_left mt15\"\u003ESeveral starvation-responsive genes were among the hypoxia-induced genes in roots after 4 and 24 h (\u003Ca href=\"#S10\"\u003ESupplementary Table 2, columns M and N\u003C\u002Fa\u003E), but the enrichment was much lower (\u003Ca href=\"#S10\"\u003ESupplementary Table 4\u003C\u002Fa\u003E) than in our previous study on complete submergence. Therefore, the carbohydrate content in roots and leaves was measured after both time points. Interestingly, leaf sugar content did not significantly differ between aeration and root hypoxia, and between genotypes (\u003Ca href=\"#F4\"\u003EFigure 4A\u003C\u002Fa\u003E). There was a slightly lower level of carbohydrates at the 24-h-time point for stress and control samples, since these plants had only 2 h of light after the 16-h-night, while the plants from the 4-h-time point had 6 h of light.\u003C\u002Fp\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"Imageheaders\"\u003EFIGURE 4\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"FigureDesc\"\u003E\r\n\u003Ca href=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_m\u002Ffpls-13-897673-g004.jpg\" name=\"figure4\" target=\"_blank\"\u003E\r\n\u003Cimg src=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_t\u002Ffpls-13-897673-g004.gif\" id=\"F4\" alt=\"www.frontiersin.org\" \u002F\u003E\u003C\u002Fa\u003E\r\n\u003Cp\u003E\u003Cstrong\u003EFigure 4.\u003C\u002Fstrong\u003E Content of carbohydrates [μmol * g FW\u003Csup\u003E–1\u003C\u002Fsup\u003E] in leaves \u003Cb\u003E(A)\u003C\u002Fb\u003E and roots \u003Cb\u003E(B)\u003C\u002Fb\u003E of two \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E cultivars (Avatar, Zhongshuang 9) in hydroponics after 4 and 24 h of root hypoxia, compared with aerated controls. At time of start of stress, plants were 15 days old. Data are means ± SD of 5 replicates. Different letters indicate significant differences for the sum of sugars (ANOVA and Tukey \u003Ci\u003Epost hoc\u003C\u002Fi\u003E test, \u003Ci\u003Ep\u003C\u002Fi\u003E < 0.05). n.s., ANOVA was not significant; *, significant compared with respective control (\u003Ci\u003ET\u003C\u002Fi\u003E-Test, \u003Ci\u003Ep\u003C\u002Fi\u003E < 0.05).\u003C\u002Fp\u003E\r\n\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"clear\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cp class=\"mb15 w100pc float_left mt15\"\u003EIn roots, carbohydrate levels, especially starch, were lower than in leaves under both control and stressed conditions (\u003Ca href=\"#F4\"\u003EFigure 4B\u003C\u002Fa\u003E). In this case, a tendency of higher sugar contents after stress treatment was observed, which was only significant for sucrose. Again, there was no difference between the genotypes. Sugar starvation due to lower sugar content can therefore be excluded. However, the transcriptomic data still suggest a starvation response (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns M and N). This could be a hint that carbohydrates were not fully available for the plant cells and their metabolism. This assumed lower consumption rate could be an explanation for the observed slight rise in sugar levels in roots.\u003C\u002Fp\u003E\r\n\u003Ch3\u003EComparison to Previous Rapeseed Transcriptome Analyses Under Flooding-Related Stress Treatments\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb15\"\u003ETwo datasets from roots of \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E plants stressed with waterlogging for 12 h have been published already (\u003Ca href=\"#B78\"\u003EZou et al., 2013a\u003C\u002Fa\u003E,\u003Ca href=\"#B81\"\u003E2015\u003C\u002Fa\u003E). In contrast to our study, the plants were grown in pots with sand and treated with waterlogging. Although this dataset is somewhat incomplete due to the missing reference genome at the time of publication, there is a good agreement with our dataset (\u003Ca href=\"#S10\"\u003ESupplementary Figure 4\u003C\u002Fa\u003E and \u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns AZ to BL). About 636 and 234 transcripts were hypoxia-responsive after 4 and 24 h in the present study and were also responsive to 6 and 12 h of waterlogging. The overlap with down-regulated genes was 222 and 89 transcripts for 4 and 24 h of hypoxia. The high number of genes only found in our dataset might be due to the different mapping basis, and probably not due to strong differences in expression (\u003Ca href=\"#S10\"\u003ESupplementary Figure 4\u003C\u002Fa\u003E compared with \u003Ca href=\"#S10\"\u003ESupplementary Figure 5\u003C\u002Fa\u003E). Indeed, 45 and 42 HRG homologs were also induced by waterlogging of Zhongshuang 9 and GH01, respectively (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, column Q).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EAnother two rapeseed datasets have been obtained from about 2- to 3-day-old seedlings that were fully submerged for 12 or 6 h (\u003Ca href=\"#B24\"\u003EGuo et al., 2020\u003C\u002Fa\u003E; \u003Ca href=\"#B41\"\u003ELi et al., 2021\u003C\u002Fa\u003E), whose gene expression was based on the reference genome sequence Darmor (\u003Ca href=\"#B13\"\u003EChalhoub et al., 2014\u003C\u002Fa\u003E). Again, there was a good agreement of gene expression data in comparison with the expression data from roots from our dataset, despite of the different developmental stages and treatment conditions (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns BM to BT, \u003Ca href=\"#S10\"\u003ESupplementary Table 7A\u003C\u002Fa\u003E). This similarity in gene expression was observed for up- and down-regulated genes and allowed for the definition of a \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E hypoxic core response gene set (BnHRGs) containing 131 commonly up-regulated genes (\u003Ca href=\"#S10\"\u003ESupplementary Table 7B\u003C\u002Fa\u003E) and 163 commonly down-regulated genes (\u003Ca href=\"#S10\"\u003ESupplementary Table 7C\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Ch3\u003EThe Leaf Response Is Less Pronounced If Only Roots Are Affected by Hypoxia\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb15\"\u003EIn leaves, only a small number of genes was induced by root hypoxia, with little overlap between the two cultivars (\u003Ca href=\"#F1\"\u003EFigure 1\u003C\u002Fa\u003E). The most enriched GO terms for Avatar were “2-(2′-methylthio)ethylmalate synthase activity” and “response to insect”, while for Zhongshuang 9 the categories “cation transmembrane transporter activity” (including zinc and iron) and “cellular response to heat” were enriched. Among the down-regulated genes, there was more functional overlap, including the categories “RNA methylation” and further ribosome-related categories as well as “cell wall” (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EIn leaves, there was no induction of HRGs (\u003Ca href=\"#S10\"\u003ESupplementary Figure 2\u003C\u002Fa\u003E and \u003Ca href=\"#S10\"\u003ESupplementary Table 4\u003C\u002Fa\u003E) and no enrichment of GO categories associated with hypoxia (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E). This does not come as a surprise, since the leaves were still in an aerobic atmosphere and with ongoing photosynthesis. The overlap with the starvation response of Arabidopsis (\u003Ca href=\"#B68\"\u003EUsadel et al., 2008\u003C\u002Fa\u003E; \u003Ca href=\"#B15\"\u003ECookson et al., 2016\u003C\u002Fa\u003E), as previously observed in submerged rapeseed leaves (\u003Ca href=\"#B73\"\u003EWittig et al., 2021\u003C\u002Fa\u003E), was much lower in this dataset (\u003Ca href=\"#S10\"\u003ESupplementary Table 4\u003C\u002Fa\u003E). There was also no indication for a modification of primary metabolism or photosynthesis due to root hypoxia (\u003Ca href=\"#S10\"\u003ESupplementary Table 5\u003C\u002Fa\u003E), with the exception of one gene, PAD4, coding for an \u003Ci\u003EALANINE:GLYOXYLATE AMINOTRANSFERASE\u003C\u002Fi\u003E (\u003Ca href=\"#B58\"\u003EParthasarathy et al., 2019\u003C\u002Fa\u003E), which was induced in leaves of the cultivar Avatar. At the 24-h-time point, there was no clear evidence for a drought response in leaves as a consequence of root damages under the stress (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E). Besides the enhanced expression of the cytokinin signaling component \u003Ci\u003EAHP4\u003C\u002Fi\u003E, no hormone-related transcripts were differentially expressed in leaves of plants with hypoxic roots (\u003Ca href=\"#S10\"\u003ESupplementary Table 6\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EWhen we compared the new data to our previous analysis under submergence (\u003Ca href=\"#B73\"\u003EWittig et al., 2021\u003C\u002Fa\u003E), there was hardly any overlap between submerged leaves and leaves from plants with hypoxic roots (\u003Ca href=\"#S10\"\u003ESupplementary Figure 6\u003C\u002Fa\u003E). Interestingly, the stressed roots after 24 h shared more induced or reduced transcripts with submerged leaves than the leaves from the two experiments (\u003Ca href=\"#S10\"\u003ESupplementary Figure 6\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Ch3\u003EAre There Differences in Gene Expression Between the Two Genotypes?\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb15\"\u003EThis analysis was done with two genotypes of \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E, one European winter type (Avatar) and one Asian semi-winter type with a previously described high flooding tolerance (Zhongshuang 9, e.g., \u003Ca href=\"#B79\"\u003EZou et al., 2013b\u003C\u002Fa\u003E,\u003Ca href=\"#B80\"\u003E2014\u003C\u002Fa\u003E). As mentioned above, the general response of roots to hypoxia was very similar between the two genotypes (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns R to AD, \u003Ca href=\"#S10\"\u003ESupplementary Table 4\u003C\u002Fa\u003E and \u003Ca href=\"#F1\"\u003EFigure 1\u003C\u002Fa\u003E). There were only small differences at certain time points, and a statistical analysis using a complex comparison revealed no clear signatures (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns AR to AX). Also, the GO analysis of these complex comparisons did only show small differences, for example a stronger reduction of “xylosyltransferase activity” in Avatar (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E). The observed differences might rather be due to differential expression of certain isoforms, while the overall transcript levels of a gene function were rather similar. Indeed, due to genome triplication and its tetraploid status (\u003Ca href=\"#B55\"\u003ENikolov and Tsiantis, 2017\u003C\u002Fa\u003E), rapeseed may contain up to 6 genes for a gene from Arabidopsis.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EHowever, there were general differences in expression between both genotypes, independent of the stress treatment (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns AE to AQ, \u003Ca href=\"#S10\"\u003ESupplementary Figure 7\u003C\u002Fa\u003E). These genotype-specific differences were similar to those observed before for submerged leaves (\u003Ca href=\"#B73\"\u003EWittig et al., 2021\u003C\u002Fa\u003E). In all root samples, about 2,900 transcripts were higher expressed in Avatar, while about 1,000 transcripts were higher in Zhongshuang 9. The difference in numbers might be partially caused by the difference in mapping rates between the two genotypes (\u003Ca href=\"#S10\"\u003ESupplementary Table 1\u003C\u002Fa\u003E). A functional analysis classified the differentially expressed genes into certain categories, but there were only a few GOs enriched in our dataset (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E). This suggests that gene copies, but not gene functions are differentially expressed between genotypes. Functional categories with higher expression levels in Avatar were enriched in ribosome function and translation, while in Zhongshuang 9 a few transport categories were enriched. Similar observations were made for leaves.\u003C\u002Fp\u003E\r\n\u003Ch3\u003EIs There a Difference in Waterlogging Tolerance Between Both Cultivars?\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb0\"\u003EThe transcriptional and biochemical analysis did not reveal obvious differences between the two rapeseed cultivars upon treatment with hypoxia in the root zone. We therefore asked whether differences exist in long-term response to hypoxia and waterlogging. First, we used the hydroponics system for a long-term gassing of plants with nitrogen in the root zone. After 7 days of treatment, plants were harvested, and fresh weight was determined (\u003Ca href=\"#F5\"\u003EFigure 5\u003C\u002Fa\u003E). The treatment caused growth retardation of the plants, resulting in significantly lowered root and shoot fresh weights. Interestingly, there was also a slight decrease in the ratio of fresh weight to dry weight (\u003Ca href=\"#S10\"\u003ESupplementary Figure 8A\u003C\u002Fa\u003E) indicating a slight drought due to root damages under prolonged root hypoxia. However, there were no differences between the two cultivars. Potentially, the treatment duration was too short, but the hydroponic system was not suitable for longer stress treatments. Furthermore, it might not perfectly mimic the situation in soil, or in agriculture.\u003C\u002Fp\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"Imageheaders\"\u003EFIGURE 5\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"FigureDesc\"\u003E\r\n\u003Ca href=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_m\u002Ffpls-13-897673-g005.jpg\" name=\"figure5\" target=\"_blank\"\u003E\r\n\u003Cimg src=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_t\u002Ffpls-13-897673-g005.gif\" id=\"F5\" alt=\"www.frontiersin.org\" \u002F\u003E\u003C\u002Fa\u003E\r\n\u003Cp\u003E\u003Cstrong\u003EFigure 5.\u003C\u002Fstrong\u003E Fresh weight of shoots \u003Cb\u003E(A)\u003C\u002Fb\u003E and roots \u003Cb\u003E(B)\u003C\u002Fb\u003E of two \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E cultivars (Avatar, Zhongshuang 9) in hydroponics after 7 days of root hypoxia, compared with aerated controls. At time of harvest, plants were 22 days old. Data are means ± SD of 4 experiments with 7-10 plants per experiment (\u003Ci\u003En\u003C\u002Fi\u003E = 34 – 40). Different letters indicate significant differences (ANOVA and Tukey \u003Ci\u003Epost hoc\u003C\u002Fi\u003E test, \u003Ci\u003Ep\u003C\u002Fi\u003E < 0.05).\u003C\u002Fp\u003E\r\n\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"clear\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cp class=\"mb15 w100pc float_left mt15\"\u003ETherefore, a more natural system was used, rapeseed plants grown on soil. After 15 days of growth on normoxic soil, plants were treated with waterlogging in the root zone. This treatment was done for 14 days. To evaluate fitness at an early timepoint in a non-invasive manner, a chlorophyll fluorescence parameter, the effective quantum yield of PSII (ΦPSII), was determined. This value slightly increased after 6 days of waterlogging in both genotypes (\u003Ca href=\"#F6\"\u003EFigure 6B\u003C\u002Fa\u003E). Overall, the ΦPSII values for Zhongshuang 9 were slightly smaller than the values for Avatar, but the trend between control and stress treatment was the same. After 14 days of stress, the differences in ΦPSII between control and stress were no longer significant. The fresh weight in this experimental set-up significantly decreased under waterlogging, as shown in the hydroponic system (\u003Ca href=\"#F6\"\u003EFigure 6A\u003C\u002Fa\u003E), but the changes were not as severe as expected. Again, no differences between the genotypes were found.\u003C\u002Fp\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"Imageheaders\"\u003EFIGURE 6\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"FigureDesc\"\u003E\r\n\u003Ca href=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_m\u002Ffpls-13-897673-g006.jpg\" name=\"figure6\" target=\"_blank\"\u003E\r\n\u003Cimg src=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_t\u002Ffpls-13-897673-g006.gif\" id=\"F6\" alt=\"www.frontiersin.org\" \u002F\u003E\u003C\u002Fa\u003E\r\n\u003Cp\u003E\u003Cstrong\u003EFigure 6.\u003C\u002Fstrong\u003E Performance of two \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E cultivars (Avatar, Zhongshuang 9) on soil under waterlogging with tap water (“WL”) for up to 14 days. At time of harvest, plants were 29 days old. \u003Cb\u003E(A)\u003C\u002Fb\u003E Fresh weight of shoots after 14 days of stress treatment compared with controls. Data are means ± SD of 3 experiments with 10 plants per experiment (n = 30). \u003Cb\u003E(B)\u003C\u002Fb\u003E chlorophyll fluorescence (ΦPSII) after 6 and 14 days of stress treatment compared with controls. Data are means ± SD of 3 experiments with 10 plants per experiment (\u003Ci\u003En\u003C\u002Fi\u003E = 30). \u003Cb\u003E(C)\u003C\u002Fb\u003E Content of carbohydrates [μmol * g FW\u003Csup\u003E–1\u003C\u002Fsup\u003E] in leaves of after 14 days of stress. Data are means ± SD of 2 experiments with 6 plants per experiment (\u003Ci\u003En\u003C\u002Fi\u003E = 12). \u003Cb\u003E(D)\u003C\u002Fb\u003E Chlorophyll content [mg * g FW\u003Csup\u003E–1\u003C\u002Fsup\u003E] in leaves of after 14 days of stress. Data are means ± SD of 2 experiments with 8 plants per experiment (n = 16). Different letters indicate significant differences (ANOVA and Tukey \u003Ci\u003Epost hoc\u003C\u002Fi\u003E test, \u003Ci\u003Ep\u003C\u002Fi\u003E < 0.05). n.s., not significant.\u003C\u002Fp\u003E\r\n\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"clear\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cp class=\"mb15 w100pc float_left mt15\"\u003ETwo additional parameters were analyzed in this system, in order to reveal any effect of the modified stress system on the plant carbohydrate and pigment system. As shown for the short-term hydroponics system (\u003Ca href=\"#F4\"\u003EFigure 4\u003C\u002Fa\u003E), the carbohydrate content of leaves from plants under waterlogging in soil did not respond to the stress treatment, even after 14 days of stress (\u003Ca href=\"#F6\"\u003EFigure 6C\u003C\u002Fa\u003E). The chlorophyll content showed a tendency to decrease after stress treatment, but no significant differences between the two genotypes were observed (\u003Ca href=\"#F6\"\u003EFigure 6D\u003C\u002Fa\u003E). These results suggest that waterlogging on soil in a controlled growth chamber might not be as severe as natural waterlogging in agriculture.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EIn order to establish a more natural system, we came across a waterlogging system with a starch solution that may cause a lower soil redox potential for plants grown in pots in climate chambers, which was successfully used for barley (\u003Ca href=\"#B44\"\u003EMano and Takeda, 2012\u003C\u002Fa\u003E; \u003Ca href=\"#B46\"\u003EMiricescu et al., 2021\u003C\u002Fa\u003E). Strikingly, the waterlogging with a 0.1% starch solution strongly enhanced the severity of the stress treatment in comparison to waterlogging in distilled water (\u003Ca href=\"#F7\"\u003EFigure 7\u003C\u002Fa\u003E and \u003Ca href=\"#S10\"\u003ESupplementary Figure 9\u003C\u002Fa\u003E) or in tap water (\u003Ca href=\"#F6\"\u003EFigure 6\u003C\u002Fa\u003E). Here, the fresh weight of aboveground organs of stressed plants was reduced to 30% of the control plants, while in distilled water it was only reduced to 90% (\u003Ca href=\"#F7\"\u003EFigure 7A\u003C\u002Fa\u003E), and in tap water to about 70% (\u003Ca href=\"#F6\"\u003EFigure 6A\u003C\u002Fa\u003E). There were also indications for a stronger drought stress when waterlogging was done in starch solution since the ratio of fresh weight to dry weight was severely reduced (\u003Ca href=\"#S10\"\u003ESupplementary Figure 8B\u003C\u002Fa\u003E). The analysis of chlorophyll fluorescence (ΦPSII) showed little changes after 7 days of stress, but a significant decrease after 14 days of waterlogging in a starch solution (\u003Ca href=\"#F7\"\u003EFigure 7C\u003C\u002Fa\u003E). For chlorophyll, estimated here with a non-invasive method, we did not observe clear differences after 14 days of stress (\u003Ca href=\"#F7\"\u003EFigure 7D\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"Imageheaders\"\u003EFIGURE 7\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"FigureDesc\"\u003E\r\n\u003Ca href=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_m\u002Ffpls-13-897673-g007.jpg\" name=\"figure7\" target=\"_blank\"\u003E\r\n\u003Cimg src=\"https:\u002F\u002Fwww.frontiersin.org\u002Ffiles\u002FArticles\u002F897673\u002Ffpls-13-897673-HTML\u002Fimage_t\u002Ffpls-13-897673-g007.gif\" id=\"F7\" alt=\"www.frontiersin.org\" \u002F\u003E\u003C\u002Fa\u003E\r\n\u003Cp\u003E\u003Cstrong\u003EFigure 7.\u003C\u002Fstrong\u003E Performance of two \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E cultivars (Avatar, Zhongshuang 9) on soil under waterlogging with a 0.1% starch solution (“starch”) or with distilled water (“WL”) for up to 14 days. At time of harvest, plants were 29 days old. \u003Cb\u003E(A)\u003C\u002Fb\u003E Fresh weight of shoots after 14 days of stress treatment compared with controls. \u003Cb\u003E(B)\u003C\u002Fb\u003E Chlorophyll fluorescence (ΦPSII) after 7 and 14 days of stress treatment compared with controls. \u003Cb\u003E(C)\u003C\u002Fb\u003E Chlorophyll content [μmol * m\u003Csup\u003E–2\u003C\u002Fsup\u003E] in leaves of after 7 and 14 days of stress. Data are means ± SD of 3 experiments with 6 plants per experiment (\u003Ci\u003En\u003C\u002Fi\u003E = 18). Different letters indicate significant differences (ANOVA and Tukey \u003Ci\u003Epost hoc\u003C\u002Fi\u003E test, \u003Ci\u003Ep\u003C\u002Fi\u003E < 0.05).\u003C\u002Fp\u003E\r\n\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"clear\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"DottedLine\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cp class=\"mb15 w100pc float_left mt15\"\u003EIn order to determine the causal reasons for these strong differences in plant growth, we also obtained chemical parameters of the waterlogging solutions in the two variants. While waterlogging with distilled water only resulted in mild decreases in oxygen content, starting at day 9, the oxygen content strongly decreased within the first 24 h of waterlogging in the starch solution, and remained at this low level for at least 10 days (\u003Ca href=\"#S10\"\u003ESupplementary Figure 10A\u003C\u002Fa\u003E). Subsequently, the oxidation-reduction potential (ORP) decreased after 2 and 3 days of waterlogging with starch solution, but it remained relatively high in distilled water (\u003Ca href=\"#S10\"\u003ESupplementary Figure 10B\u003C\u002Fa\u003E). The increase in both oxygen and ORP after 10 days of waterlogging might suggest a partial recovery of the system due to exhaustion of starch. The pH value temporarily decreased in the waterlogging treatment with starch (\u003Ca href=\"#S10\"\u003ESupplementary Figure 10C\u003C\u002Fa\u003E), while the conductivity increased with time in both variants, with a slightly stronger increase in starch solution (\u003Ca href=\"#S10\"\u003ESupplementary Figure 10D\u003C\u002Fa\u003E). The latter could be due to enhanced root death and subsequent release of ions into the solution.\u003C\u002Fp\u003E\r\n\u003Ca id=\"h5\" name=\"h5\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003EDiscussion\u003C\u002Fh2\u003E\r\n\u003Ch3 class=\"pt0\"\u003E\u003Ci\u003EBrassica napus\u003C\u002Fi\u003E Roots Strongly Respond to Hypoxia\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb15\"\u003EThe oil crop plant \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E is described to be very sensitive to soil waterlogging (\u003Ca href=\"#B80\"\u003EZou et al., 2014\u003C\u002Fa\u003E). It is not able to form aerenchyma in its roots as part of an avoidance strategy (\u003Ca href=\"#B70\"\u003EVoesenek et al., 1999\u003C\u002Fa\u003E; \u003Ca href=\"#B60\"\u003EPloschuk et al., 2018\u003C\u002Fa\u003E), and will therefore experience hypoxia inside root tissues under waterlogging. We were therefore interested in its transcriptional response to this aspect of waterlogging stress to estimate whether rapeseed was able to induce biochemical acclimations as part of the tolerance strategy. After 4 and 24 h of root hypoxia, a high number of genes was differentially expressed in both cultivars compared to aerated controls (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns R to AD and \u003Ca href=\"#F1\"\u003EFigure 1\u003C\u002Fa\u003E). More transcripts were down-regulated than up-regulated.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EThe functional analysis of up-regulated genes revealed the induction of a strong hypoxia response, as indicated by the enrichment of hypoxia-associated GO terms (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E). Furthermore, there was a significant overlap with hypoxia-induced genes in Arabidopsis in general as well as with the hypoxia core response genes (HRGs, \u003Ca href=\"#B54\"\u003EMustroph et al., 2009\u003C\u002Fa\u003E; \u003Ca href=\"#F2\"\u003EFigure 2\u003C\u002Fa\u003E and \u003Ca href=\"#S10\"\u003ESupplementary Figure 2\u003C\u002Fa\u003E, \u003Ca href=\"#S10\"\u003ESupplementary Table 4\u003C\u002Fa\u003E). Among the hypoxia-induced genes were transcripts coding for fermentative enzymes (\u003Ci\u003EADH1\u003C\u002Fi\u003E, \u003Ci\u003EPDC1\u003C\u002Fi\u003E, \u003Ci\u003EPDC3\u003C\u002Fi\u003E), glycolytic enzymes (\u003Ci\u003ESUS1\u003C\u002Fi\u003E, \u003Ci\u003EFRK2\u003C\u002Fi\u003E, \u003Ci\u003EPFK3\u003C\u002Fi\u003E, \u003Ci\u003EPFK6\u003C\u002Fi\u003E, \u003Ci\u003EFBA6\u003C\u002Fi\u003E) as well as transcriptional regulators (\u003Ci\u003EHRE1\u003C\u002Fi\u003E, \u003Ci\u003EHRE2\u003C\u002Fi\u003E, \u003Ci\u003EHRA1\u003C\u002Fi\u003E, \u003Ci\u003ELBD41\u003C\u002Fi\u003E). Both plant species are rather sensitive to waterlogging stress, and it remains to be evaluated whether differences in tolerance exist between the two species.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EGlycolysis and fermentation are important processes to maintain energy balance under hypoxia since mitochondrial respiration is strongly inhibited. Their induction is therefore an essential component of the tolerance to low-oxygen stress. As Arabidopsis, also rapeseed was able to induce the expression of the associated genes under root hypoxia (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns R to AD), which may also result in higher enzyme activities as shown here for the ADH activity during prolonged stress treatment (\u003Ca href=\"#F3\"\u003EFigure 3\u003C\u002Fa\u003E), and therefore might hint at an acclimation response of rapeseed plants. Mutants with a defect in fermentative enzymes indeed showed a lower tolerance to flooding-related stresses, for example in rice (\u003Ca href=\"#B63\"\u003ESaika et al., 2006\u003C\u002Fa\u003E; \u003Ca href=\"#B66\"\u003ETakahashi et al., 2014\u003C\u002Fa\u003E), maize (\u003Ca href=\"#B65\"\u003ESchwartz, 1969\u003C\u002Fa\u003E; \u003Ca href=\"#B30\"\u003EJohnson et al., 1994\u003C\u002Fa\u003E) or Arabidopsis (\u003Ca href=\"#B29\"\u003EJacobs et al., 1988\u003C\u002Fa\u003E; \u003Ca href=\"#B28\"\u003EIsmond et al., 2003\u003C\u002Fa\u003E). Interestingly, the proposed enhancement of glycolysis and fermentation does not cause a carbohydrate limitation in our system (\u003Ca href=\"#F4\"\u003EFigure 4\u003C\u002Fa\u003E), most likely due to ongoing photosynthesis in the leaves.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EIn addition, many plant species induced enzymes with alternative energy requirements upon hypoxia treatment, mainly sucrose synthase, the pyrophosphate-dependent phosphofructokinases (PFP) as well as PPDK (\u003Ca href=\"#B27\"\u003EHuang et al., 2008\u003C\u002Fa\u003E; \u003Ca href=\"#B51\"\u003EMustroph et al., 2014\u003C\u002Fa\u003E, \u003Ca href=\"#B53\"\u003E2018\u003C\u002Fa\u003E; \u003Ca href=\"#B4\"\u003EAtwell et al., 2015\u003C\u002Fa\u003E). Interestingly and unlike Arabidopsis (\u003Ca href=\"#B54\"\u003EMustroph et al., 2009\u003C\u002Fa\u003E), rapeseed induced two genes coding for the PFP alpha subunit in hypoxic roots, and this induction was stronger after 4 than after 24 h. This might be a hint for an alternative energy usage in \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E. Several transcripts coding for PPDK and SUS are also among the hypoxia-induced genes in rapeseed (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns R to AD, \u003Ca href=\"#S10\"\u003ESupplementary Table 5\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EAmong transcriptional regulators, the function of LBD41 is still unclear, but it is commonly induced by hypoxia in many plant species (\u003Ca href=\"#B52\"\u003EMustroph et al., 2010\u003C\u002Fa\u003E; \u003Ca href=\"#B18\"\u003EGasch et al., 2016\u003C\u002Fa\u003E). HRE1 and HRE2 are members of the group VII ERFs, which are important regulators of the hypoxia-specific transcription (\u003Ca href=\"#B21\"\u003EGibbs et al., 2011\u003C\u002Fa\u003E; \u003Ca href=\"#B42\"\u003ELicausi et al., 2011\u003C\u002Fa\u003E). Both proteins are probably not involved in the initial response to hypoxia (\u003Ca href=\"#B18\"\u003EGasch et al., 2016\u003C\u002Fa\u003E), but most likely in the later stages of hypoxia (\u003Ca href=\"#B43\"\u003ELicausi et al., 2010\u003C\u002Fa\u003E). HRA1 has been described as a negative regulator of hypoxia-specific transcription (\u003Ca href=\"#B22\"\u003EGiuntoli et al., 2014\u003C\u002Fa\u003E, \u003Ca href=\"#B23\"\u003E2017\u003C\u002Fa\u003E). The transcriptional regulation of the hypoxic response in rapeseed might therefore be very similar to Arabidopsis.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EAmong the genes with reduced expression under hypoxia there are many whose products are involved in biosynthetic processes such as sterol, xylan and suberin biosynthesis, and in growth-related GO terms such as DNA replication, cell wall and cell proliferation (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E). This is not surprising since it has been previously suggested that the hypoxia acclimation strategy includes down-regulation of growth and biosynthesis in Arabidopsis (\u003Ca href=\"#B10\"\u003EBranco-Price et al., 2008\u003C\u002Fa\u003E; \u003Ca href=\"#B54\"\u003EMustroph et al., 2009\u003C\u002Fa\u003E). In accordance, growth of rapeseed plants is reduced under root hypoxia (\u003Ca href=\"#F5\"\u003EFigure 5\u003C\u002Fa\u003E). Moreover, the low-oxygen quiescence strategy is a response of certain rice cultivars that show enhanced survival under relatively deep floods (\u003Ca href=\"#B76\"\u003EXu et al., 2006\u003C\u002Fa\u003E; \u003Ca href=\"#B17\"\u003EFukao and Bailey-Serres, 2008\u003C\u002Fa\u003E). Therefore, growth reduction of rapeseed plants could be a positive acclimation strategy under waterlogging (this work) as well as under submergence (\u003Ca href=\"#B73\"\u003EWittig et al., 2021\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EWhether the down-regulation of growth and biosynthesis is an active process in \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E remains to be elucidated. However, the fast down-regulation of many growth-related genes might suggest a controlled response. It is unlikely that the growth regulation is caused by sugar starvation since there is no indication for a carbohydrate starvation in rapeseed plants under root-zone hypoxia, and sugar content is rather higher than lower under stress (\u003Ca href=\"#F4\"\u003EFigure 4\u003C\u002Fa\u003E). This phenomenon has been previously observed in waterlogged plants of many species, for example in wheat and maize (e.g., \u003Ca href=\"#B26\"\u003EHuang and Johnson, 1995\u003C\u002Fa\u003E; \u003Ca href=\"#B49\"\u003EMustroph and Albrecht, 2003\u003C\u002Fa\u003E; \u003Ca href=\"#B1\"\u003EAlbrecht et al., 2004\u003C\u002Fa\u003E), tomato (\u003Ca href=\"#B20\"\u003EGharbi et al., 2009\u003C\u002Fa\u003E), potato (\u003Ca href=\"#B7\"\u003EBiemelt et al., 1999\u003C\u002Fa\u003E), and rapeseed (\u003Ca href=\"#B40\"\u003ELeul and Zhou, 1999\u003C\u002Fa\u003E). It might either be explained by a higher transport rate from the shoot, a reduced growth rate of roots, a limited sugar usage capacity in root cells, or a controlled down-regulation of root metabolism (\u003Ca href=\"#B19\"\u003EGeigenberger et al., 2000\u003C\u002Fa\u003E; \u003Ca href=\"#B1\"\u003EAlbrecht et al., 2004\u003C\u002Fa\u003E; \u003Ca href=\"#B20\"\u003EGharbi et al., 2009\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EThe underlying factors for the observed growth reduction, however, are not known yet. Hormones known to play a role under flooding-related stresses are abscisic acid (ABA) and gibberellic acid (GA) (summarized in \u003Ca href=\"#B5\"\u003EBailey-Serres et al., 2012\u003C\u002Fa\u003E; \u003Ca href=\"#B69\"\u003EVoesenek and Bailey-Serres, 2015\u003C\u002Fa\u003E). The GA-sensing DELLA proteins, who are responsible for growth reduction in rice under submergence (\u003Ca href=\"#B17\"\u003EFukao and Bailey-Serres, 2008\u003C\u002Fa\u003E), are not modified in their expression in rapeseed (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns R to AD; \u003Ca href=\"#S10\"\u003ESupplementary Table 6\u003C\u002Fa\u003E). However, a transcript coding for the GA degradation enzyme \u003Ci\u003EGIBBERELLIN 2-OXIDASE 3\u003C\u002Fi\u003E (\u003Ci\u003EGA2OX3\u003C\u002Fi\u003E, \u003Ca href=\"#B61\"\u003ERieu et al., 2008\u003C\u002Fa\u003E) is strongly induced in hypoxic rapeseed roots (\u003Ci\u003EBnaA05g09290D\u003C\u002Fi\u003E), which might play a role in reduction of growth in this species, while its homolog \u003Ci\u003EGA2OX2\u003C\u002Fi\u003E is seldomly induced by hypoxia in Arabidopsis (\u003Ca href=\"#B52\"\u003EMustroph et al., 2010\u003C\u002Fa\u003E). An involvement of the stress hormone ABA in growth reduction is also possible since several genes coding for the biosynthesis enzyme 9-cis-epoxycarotenoid dioxygenase (\u003Ci\u003ENCED\u003C\u002Fi\u003E) are reduced in their expression (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns R to AD; \u003Ca href=\"#S10\"\u003ETable 6\u003C\u002Fa\u003E). However, the HRG from Arabidopsis, \u003Ci\u003ECYP707A3\u003C\u002Fi\u003E, which is involved in the degradation of ABA (\u003Ca href=\"#B56\"\u003EOkamoto et al., 2011\u003C\u002Fa\u003E), is not induced by hypoxia in rapeseed roots (\u003Ca href=\"#F2\"\u003EFigure 2\u003C\u002Fa\u003E). In addition, other hormone pathways are differentially expressed and might be involved in the growth reduction, for example brassinosteroids, whose biosynthesis enzymes are strongly reduced in hypoxic roots (\u003Ca href=\"#S10\"\u003ESupplementary Table 6\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EThe transcriptional response in this work was compared to other published data of rapeseed as well as to Arabidopsis. In two publications, young rapeseed seedlings (about 3 days old) were subjected to full submergence (\u003Ca href=\"#B24\"\u003EGuo et al., 2020\u003C\u002Fa\u003E; \u003Ca href=\"#B41\"\u003ELi et al., 2021\u003C\u002Fa\u003E). Despite the different systems, there was a substantial and significant overlap between the different treatments and developmental stages (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns BM to BT, \u003Ca href=\"#S10\"\u003ESupplementary Table 7A\u003C\u002Fa\u003E). Many HRGs were among the induced genes under diverse flooding-related conditions. The direct comparison of our and earlier studies allowed us to define a set of hypoxia core response genes for \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E (BnHRGs, \u003Ca href=\"#S10\"\u003ESupplementary Tables 7B,C\u003C\u002Fa\u003E). 131 up-regulated and 163 down-regulated genes were in this dataset. While a large number of the up-regulated genes was also among HRGs in Arabidopsis (27), or was also hypoxia-responsive in Arabidopsis (90), a few genes seemed to be specific for rapeseed (14). Surprisingly, we found two transcription factors that are not yet described as HRGs in Arabidopsis, and that are rather linked to ABA, drought or wounding, namely \u003Ci\u003EETHYLENE RESPONSE FACTOR #111\u003C\u002Fi\u003E (\u003Ci\u003EERF#111\u003C\u002Fi\u003E, \u003Ci\u003EABR1\u003C\u002Fi\u003E) and \u003Ci\u003EDEHYDRATION-RESPONSIVE ELEMENT BINDING PROTEIN 2C\u003C\u002Fi\u003E (\u003Ci\u003EDREB2C\u003C\u002Fi\u003E) (e.g., \u003Ca href=\"#B36\"\u003ELee et al., 2010\u003C\u002Fa\u003E; \u003Ca href=\"#B31\"\u003EKim et al., 2011\u003C\u002Fa\u003E; \u003Ca href=\"#B6\"\u003EBäumler et al., 2019\u003C\u002Fa\u003E). The importance of these transcription factors under waterlogging and hypoxia in rapeseed remains to be elucidated.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EComparing our expression data to the expression of Arabidopsis under hypoxia (e.g., \u003Ca href=\"#B10\"\u003EBranco-Price et al., 2008\u003C\u002Fa\u003E; \u003Ca href=\"#B54\"\u003EMustroph et al., 2009\u003C\u002Fa\u003E, \u003Ca href=\"#B52\"\u003E2010\u003C\u002Fa\u003E and references therein; \u003Ca href=\"#B25\"\u003EHsu et al., 2011\u003C\u002Fa\u003E) revealed a strong overlap (\u003Ca href=\"#S10\"\u003ESupplementary Table 4\u003C\u002Fa\u003E). This included many, but not all HRGs. For example, the genes coding for \u003Ci\u003EACHT5\u003C\u002Fi\u003E, \u003Ci\u003ECYP707A3\u003C\u002Fi\u003E, and \u003Ci\u003EFHL\u003C\u002Fi\u003E were not induced by hypoxia in \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E. On the other hand, several genes were strongly induced in rapeseed by hypoxia, but not in Arabidopsis, for example \u003Ci\u003EPEPTIDEMETHIONINE SULFOXIDE REDUCTASE 3\u003C\u002Fi\u003E (\u003Ci\u003EPMSR3\u003C\u002Fi\u003E), ATP-dependent Clp protease (\u003Ci\u003EAT1G33360\u003C\u002Fi\u003E), \u003Ci\u003EEXPANSIN-LIKE B1\u003C\u002Fi\u003E (\u003Ci\u003EEXLB1\u003C\u002Fi\u003E), and two genes involved in hormone pathways already mentioned above (\u003Ci\u003EAHP4\u003C\u002Fi\u003E, \u003Ci\u003EGA2OX3\u003C\u002Fi\u003E). The function of these proteins in the context of hypoxic acclimation of rapeseed remains to be examined. A possible function of \u003Ci\u003EPMSR3\u003C\u002Fi\u003E could be the protection of proteins against oxidation of methionine residues (\u003Ca href=\"#B62\"\u003ESadanandom et al., 2000\u003C\u002Fa\u003E), but its induction in rapeseed seems to be only temporary.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EThere was also some overlap with genes commonly reduced by hypoxia in Arabidopsis. Although a previous work could not define a general set of down-regulated HRGs, there were seven genes that displayed a common root-specific down-regulation under hypoxia (\u003Ca href=\"#B54\"\u003EMustroph et al., 2009\u003C\u002Fa\u003E). Of those seven genes, three were also commonly reduced in hypoxic rapeseed roots, namely \u003Ci\u003ECYP83B1\u003C\u002Fi\u003E, \u003Ci\u003EMYB DOMAIN PROTEIN 34\u003C\u002Fi\u003E (\u003Ci\u003EMYB34\u003C\u002Fi\u003E) and \u003Ci\u003ESLAC1 HOMOLOG 3\u003C\u002Fi\u003E (\u003Ci\u003ESLAH3\u003C\u002Fi\u003E). The first two gene products are involved in tryptophan biosynthesis and its regulation, and thereby might affect glucosinolate biosynthesis (\u003Ca href=\"#B12\"\u003ECelenza et al., 2005\u003C\u002Fa\u003E). Their common down-regulation supports our hypothesis that biosynthetic processes are mainly reduced under hypoxic conditions. The third gene codes for an anion channel, which recently has been described to be involved in depolarization of membranes due to cytoplasmic acidosis, for example caused by flooding and hypoxia (\u003Ca href=\"#B39\"\u003ELehmann et al., 2021\u003C\u002Fa\u003E). Indeed, Arabidopsis plants with a defect in \u003Ci\u003ESLAH3\u003C\u002Fi\u003E were more resistant to full submergence in darkness, and the down-regulation of its expression in Arabidopsis as well as rapeseed might be an advantage for survival.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EOur experiments allow the conclusion that rapeseed roots can strongly respond to hypoxia in a coordinated way, and that this response is similar, but not identical to the response of Arabidopsis. Knowledge from the model plant \u003Ci\u003EArabidopsis thaliana\u003C\u002Fi\u003E, for example about the transcriptional regulation of the hypoxia response and mechanisms of metabolic acclimation, might therefore be reasonably transferrable to the crop \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E, in order to improve its tolerance against flooding. However, rapeseed has a much higher gene number due to whole-genome triplication and the tetraploid status (\u003Ca href=\"#B55\"\u003ENikolov and Tsiantis, 2017\u003C\u002Fa\u003E), making it a difficult species for genetic analyses. Indeed, most Arabidopsis genes have 2 to 8 isogenes in \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E, which is also true for many HRGs. Most, but not all isogenes for one Arabidopsis HRG are regulated in a similar way in rapeseed (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, column Q; \u003Ca href=\"#S10\"\u003ESupplementary Figure 2\u003C\u002Fa\u003E). It remains to be determined how the differential expression among isogenes is regulated, and whether previously defined promoter elements such as the HRPE (\u003Ca href=\"#B18\"\u003EGasch et al., 2016\u003C\u002Fa\u003E) are mutated or modified in some isogenes.\u003C\u002Fp\u003E\r\n\u003Ch3\u003E\u003Ci\u003EBrassica napus\u003C\u002Fi\u003E Leaves Show Only a Minor Response to Root Hypoxia\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb15\"\u003EPreviously we have identified a set of genes that is strongly induced under submergence in leaves of two \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E cultivars (\u003Ca href=\"#B73\"\u003EWittig et al., 2021\u003C\u002Fa\u003E). This analysis revealed a signature for carbohydrate starvation, which was in line with a severe decline in carbohydrate levels under water within a few hours, but hardly any induction of hypoxia-responsive genes. In the present work, leaves of \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E plants with root hypoxia showed little changes in gene expression (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns R to AD) indicating that the shoot was not yet affected by the stress of the root system, including the carbohydrate levels (\u003Ca href=\"#F4\"\u003EFigure 4\u003C\u002Fa\u003E). Previous analyses, however, have observed different responses in shoots of plants under root hypoxia or waterlogging. In Arabidopsis (\u003Ca href=\"#B25\"\u003EHsu et al., 2011\u003C\u002Fa\u003E) and cotton (\u003Ca href=\"#B14\"\u003EChristianson et al., 2010\u003C\u002Fa\u003E), many transcripts in the shoot responded to the root stress after 12 and 24 h, respectively. An analysis of rapeseed under root waterlogging also revealed massive transcriptional changes in leaves after 36 and 72 h of stress (\u003Ca href=\"#B38\"\u003ELee et al., 2014\u003C\u002Fa\u003E). Only in poplar, a waterlogging treatment did not result in significant expression differences in leaves, as determined after 7 days of stress (\u003Ca href=\"#B32\"\u003EKreuzwieser et al., 2009\u003C\u002Fa\u003E). Possible explanations for such a small response in our system could be that (1) the timepoint was too early to observe transcriptional changes, (2) the stress treatment was not severe enough to induce changes in the shoot system, or (3) changes occurred mainly in other parts of the shoots, for example the meristem or the stem. Indeed, the work on Arabidopsis harvested whole shoots (\u003Ca href=\"#B25\"\u003EHsu et al., 2011\u003C\u002Fa\u003E), and this was also the case for the previous work on rapeseed (\u003Ca href=\"#B38\"\u003ELee et al., 2014\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003ESurprisingly, the low number of transcripts in leaves responding to root hypoxia are hardly related to any specific GO term, and almost no modifications were observed for photosynthesis-related genes, as it has been previously observed (\u003Ca href=\"#B38\"\u003ELee et al., 2014\u003C\u002Fa\u003E). Also, no modification of ROS metabolism and no induction of ABA biosynthesis genes that might indicate problems with water uptake were observed in our experiment. This is in accordance with the small changes within the physiological data, i.e., the sugar content in leaves (\u003Ca href=\"#F4\"\u003EFigure 4\u003C\u002Fa\u003E), and no symptoms of wilting. Only after 7 days of stress treatment, the fresh weight in the hydroponic system was negatively affected (\u003Ca href=\"#F5\"\u003EFigure 5\u003C\u002Fa\u003E), and a slightly lower water content was observed (\u003Ca href=\"#S10\"\u003ESupplementary Figure 8A\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EAfter longer durations of the stress in the soil waterlogging system, a decrease in chlorophyll content was detected, but only with the invasive method (Figjure 6D). Decreases in chlorophyll content in rapeseed under root waterlogging have been found before (\u003Ca href=\"#B3\"\u003EAshraf and Mehmood, 1990\u003C\u002Fa\u003E; \u003Ca href=\"#B40\"\u003ELeul and Zhou, 1999\u003C\u002Fa\u003E; \u003Ca href=\"#B38\"\u003ELee et al., 2014\u003C\u002Fa\u003E), but they were more pronounced in the recovery phase. Surprisingly, the photosynthetic efficiency around PSII was only marginally affected under root waterlogging, as measured in the soil system (\u003Ca href=\"#F6\"\u003EFigures 6B\u003C\u002Fa\u003E, 7C). These results suggest that photosynthesis was only mildly affected in our stress treatment, thus explaining little changes in gene expression or sugar status (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E and \u003Ca href=\"#F4\"\u003EFigure 4\u003C\u002Fa\u003E). Therefore, a later timepoint might reveal more changes in gene expression in shoots, and potentially also a more severe treatment variant (\u003Ca href=\"#F7\"\u003EFigure 7\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EA common response of leaves in both genotypes was observed among down-regulated genes. Here, many genes associated with ribosomes and translation were lower expressed in leaves when roots were treated with hypoxia (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E). This is a hint that there is indeed some regulation of gene expression in leaves of plants with roots under stress. The down-regulation of ribosomal proteins suggests a down-regulation of translation in general, as it has been observed before for Arabidopsis seedlings (\u003Ca href=\"#B10\"\u003EBranco-Price et al., 2008\u003C\u002Fa\u003E; \u003Ca href=\"#B54\"\u003EMustroph et al., 2009\u003C\u002Fa\u003E). The signal that transmits the root stress to the shoots is, however, still unclear and remains to be solved.\u003C\u002Fp\u003E\r\n\u003Ch3\u003ENo Difference in the Response to Hypoxia and Waterlogging Between the Two Cultivars\u003C\u002Fh3\u003E\r\n\u003Cp class=\"mb15\"\u003EOne goal of this experimental set-up was to identify potential differences between two rapeseed cultivars, of which one had been described as tolerant toward waterlogging (e.g., \u003Ca href=\"#B79\"\u003EZou et al., 2013b\u003C\u002Fa\u003E,\u003Ca href=\"#B80\"\u003E2014\u003C\u002Fa\u003E). However, in none of our experimental set-ups, root-zone hypoxia in hydroponics (\u003Ca href=\"#F3\"\u003EFigures 3-5\u003C\u002Fa\u003E), waterlogging on soil (\u003Ca href=\"#F6\"\u003EFigure 6\u003C\u002Fa\u003E), and waterlogging with a starch solution (\u003Ca href=\"#F7\"\u003EFigure 7\u003C\u002Fa\u003E), we observed significant differences between the cultivars. Also, the gene expression analysis did not reveal clear differences in stress response between the genotypes (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns AR to AX). This might lead to the conclusion that the cultivars do not differ in their tolerance to waterlogging and root hypoxia, as previously demonstrated for treatment with submergence using the same two cultivars (\u003Ca href=\"#B73\"\u003EWittig et al., 2021\u003C\u002Fa\u003E). However, we cannot exclude a difference in tolerance at other developmental stages, in the recovery phase, or in field trials. It is also important to note that other rapeseed cultivars with contrasting response to waterlogging might exist. Furthermore, we have not evaluated whether differences in the genomic sequence of hypoxia-regulated genes exist between Avatar and Zhongshuang 9, and whether such differences might modify waterlogging and hypoxia tolerance. Indeed, certain single nucleotide polymorphisms (SNPs) that might be associated with submergence tolerance have been detected in a panel of rapeseed cultivars (\u003Ca href=\"#B71\"\u003EWang et al., 2020\u003C\u002Fa\u003E), but genome-wide association studies under waterlogging are still missing.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EThere are overall differences in gene expression between genotypes (\u003Ca href=\"#S10\"\u003ESupplementary Figure 7\u003C\u002Fa\u003E and \u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns AE to AQ), but they were seldomly related with a specific gene function (\u003Ca href=\"#S10\"\u003ESupplementary Table 3\u003C\u002Fa\u003E). Ribosomal proteins are generally more expressed in Avatar than in Zhongshuang 9, and especially leaves show a slight enrichment of photosynthesis-associated genes, which might correlate with a slightly higher chlorophyll content (\u003Ca href=\"#F6\"\u003EFigure 6D\u003C\u002Fa\u003E). Zhongshuang 9 showed even less functional categories with differential expression, which could be also due to a slightly lower mapping rate in comparison to the cultivar Avatar (\u003Ca href=\"#S10\"\u003ESupplementary Table 1\u003C\u002Fa\u003E).\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb15\"\u003EPrevious analyses have suggested that Zhongshuang 9 is more tolerant to waterlogging than GH01 due to expression differences for several genes (\u003Ca href=\"#B78\"\u003EZou et al., 2013a\u003C\u002Fa\u003E,\u003Ca href=\"#B81\"\u003E2015\u003C\u002Fa\u003E). However, the overall expression changes in response to the stress treatment in both cultivars were surprisingly similar (\u003Ca href=\"#S10\"\u003ESupplementary Table 2\u003C\u002Fa\u003E, columns AZ to BL). In order to evaluate the previously observed expression differences, we extracted the respective \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E gene IDs and looked for differential expression between our genotypes in the current genome assembly. However, none of the suggested candidates was differentially expressed between genotypes in our dataset (\u003Ca href=\"#S10\"\u003ESupplementary Table 8A\u003C\u002Fa\u003E). Moreover, our overview reveals multiple genes coding for one gene function, and the sum over all transcripts might be more similar than single gene copies suggest, for example the nine transcripts coding for glyceraldehyde-3-phosphate dehydrogenase C subunit 1 (\u003Ci\u003EGAPC1\u003C\u002Fi\u003E, \u003Ca href=\"#S10\"\u003ESupplementary Table 8A\u003C\u002Fa\u003E). In addition, a recent quantitative trait locus (QTL) analysis of the same two genotypes suggested another set of genes to be differentially expressed (\u003Ca href=\"#B16\"\u003EDing et al., 2020\u003C\u002Fa\u003E). However, there was no overlap of gene IDs between the two studies (\u003Ca href=\"#B81\"\u003EZou et al., 2015\u003C\u002Fa\u003E; \u003Ca href=\"#B16\"\u003EDing et al., 2020\u003C\u002Fa\u003E), and we could observe similar transcriptional changes for only a few transcripts in Zhongshuang 9 (\u003Ca href=\"#S10\"\u003ESupplementary Table 8B\u003C\u002Fa\u003E). This suggests that (1) the candidate genes from both studies are not differentially expressed at all developmental stages or stress variants, (2) other genes might be responsible for the QTLs defined in \u003Ca href=\"#B16\"\u003EDing et al. (2020)\u003C\u002Fa\u003E, or (3) the genotype Avatar does not differ as much from Zhongshuang 9 as GH01. In fact, most differences between the cultivars might occur only at the recovery phase after stress, as it has been recently demonstrated (\u003Ca href=\"#B33\"\u003EKuai et al., 2020a\u003C\u002Fa\u003E,\u003Ca href=\"#B34\"\u003Eb\u003C\u002Fa\u003E). Interestingly, the impact of nitrogen fertilizer on growth after flooding was as high or even higher than the impact of the genotype in these two publications.\u003C\u002Fp\u003E\r\n\u003Cp class=\"mb0\"\u003EMore work is therefore needed, with the inclusion of more and diverse genotypes, in order to find and develop flooding-tolerant rapeseed genotypes. One improvement to previous waterlogging treatments could be the addition of 0.1% starch to the solution. The addition of starch strongly decreased the oxygen content and increased the reduction potential (\u003Ca href=\"#S10\"\u003ESupplementary Figure 10\u003C\u002Fa\u003E), and therefore resembles more natural conditions than waterlogging with pure water, as previously demonstrated in barley (\u003Ca href=\"#B44\"\u003EMano and Takeda, 2012\u003C\u002Fa\u003E; \u003Ca href=\"#B46\"\u003EMiricescu et al., 2021\u003C\u002Fa\u003E). In our hands, the stress treatment with a starch solution was more severe compared with waterlogging with tap water (\u003Ca href=\"#F7\"\u003EFigure 7\u003C\u002Fa\u003E and \u003Ca href=\"#S10\"\u003ESupplementary Figure 9\u003C\u002Fa\u003E), and subsequent screening methods should consider this modified type of waterlogging stress, together with the addition of a recovery phase.\u003C\u002Fp\u003E\r\n\u003Ca id=\"h6\" name=\"h6\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003EConclusion\u003C\u002Fh2\u003E\r\n\u003Cp class=\"mb0\"\u003EThis work demonstrates that rapeseed is indeed able to strongly respond to waterlogging-associated hypoxia in the root zone at the transcriptional level. These responses might indicate an acclimation response to the stress, but they could also include responses to stress damage. A core hypoxia response for rapeseed plants could be defined, which can be used for future studies. However, a genotype-specific response to hypoxia and waterlogging between cultivars from different origin (Europe and Asia) could not be detected. However, we cannot exclude that SNPs related to tolerance are more important than overall transcriptional levels. In future, differences in gene sequences should be analyzed as well, for example by using a genome-wide association mapping approach, potentially together with QTL analyses. So far, only very few studies on rapeseed under flooding stress contain sufficient data for such an approach (\u003Ca href=\"#B16\"\u003EDing et al., 2020\u003C\u002Fa\u003E; \u003Ca href=\"#B71\"\u003EWang et al., 2020\u003C\u002Fa\u003E), and more work is required in this direction. The present dataset and a modified waterlogging treatment of plants grown in pots by use of a starch solution might help to identify potential tolerance-related genes in certain QTL regions, which ultimately could result in waterlogging-tolerant rapeseed genotypes.\u003C\u002Fp\u003E\r\n\u003Ca id=\"h7\" name=\"h7\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003EData Availability Statement\u003C\u002Fh2\u003E\r\n\u003Cp class=\"mb0\"\u003EThe datasets presented in this study can be found in online repositories. The names of the repository\u002Frepositories and accession number(s) can be found below: National Center for Biotechnology Information (NCBI) BioProject database under accession number GSE180262.\u003C\u002Fp\u003E\r\n\u003Ca id=\"h8\" name=\"h8\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003EAuthor Contributions\u003C\u002Fh2\u003E\r\n\u003Cp class=\"mb0\"\u003EAM designed the experiments, analyzed the data and wrote the manuscripts. BB developed the methods. SA, MK, PW, and AM performed the experiments. All authors contributed to the article and approved the submitted version.\u003C\u002Fp\u003E\r\n\u003Ca id=\"fun1\" name=\"fun1\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003EFunding\u003C\u002Fh2\u003E\r\n\u003Cp class=\"mb0\"\u003EThis study was supported by the Bavarian State Ministry of the Environment and Consumer Protection, project network BayKlimaFit [grant number TGC01GCUFuE69742]. This study was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) [491183248] and by the Open Access Publishing Fund of the University of Bayreuth.\u003C\u002Fp\u003E\r\n\u003Ca id=\"conf1\" name=\"conf1\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003EConflict of Interest\u003C\u002Fh2\u003E\r\n\u003Cp class=\"mb0\"\u003EThe authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.\u003C\u002Fp\u003E\r\n\u003Ca id=\"disclaimer1\" name=\"disclaimer1\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003EPublisher’s Note\u003C\u002Fh2\u003E\r\n\u003Cp class=\"mb0\"\u003EAll claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.\u003C\u002Fp\u003E\r\n\u003Ca id=\"ack1\" name=\"ack1\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003EAcknowledgments\u003C\u002Fh2\u003E\r\n\u003Cp class=\"mb0\"\u003EWe thank Alois Aigner and Xi-Ling Zou for providing \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E seeds. Maria Klecker is acknowledged for critical reading of the manuscript, and the students Verena Geiger and Jonas Freiberg are acknowledged for help with the experiments.\u003C\u002Fp\u003E\r\n\u003Ca id=\"S10\" name=\"S10\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003ESupplementary Material\u003C\u002Fh2\u003E\r\n\u003Cp class=\"mb0\"\u003EThe Supplementary Material for this article can be found online at: \u003Ca href=\"https:\u002F\u002Fwww.frontiersin.org\u002Farticles\u002F10.3389\u002Ffpls.2022.897673\u002Ffull#supplementary-material\"\u003Ehttps:\u002F\u002Fwww.frontiersin.org\u002Farticles\u002F10.3389\u002Ffpls.2022.897673\u002Ffull#supplementary-material\u003C\u002Fa\u003E\u003C\u002Fp\u003E\r\n\u003Ca id=\"abbr1\" name=\"abbr1\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003EAbbreviations\u003C\u002Fh2\u003E\r\n\u003Cp class=\"mb0\"\u003EADH, alcohol dehydrogenase; ERF, ethylene response factor; FDR, false discovery rate; GO, gene ontology; HRG, hypoxia core-response gene; PDC, pyruvate decarboxylase; SNP, single nucleotide polymorphism; QTL, quantitative trail locus.\u003C\u002Fp\u003E\r\n\u003Ca id=\"refer1\" name=\"refer1\"\u003E\u003C\u002Fa\u003E\u003Ch2\u003EReferences\u003C\u002Fh2\u003E\r\n\u003Cdiv class=\"References\" style=\"margin-bottom:0.5em;\"\u003E\r\n\u003Cp class=\"ReferencesCopy1\"\u003E\u003Ca name=\"B1\" id=\"B1\"\u003E\u003C\u002Fa\u003EAlbrecht, G., Mustroph, A., and Fox, T. 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A comparison of screening methods to identify waterlogging tolerance in the field in \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E L. during plant ontogeny. \u003Ci\u003EPLoS One\u003C\u002Fi\u003E 9:e89731. doi: 10.1371\u002Fjournal.pone.0089731\u003C\u002Fp\u003E\r\n\u003Cp class=\"ReferencesCopy2\"\u003E\u003Ca href=\"https:\u002F\u002Fpubmed.ncbi.nlm.nih.gov\u002F24594687\" target=\"_blank\"\u003EPubMed Abstract\u003C\u002Fa\u003E | \u003Ca href=\"https:\u002F\u002Fdoi.org\u002F10.1371\u002Fjournal.pone.0089731\" target=\"_blank\"\u003ECrossRef Full Text\u003C\u002Fa\u003E | \u003Ca href=\"http:\u002F\u002Fscholar.google.com\u002Fscholar_lookup?&title=A+comparison+of+screening+methods+to+identify+waterlogging+tolerance+in+the+field+in+Brassica+napus+L%2E+during+plant+ontogeny%2E&journal=PLoS+One&author=Zou+X.+L.&author=Hu+C.+W.&author=Zeng+L.&author=Cheng+Y.&author=Xu+M.+Y.&author=Zhang+X.+K.&publication_year=2014&volume=9&issue=e89731\" target=\"_blank\"\u003EGoogle Scholar\u003C\u002Fa\u003E\u003C\u002Fp\u003E\r\n\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"References\" style=\"margin-bottom:0.5em;\"\u003E\r\n\u003Cp class=\"ReferencesCopy1\"\u003E\u003Ca name=\"B81\" id=\"B81\"\u003E\u003C\u002Fa\u003EZou, X. L., Zeng, L., Lu, G. Y., Cheng, Y., Xu, J. S., and Zhang, X. K. (2015). Comparison of transcriptomes undergoing waterlogging at the seedling stage between tolerant and sensitive varieties of \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E L. \u003Ci\u003EJ. Integr. Agric.\u003C\u002Fi\u003E 14, 1723–1734. doi: 10.1016\u002Fs2095-3119(15)61138-8\u003C\u002Fp\u003E\r\n\u003Cp class=\"ReferencesCopy2\"\u003E\u003Ca href=\"https:\u002F\u002Fdoi.org\u002F10.1016\u002Fs2095-3119(15)61138-8\" target=\"_blank\"\u003ECrossRef Full Text\u003C\u002Fa\u003E | \u003Ca href=\"http:\u002F\u002Fscholar.google.com\u002Fscholar_lookup?&title=Comparison+of+transcriptomes+undergoing+waterlogging+at+the+seedling+stage+between+tolerant+and+sensitive+varieties+of+Brassica+napus+L%2E&journal=J%2E+Integr%2E+Agric%2E&author=Zou+X.+L.&author=Zeng+L.&author=Lu+G.+Y.&author=Cheng+Y.&author=Xu+J.+S.&author=Zhang+X.+K.&publication_year=2015&volume=14&pages=1723–1734\" target=\"_blank\"\u003EGoogle Scholar\u003C\u002Fa\u003E\u003C\u002Fp\u003E\r\n\u003C\u002Fdiv\u003E\r\n\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"thinLineM20\"\u003E\u003C\u002Fdiv\u003E\r\n\u003Cdiv class=\"AbstractSummary\"\u003E\r\n\u003Cp\u003E\u003Cspan\u003EKeywords\u003C\u002Fspan\u003E: \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E, waterlogging, root-zone hypoxia, fermentation, RNA sequencing\u003C\u002Fp\u003E\r\n\u003Cp\u003E\u003Cspan\u003ECitation:\u003C\u002Fspan\u003E Ambros S, Kotewitsch M, Wittig PR, Bammer B and Mustroph A (2022) Transcriptional Response of Two \u003Ci\u003EBrassica napus\u003C\u002Fi\u003E Cultivars to Short-Term Hypoxia in the Root Zone. \u003Ci\u003EFront. Plant Sci.\u003C\u002Fi\u003E 13:897673. doi: 10.3389\u002Ffpls.2022.897673\u003C\u002Fp\u003E\r\n\u003Cp id=\"timestamps\"\u003E\r\n\u003Cspan\u003EReceived:\u003C\u002Fspan\u003E 16 March 2022; \u003Cspan\u003EAccepted:\u003C\u002Fspan\u003E 11 April 2022;\u003Cbr\u002F\u003E\u003Cspan\u003EPublished:\u003C\u002Fspan\u003E 29 April 2022.\u003C\u002Fp\u003E\r\n\u003Cdiv\u003E\r\n\u003Cp\u003EEdited by:\u003C\u002Fp\u003E\r\n\u003Ca href=\"https:\u002F\u002Floop.frontiersin.org\u002Fpeople\u002F698294\u002Foverview\"\u003ESilvia Pampana\u003C\u002Fa\u003E, University of Pisa, Italy\u003C\u002Fdiv\u003E\r\n\u003Cdiv\u003E\r\n\u003Cp\u003EReviewed by:\u003C\u002Fp\u003E\r\n\u003Ca href=\"https:\u002F\u002Floop.frontiersin.org\u002Fpeople\u002F357256\u002Foverview\"\u003EDavid Jespersen\u003C\u002Fa\u003E, University of Georgia, United States\u003Cbr\u002F\u003E\r\n\u003Ca href=\"https:\u002F\u002Floop.frontiersin.org\u002Fpeople\u002F811663\u002Foverview\"\u003EMuhammad Farooq\u003C\u002Fa\u003E, University of Teramo, Italy\u003Cbr\u002F\u003E\r\n\u003Ca href=\"https:\u002F\u002Floop.frontiersin.org\u002Fpeople\u002F140716\u002Foverview\"\u003EArun K. Shanker\u003C\u002Fa\u003E, Central Research Institute for Dryland Agriculture (ICAR), India\u003C\u002Fdiv\u003E\r\n\u003Cp\u003E\u003Cspan\u003ECopyright\u003C\u002Fspan\u003E © 2022 Ambros, Kotewitsch, Wittig, Bammer and Mustroph. This is an open-access article distributed under the terms of the \u003Ca rel=\"license\" href=\"http:\u002F\u002Fcreativecommons.org\u002Flicenses\u002Fby\u002F4.0\u002F\" target=\"_blank\"\u003ECreative Commons Attribution License (CC BY)\u003C\u002Fa\u003E. The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.\u003C\u002Fp\u003E\r\n\u003Cp\u003E\u003Cspan\u003E*Correspondence:\u003C\u002Fspan\u003E Angelika Mustroph, \u003Ca href=\"mailto:angelika.mustroph@uni-bayreuth.de\"\u003Eangelika.mustroph@uni-bayreuth.de\u003C\u002Fa\u003E\u003C\u002Fp\u003E\r\n\u003Cdiv class=\"clear\"\u003E\u003C\u002Fdiv\u003E\r\n\u003C\u002Fdiv\u003E",menuHtml:"\u003Cul class=\"flyoutJournal\"\u003E\r\n\u003Cli\u003E\u003Ca href=\"#h1\"\u003EAbstract\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#h2\"\u003EIntroduction\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#h3\"\u003EMaterials and Methods\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#h4\"\u003EResults\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#h5\"\u003EDiscussion\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#h6\"\u003EConclusion\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#h7\"\u003EData Availability Statement\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#h8\"\u003EAuthor Contributions\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#fun1\"\u003EFunding\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#conf1\"\u003EConflict of Interest\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#disclaimer1\"\u003EPublisher’s Note\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#ack1\"\u003EAcknowledgments\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#S10\"\u003ESupplementary Material\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#abbr1\"\u003EAbbreviations\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003Cli\u003E\u003Ca href=\"#refer1\"\u003EReferences\u003C\u002Fa\u003E\u003C\u002Fli\u003E\r\n\u003C\u002Ful\u003E\r\n"},files:[{name:"EPUB.epub",fileServerPackageEntryId:g,type:{code:at,name:at}},{name:au,fileServerPackageEntryId:"fpls-13-897673\u002Ffpls-13-897673.pdf",type:{code:o,name:o}},{name:au,fileServerPackageEntryId:g,type:{code:o,name:o}},{name:"fpls-13-897673.xml",fileServerPackageEntryId:"fpls-13-897673\u002Ffpls-13-897673.xml",type:{code:"NLM_XML",name:"XML"}},{name:"Provisional PDF.pdf",fileServerPackageEntryId:g,type:{code:o,name:o}}]},currentArticlePageMetaInfo:{title:av,link:[{rel:"canonical",href:aw}],meta:[{hid:z,property:z,name:z,content:ax},{hid:ay,property:ay,name:"title",content:av},{hid:az,property:az,name:z,content:ax},{hid:aA,name:aA,content:"Brassica napus,waterlogging,root-zone hypoxia,fermenation,RNA 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Bayreuth","Germany","citation_author","citation_author_institution","Department of Plant Physiology, University of Bayreuth, Germany",4,2,"description","Frontiers","Help center","Link","Grey","Medium","ssph-journal.org","fship","Front. Plant Sci.","1664-462X",void 0,18,9,13,1920,"por-journal.com",7,"escubed.org",1918,"fipp","https:\u002F\u002Fd2csxpduxe849s.cloudfront.net\u002Fmedia\u002FE32629C6-9347-4F84-81FEAEF7BFA342B3\u002F450E9326-0272-405C-B8D614C72BED9F89\u002Fwebimage-00A7F7FD-61FC-4329-B3BFCC0119B4B276.jpg","image","2022-06-27T10:00:48Z","fpls",66,"journal_field","10.3389\u002Ffpls.2022.897673","Transcriptional Response of Two Brassica napus Cultivars to Short-Term Hypoxia in the Root Zone","\u003Cp\u003EWaterlogging is one major stress for crops and causes multiple problems for plants, for example low gas diffusion, changes in redox potential and accumulation of toxic metabolites. \u003Citalic\u003EBrassica napus\u003C\u002Fitalic\u003E is an important oil crop with high waterlogging sensitivity, which may cause severe yield losses. Its reactions to the stress are not fully understood. In this work the transcriptional response of rapeseed to one aspect of waterlogging, hypoxia in the root zone, was analyzed by RNAseq, including two rapeseed cultivars from different origin, Avatar from Europe and Zhongshuang 9 from Asia. Both cultivars showed a high number of differentially expressed genes in roots after 4 and 24 h of hypoxia. The response included many well-known hypoxia-induced genes such as genes coding for glycolytic and fermentative enzymes, and strongly resembled the hypoxia response of the model organism \u003Citalic\u003EArabidopsis thaliana\u003C\u002Fitalic\u003E. The carbohydrate status of roots, however, was minimally affected by root hypoxia, with a tendency of carbohydrate accumulation rather than a carbon starvation. Leaves did not respond to the root stress after a 24-h treatment. In agreement with the gene expression data, subsequent experiments with soil waterlogging for up to 14 days revealed no differences in response or tolerance to waterlogging between the two genotypes used in this study. Interestingly, using a 0.1% starch solution for waterlogging, which caused a lowered soil redox potential, resulted in much stronger effects of the stress treatment than using pure water suggesting a new screening method for rapeseed cultivars in future experiments.\u003C\u002Fp\u003E",15,"Stefanie","Mona","Philipp R.","Bettina",27285,"Angelika",698294,"Silvia","Italy",140716,357256,"David",811663,"Muhammad",{},1312,"Plant Abiotic Stress","plant-abiotic-stress","EPUB","fpls-13-897673.pdf","Frontiers | Transcriptional Response of Two Brassica napus Cultivars to Short-Term Hypoxia in the Root Zone","https:\u002F\u002Fwww.frontiersin.org\u002Fjournals\u002Fplant-science\u002Farticles\u002F10.3389\u002Ffpls.2022.897673\u002Ffull","Waterlogging is one major stress for crops and causes multiple problems for plants, for example low gas diffusion, changes in redox potential and 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