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class="widget widget-ArticleJumpLinks widget-instance-OUP_ArticleJumpLinks_Widget"> <h3 class="contents-title" >Article Contents</h3> <ul class="jumplink-list js-jumplink-list"> <li class="section-jump-link head-1" link-destination="136423268"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#136423268">Abstract</a> </div> </li> <li class="section-jump-link head-1" link-destination="136423270"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#136423270">Introduction</a> </div> </li> <li class="section-jump-link head-1" link-destination="136423280"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#136423280">Stress-induced cell death, autophagy, and proteases</a> </div> </li> <li class="section-jump-link head-1" link-destination="136423287"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#136423287">Endogenous auxin</a> </div> </li> <li class="section-jump-link head-1" link-destination="136423293"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#136423293">Epigenetic modifications and chromatin remodelling</a> </div> </li> <li class="section-jump-link head-1" link-destination="136423302"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#136423302">Cell wall remodelling: pectins and AGPs</a> </div> </li> <li class="section-jump-link head-1" link-destination="136423307"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#136423307">Concluding remarks</a> </div> </li> <li class="section-jump-link head-1" link-destination="136423311"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" href="#136423311">Acknowledgements</a> </div> </li> <li class="section-jump-link head-1 backReferenceLink" link-destination="136423313"> <div class="section-jump-link__link-wrap"> <a class="js-jumplink scrollTo" 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</div> </div> <div class="content-inner-wrap"> <div class="widget widget-ArticleTopInfo widget-instance-OUP_ArticleTop_Info_Widget"> <div class="module-widget article-top-widget"> <div class="access-state-logos all-viewports"> <span class="journal-info__format-label">Journal Article</span> </div> <div class="widget-items"> <div class="title-wrap"> <h1 class="wi-article-title article-title-main accessible-content-title at-articleTitle"> Microspore embryogenesis: targeting the determinant factors of stress-induced cell reprogramming for crop improvement <i class='icon-availability_free' title='Free' ></i> </h1> </div> <div class="wi-authors at-ArticleAuthors"> <div class="al-authors-list"> <span class="al-author-name-more js-flyout-wrap"> <button type="button" class="linked-name js-linked-name-trigger btn-as-link">Pilar S Testillano</button><span class='delimiter'></span> <span class="al-author-info-wrap arrow-up"> <div class="info-card-author authorInfo_OUP_ArticleTop_Info_Widget"> <div class="name-role-wrap"> <div class="info-card-name"> Pilar S Testillano <span class="info-card-footnote"><span class="xrefLink" id="jumplink-c1"></span><a href="javascript:;" reveal-id="c1" data-open="c1" class="link link-ref link-reveal xref-default"></a></span> </div> </div> <div class="info-card-affilitation"> <div class="aff">Pollen Biotechnology of Crop Plants group, Biological Research Center, CIB-CSIC, Ramiro de Maeztu, Madrid, Spain</div> </div> <div class="info-author-correspondence"> <div content-id="c1">Correspondence: <a href="mailto:testillano@cib.csic.es" target="_blank">testillano@cib.csic.es</a></div> </div> <div class="info-card-location"> <a id="contrib-orcid-0000-0003-4509-7646" href="https://orcid.org/0000-0003-4509-7646"> <img class="orchid-icon" alt="ORCID logo" aria-hidden="true" src="//oup.silverchair-cdn.com/Themes/Silver/app/img/mini-icon.png"/>  https://orcid.org/0000-0003-4509-7646 </a> </div> <div class="info-card-search-label"> Search for other works by this author on: </div> <div class="info-card-search info-card-search-internal"> <a href="/jxb/search-results?f_Authors=Pilar+S+Testillano" rel="nofollow">Oxford Academic</a> </div> <div class="info-card-search info-card-search-pubmed"> <a href="http://www.ncbi.nlm.nih.gov/pubmed?cmd=search&term=Testillano P">PubMed</a> </div> <div class="info-card-search info-card-search-google"> <a href="http://scholar.google.com/scholar?q=author:%22Testillano Pilar S%22">Google Scholar</a> </div> </div> </span> </span> </div> </div> <div class="pub-history-wrap clearfix js-history-dropdown-wrap"> <div class="pub-history-row clearfix"> <div class="ww-citation-primary"><em>Journal of Experimental Botany</em>, Volume 70, Issue 11, 15 May 2019, Pages 2965–2978, <a href='https://doi.org/10.1093/jxb/ery464'>https://doi.org/10.1093/jxb/ery464</a></div> </div> <div class="pub-history-row clearfix"> <div class="ww-citation-date-wrap"> <div class="citation-label">Published:</div> <div class="citation-date">08 February 2019</div> </div> <a href="javascript:;" class="history-label js-history-dropdown-trigger st-article-history at-ArticleHistory"> <span>Article history</span><i class="icon-general-arrow-filled-down arrow-icon"></i> </a> </div> <div class="ww-history js-history-entries-wrap at-history-entries-wrap"> <div class="history-entry at-history-entry"> <div class="wi-state">Received:</div> <div class="wi-date">31 October 2018</div> </div> <div class="history-entry at-history-entry"> <div class="wi-state">Accepted:</div> <div class="wi-date">17 December 2018</div> </div> <div class="history-entry at-history-entry"> <div class="wi-state">Published:</div> <div class="wi-date">08 February 2019</div> </div> </div> </div> </div> </div> <script> $(document).ready(function () { $('.article-top-widget').on('click', '.ati-toggle-trigger', function () { $(this).find('.icon-general-add, .icon-minus').toggleClass('icon-minus icon-general-add'); 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/> </div> </div> </div> </div> <div id="ContentTab" class="content active"> <div class="widget widget-ArticleFulltext widget-instance-OUP_Article_FullText_Widget"> <div class="module-widget"> <div class="widget-items" data-widgetname="ArticleFulltext"> <h2 scrollto-destination=136423268 id="136423268" class="abstract-title js-splitscreen-abstract-title" >Abstract</h2> <section class="abstract"><p class="chapter-para">Under stress, isolated microspores are reprogrammed <em>in vitro</em> towards embryogenesis, producing doubled haploid plants that are useful biotechnological tools in plant breeding as a source of new genetic variability, fixed in homozygous plants in only one generation. Stress-induced cell death and low rates of cell reprogramming are major factors that reduce yield. Knowledge gained in recent years has revealed that initiation and progression of microspore embryogenesis involve a complex network of factors, whose roles are not yet well understood. Here, I review recent findings on the determinant factors underlying stress-induced microspore embryogenesis, focusing on the role of autophagy, cell death, auxin, chromatin modifications, and the cell wall. Autophagy and cell death proteases are crucial players in the response to stress, while cell reprogramming and acquisition of totipotency are regulated by hormonal and epigenetic mechanisms. Auxin biosynthesis, transport, and action are required for microspore embryogenesis. Initial stages involve DNA hypomethylation, H3K9 demethylation, and H3/H4 acetylation. Cell wall remodelling, with pectin de-methylesterification and arabinogalactan protein expression, is necessary for embryo development. Recent reports show that treatments with small modulators of autophagy, proteases, and epigenetic marks reduce cell death and enhance embryogenesis initiation in several crops, opening up new possibilities for improving <em>in vitro</em> embryo production in breeding programmes.</p></section> <div class="article-metadata-panel clearfix at-ArticleMetadata"></div> <div class="kwd-group"><a class="kwd-part kwd-main" href="javascript:;" data-keyword="Autophagy">Autophagy</a>, <a class="kwd-part kwd-main" href="javascript:;" data-keyword=""cell death"">cell death</a>, <a class="kwd-part kwd-main" href="javascript:;" data-keyword=""cell fate"">cell fate</a>, <a class="kwd-part kwd-main" href="javascript:;" data-keyword=""cell totipotency"">cell totipotency</a>, <a class="kwd-part kwd-main" href="javascript:;" data-keyword=""cell wall"">cell wall</a>, <a class="kwd-part kwd-main" href="javascript:;" data-keyword="differentiation">differentiation</a>, <a class="kwd-part kwd-main" href="javascript:;" data-keyword=""epigenetic marks"">epigenetic marks</a>, <a class="kwd-part kwd-main" href="javascript:;" data-keyword=""microspore embryogenesis"">microspore embryogenesis</a>, <a class="kwd-part kwd-main" href="javascript:;" data-keyword="phytohormones">phytohormones</a>, <a class="kwd-part kwd-main" href="javascript:;" data-keyword="stress">stress</a></div> <h2 scrollto-destination=136423270 id="136423270" class="section-title js-splitscreen-section-title" data-legacy-id=s1>Introduction</h2> <p class="chapter-para">Plants, unlike animals, exhibit extraordinary developmental plasticity as they continuously form organs during post-embryonic development. The plasticity of plant cells, particularly their ability to regenerate embryos through <em>in vitro</em> culture, has been extensively exploited for decades for the purpose of plant propagation, breeding, and conservation, with relevant applications in agriculture, forestry, and the preservation of genetic resources (<span class="xrefLink" id="jumplink-CIT0043"></span><a href="javascript:;" reveal-id="CIT0043" data-open="CIT0043" class="link link-ref link-reveal xref-bibr">Germaná and Lambardi, 2016</a>). <em>In vitro</em> embryogenesis is a fascinating example of cellular totipotency, as different kinds of somatic cells can be reprogrammed, giving rise to an entire embryo and ultimately a plant.</p><p class="chapter-para">Microspore embryogenesis is an <em>in vitro</em> system in which the haploid microspore (pollen mother cell) is reprogrammed by the application of external stress treatments and enters into an embryogenesis pathway (<span class="xrefLink" id="jumplink-F1"></span><a href="javascript:;" data-modal-source-id="F1" class="link xref-fig">Fig. 1</a>). The resulting haploid embryo can diploidize either spontaneously or by application of chromosome doubling agents (<span class="xrefLink" id="jumplink-CIT0136"></span><a href="javascript:;" reveal-id="CIT0136" data-open="CIT0136" class="link link-ref link-reveal xref-bibr">Testillano <em>et al.</em>, 2004</a>; <span class="xrefLink" id="jumplink-CIT0101"></span><a href="javascript:;" reveal-id="CIT0101" data-open="CIT0101" class="link link-ref link-reveal xref-bibr">Pintos <em>et al.</em>, 2007</a>; <span class="xrefLink" id="jumplink-CIT0018"></span><a href="javascript:;" reveal-id="CIT0018" data-open="CIT0018" class="link link-ref link-reveal xref-bibr">Castillo <em>et al.</em>, 2009</a>), producing doubled haploid (DH) plants that are fully homozygous for each locus. DHs are important biotechnological tools in plant breeding mainly because they permit the breeding process to be considerably shortened (<span class="xrefLink" id="jumplink-CIT0077"></span><a href="javascript:;" reveal-id="CIT0077" data-open="CIT0077" class="link link-ref link-reveal xref-bibr">Maluszynski <em>et al</em>., 2003</a>; <span class="xrefLink" id="jumplink-CIT0038"></span><a href="javascript:;" reveal-id="CIT0038" data-open="CIT0038" class="link link-ref link-reveal xref-bibr">Forster <em>et al.</em>, 2007</a>; <span class="xrefLink" id="jumplink-CIT0089"></span><a href="javascript:;" reveal-id="CIT0089" data-open="CIT0089" class="link link-ref link-reveal xref-bibr">Murovec and Bohanec, 2012</a>). With DH technology, completely homozygous plants can be established in only one generation, while in a conventional breeding programme the development of homozygous lines normally involves several generations of selfing and selection. DHs can be used as parental lines for hybrid production; they increase the selection efficiency since recessive alleles of improved characters are fixed and directly expressed in one generation. On the other hand, due to the homozygous condition of DHs, deleterious recessive alleles are eliminated at early steps of the breeding programme (<span class="xrefLink" id="jumplink-CIT0104"></span><a href="javascript:;" reveal-id="CIT0104" data-open="CIT0104" class="link link-ref link-reveal xref-bibr">Prem <em>et al.</em>, 2004</a>; <span class="xrefLink" id="jumplink-CIT0041"></span><a href="javascript:;" reveal-id="CIT0041" data-open="CIT0041" class="link link-ref link-reveal xref-bibr">Germaná, 2011</a>; <span class="xrefLink" id="jumplink-CIT0089"></span><a href="javascript:;" reveal-id="CIT0089" data-open="CIT0089" class="link link-ref link-reveal xref-bibr">Murovec and Bohanec, 2012</a>; <span class="xrefLink" id="jumplink-CIT0028"></span><a href="javascript:;" reveal-id="CIT0028" data-open="CIT0028" class="link link-ref link-reveal xref-bibr">Dwivedi <em>et al.</em>, 2015</a>). Another advantage of DHs in crop breeding is the increase of the genetic gain; DH plants are regenerated from individual microspores and, therefore, due to meiotic recombination, they contain new gene combinations which represent new recombinant products of the parental genomes fixed in the homozygous state. Besides these advantages, DHs can be combined with other breeding approaches such as mutation or gene transformation, leading to greatly accelerated cultivar development (<span class="xrefLink" id="jumplink-CIT0104"></span><a href="javascript:;" reveal-id="CIT0104" data-open="CIT0104" class="link link-ref link-reveal xref-bibr">Prem <em>et al.</em>, 2004</a>; <span class="xrefLink" id="jumplink-CIT0050"></span><a href="javascript:;" reveal-id="CIT0050" data-open="CIT0050" class="link link-ref link-reveal xref-bibr">Gurushidze <em>et al.</em>, 2014</a>; <span class="xrefLink" id="jumplink-CIT0028"></span><a href="javascript:;" reveal-id="CIT0028" data-open="CIT0028" class="link link-ref link-reveal xref-bibr">Dwivedi <em>et al.</em>, 2015</a>; <span class="xrefLink" id="jumplink-CIT0107"></span><a href="javascript:;" reveal-id="CIT0107" data-open="CIT0107" class="link link-ref link-reveal xref-bibr">Ren <em>et al.</em>, 2017</a>; <span class="xrefLink" id="jumplink-CIT0113"></span><a href="javascript:;" reveal-id="CIT0113" data-open="CIT0113" class="link link-ref link-reveal xref-bibr">Rustgi <em>et al.</em>, 2017</a>). For all these reasons, microspore embryogenesis <em>in vitro</em> systems are widely used by plant nursery and seed companies to generate new isogenic lines rapidly for breeding programmes. Since 1964, the year in which the production of haploid embryos was first achieved from anther cultures of <em>Datura</em> (<span class="xrefLink" id="jumplink-CIT0049"></span><a href="javascript:;" reveal-id="CIT0049" data-open="CIT0049" class="link link-ref link-reveal xref-bibr">Guha and Maheshwari, 1964</a>), <em>in vitro</em> systems of microspore embryogenesis have been developed for >250 plant species belonging to a wide range of families (reviewed in <span class="xrefLink" id="jumplink-CIT0077"></span><a href="javascript:;" reveal-id="CIT0077" data-open="CIT0077" class="link link-ref link-reveal xref-bibr">Maluszynski <em>et al.</em>, 2003</a>), with variable efficiency. Even though the application of microspore embryogenesis to DH production is currently widely exploited, it is still highly, or even completely, inefficient in many species of economic interest in the fields of agriculture and forestry.</p> <a id="136423273" scrollto-destination="136423273"></a> <div data-id="f1" data-content-id="f1" class="fig fig-section js-fig-section" swap-content-for-modal="true"><div class="graphic-wrap"><img class="content-image" src="https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/jxb/70/11/10.1093_jxb_ery464/1/m_exbotj_ery464_f0001.jpeg?Expires=1735137917&Signature=Z9cn14k2T9RPZDBqEUETcqfVKS9FiAfxlxIl54yhHbmsWqs1TLLJ~AxUxVCUn8uw4n4Zpv6XMoZWeDjKi7PEEnf2nc0QVKUwdtB7Du7akV3rfsZ8h-oiOeFmkF5qWmwhp7bxojVgkT5L1Xmfi72uoTv~1joCU1nTFg4lVWK0lBXuabjPtyYYGJO7LFdoZXD8ff5kllqmmsou3QW00CoKtP4rYVIvADLfE-f9l2L~lZSvikzH~C-br~IyOuv8EWe0GGvQlymR5KMoK3YOEVwrKM4QnKZhM9eZfJmGx-pYaXf15LSMpdohmh80EXn2cvKUH6xKTwx1ZYRSWRDZWLhfTg__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA" alt="Schematic representation of the two developmental pathways of the microspore. In vivo, the vacuolated microspore divides asymmetrically giving rise to the bicellular pollen grain, which follows the gametophytic development and produces the tricellular pollen. In vitro, by the application of specific stress treatments, the vacuolated microspore is reprogrammed towards an embryogenic pathway, initially producing proembryos (multicellular structures confined by the microspore wall) and later fully differentiated embryos, able to germinate and produce doubled haploid plants. In this in vitro pathway, some microspores do not respond to reprogramming and die, after the stress." data-path-from-xml="exbotj_ery464_f0001.jpg" /><div class="graphic-bottom"><div class="label fig-label" id="label-136423273">Fig. 1.</div><div class="caption fig-caption"><p class="chapter-para">Schematic representation of the two developmental pathways of the microspore. <em>In vivo</em>, the vacuolated microspore divides asymmetrically giving rise to the bicellular pollen grain, which follows the gametophytic development and produces the tricellular pollen. <em>In vitro</em>, by the application of specific stress treatments, the vacuolated microspore is reprogrammed towards an embryogenic pathway, initially producing proembryos (multicellular structures confined by the microspore wall) and later fully differentiated embryos, able to germinate and produce doubled haploid plants. In this <em>in vitro</em> pathway, some microspores do not respond to reprogramming and die, after the stress.</p></div><div class="ajax-articleAbstract-exclude-regex fig-orig original-slide figure-button-wrap"><a class="fig-view-orig js-view-large at-figureViewLarge openInAnotherWindow" role="button" aria-describedby="label-136423273" href="/view-large/figure/136423273/exbotj_ery464_f0001.jpg" data-path-from-xml="exbotj_ery464_f0001.jpg" target="_blank">Open in new tab</a><a class="download-slide" role="button" aria-describedby="label-136423273" data-section="136423273" href="/DownloadFile/DownloadImage.aspx?image=https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/jxb/70/11/10.1093_jxb_ery464/1/exbotj_ery464_f0001.jpeg?Expires=1735137917&Signature=XathiASUS40M3eleSwNd6gQIaiAdSPwVjE~JokGlCQaqtjlbo~cnLEwMsmXbq413T1XFAiPs5gPzYh9USQ~2vs0Mja~qRNBKzIMzXSbtTDgcQBwE6huIo6PicTY9DJV3GQ1yfLi7Vphka1j1~lcQPWJKxxUlpZ~flJZ07tEUZptwImO07zEYE-0ZAeyDYnLNzWdF62OZoI-vl6s0bth7BNQgqSwMumWovh4VDeju4e-n~3hWZ602uT9Q7sc2yfOb232h0qrGIMeISymo7zp0ppN8OzWyo2BoYwTBdXxzmucDasiAERPTr3orFYZAV1NTaFUoe7ChOovk1696VPylzg__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA&sec=136423273&ar=5310108&xsltPath=~/UI/app/XSLT&imagename=&siteId=5304" data-path-from-xml="exbotj_ery464_f0001.jpg">Download slide</a></div></div></div></div><p class="chapter-para">The yield of microspore-derived embryo production has several bottlenecks at various stages of the process, such as induction and initiation of embryogenesis, which are both crucial steps. Induction of microspore embryogenesis is performed by application of specific stress treatments, such as cold, heat, or starvation, using either anthers or isolated microspore cultures (<span class="xrefLink" id="jumplink-CIT0147"></span><a href="javascript:;" reveal-id="CIT0147" data-open="CIT0147" class="link link-ref link-reveal xref-bibr">Touraev <em>et al.</em>, 1996</a>; <span class="xrefLink" id="jumplink-CIT0115"></span><a href="javascript:;" reveal-id="CIT0115" data-open="CIT0115" class="link link-ref link-reveal xref-bibr">Shariatpanahi <em>et al.</em>, 2006</a>). After induction, the responsive microspores switch their developmental programme from the gametophytic to the embryogenic pathway, while many other microspores die during the first days of <em>in vitro</em> culture (<span class="xrefLink" id="jumplink-F1"></span><a href="javascript:;" data-modal-source-id="F1" class="link xref-fig">Fig. 1</a>) (<span class="xrefLink" id="jumplink-CIT0079"></span><a href="javascript:;" reveal-id="CIT0079" data-open="CIT0079" class="link link-ref link-reveal xref-bibr">Maraschin <em>et al.</em>, 2005</a>; <span class="xrefLink" id="jumplink-CIT0116"></span><a href="javascript:;" reveal-id="CIT0116" data-open="CIT0116" class="link link-ref link-reveal xref-bibr">Satpute <em>et al.</em>, 2005</a>; <span class="xrefLink" id="jumplink-CIT0112"></span><a href="javascript:;" reveal-id="CIT0112" data-open="CIT0112" class="link link-ref link-reveal xref-bibr">Rodríguez-Serrano <em>et al.</em>, 2012</a>). Efficient induction of microspore embryogenesis depends on multiple factors such as genotype, donor plant condition, composition of the culture media, and type of inductive stress applied. Besides these factors, the developmental stage of microspores is a critical parameter; the late vacuolated microspore stage (<span class="xrefLink" id="jumplink-F2"></span><a href="javascript:;" data-modal-source-id="F2" class="link xref-fig">Fig. 2A</a>) has been reported as the most responsive for embryogenesis induction in a wide range of plant species, including cereals and horticultural crops, as well as forest and fruit trees (<span class="xrefLink" id="jumplink-CIT0045"></span><a href="javascript:;" reveal-id="CIT0045" data-open="CIT0045" class="link link-ref link-reveal xref-bibr">González-Melendi <em>et al.</em>, 1995</a>; <span class="xrefLink" id="jumplink-CIT0017"></span><a href="javascript:;" reveal-id="CIT0017" data-open="CIT0017" class="link link-ref link-reveal xref-bibr">Bueno <em>et al.</em>, 2003</a>; <span class="xrefLink" id="jumplink-CIT0104"></span><a href="javascript:;" reveal-id="CIT0104" data-open="CIT0104" class="link link-ref link-reveal xref-bibr">Prem <em>et al.</em>, 2004</a>; <span class="xrefLink" id="jumplink-CIT0127"></span><a href="javascript:;" reveal-id="CIT0127" data-open="CIT0127" class="link link-ref link-reveal xref-bibr">Solís <em>et al.</em>, 2008</a>; <span class="xrefLink" id="jumplink-CIT0040"></span><a href="javascript:;" reveal-id="CIT0040" data-open="CIT0040" class="link link-ref link-reveal xref-bibr">Germanà, 2009</a>; <span class="xrefLink" id="jumplink-CIT0042"></span><a href="javascript:;" reveal-id="CIT0042" data-open="CIT0042" class="link link-ref link-reveal xref-bibr">Germanà <em>et al.</em>, 2011</a>; <span class="xrefLink" id="jumplink-CIT0105"></span><a href="javascript:;" reveal-id="CIT0105" data-open="CIT0105" class="link link-ref link-reveal xref-bibr">Prem <em>et al.</em>, 2012</a>). At the beginning of the process, the main limiting factors of initiation of microspore embryogenesis are high levels of cell death and low reprogramming efficiency.</p> <a id="136423275" scrollto-destination="136423275"></a> <div data-id="f2" data-content-id="f2" class="fig fig-section js-fig-section" swap-content-for-modal="true"><div class="graphic-wrap"><img class="content-image" src="https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/jxb/70/11/10.1093_jxb_ery464/1/m_exbotj_ery464_f0002.jpeg?Expires=1735137917&Signature=0e8P8EPEyLZpRooLDY9U5sJ~W61Qyt-lDb6nau5Z6wI84ZKhPGYN37JfIayrP69gflloswkEoHktgISi9LSBCigplFDuAluck4jXV8lbTlb0ZUKJhMaVfHaaErhF1ltVn7QYgTOxvxF2Erw7FNIAo7L9csux8qrFof-gzKUTho6BsKkV8pyxaNh1BlQoeMLpuip-fM8V5DYt1JjAZ1daC1pkFMWthp8Jgih77olewKXiXxeryXDrJE7zN2d6tB1G7FfQUuVseM2M1xwyEzANSeSCILRSsVYyBNfqn9OrkQhBYv39QybjcFxIGj~PeNR-hcnHEOXt7UHvblqFLAg-4g__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA" alt="Main stages of microspore embryogenesis in Brassica napus. (A) Vacuolated microspore at the beginning of the culture. (B) Proembryo formed after a few days (4–6 d) in culture, by several divisions of the microspore. (C) Globular, heart, and torpedo embryos developed from microspore cultures after 15–20 d in culture. (D) Cotyledonary embryos completely differentiated after 30 d in culture. (A, B) Micrographs of resin sections stained by toluidine blue. (C, D) Views from as tereomicroscope of embryos in Petri dishes of microspore cultures. Scale bars in (A, B): 20 µm; in (C, D): 1 mm." data-path-from-xml="exbotj_ery464_f0002.jpg" /><div class="graphic-bottom"><div class="label fig-label" id="label-136423275">Fig. 2.</div><div class="caption fig-caption"><p class="chapter-para">Main stages of microspore embryogenesis in <em>Brassica napus</em>. (A) Vacuolated microspore at the beginning of the culture. (B) Proembryo formed after a few days (4–6 d) in culture, by several divisions of the microspore. (C) Globular, heart, and torpedo embryos developed from microspore cultures after 15–20 d in culture. (D) Cotyledonary embryos completely differentiated after 30 d in culture. (A, B) Micrographs of resin sections stained by toluidine blue. (C, D) Views from as tereomicroscope of embryos in Petri dishes of microspore cultures. Scale bars in (A, B): 20 µm; in (C, D): 1 mm.</p></div><div class="ajax-articleAbstract-exclude-regex fig-orig original-slide figure-button-wrap"><a class="fig-view-orig js-view-large at-figureViewLarge openInAnotherWindow" role="button" aria-describedby="label-136423275" href="/view-large/figure/136423275/exbotj_ery464_f0002.jpg" data-path-from-xml="exbotj_ery464_f0002.jpg" target="_blank">Open in new tab</a><a class="download-slide" role="button" aria-describedby="label-136423275" data-section="136423275" href="/DownloadFile/DownloadImage.aspx?image=https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/jxb/70/11/10.1093_jxb_ery464/1/exbotj_ery464_f0002.jpeg?Expires=1735137917&Signature=KBpievo6Fuolsb58be5jSMV8qNQXbuoMASHEeaNyv1AHQ8lFp8ng2lkTn~u71hxkuhlor5p15Jd1F1qH~x55yVW1VRNHlp4Mv6Mg9Nu81rTv1TNsMuRxD2XxJORLv-1xTsRlsophD~fLmGhvALM-048Bd8GQe9hSURvVoZVTX1J0MwnV6idf3xXXRVHFQWKNWHvFfkN6QCgxiqMNjc9QooM~eRoYsRE~eC~op7fr5fIRUihytOFhXE-aZEBABrNiDOcqxGLAnnUJmsh5DSbjU49GmJ-YNElmIhSvcznTKZ4PT-E8u2iGYzEHdyWudXuUyaJZ-6kZUEuWve~7qamR~Q__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA&sec=136423275&ar=5310108&xsltPath=~/UI/app/XSLT&imagename=&siteId=5304" data-path-from-xml="exbotj_ery464_f0002.jpg">Download slide</a></div></div></div></div><p class="chapter-para">Stress-induced microspore embryogenesis is also an excellent <em>in vitro</em> system to study the regulatory mechanisms of cell reprogramming, totipotency, cell fate decisions, and early embryogenesis, since zygotes and immature embryos produced <em>in planta</em> are surrounded by maternal tissues and difficult to dissect. For decades, advances in plant <em>in vitro</em> protocols have been mostly based on trial-and-error approaches since the mechanisms underlying the induction of dedifferentiation of a somatic cell and its reprogramming and conversion into a totipotent embryogenic cell remain elusive. A better understanding of the processes involved in the induction of reprogramming and acquisition of embryogenic competence will help to identify new targets and design new strategies to improve the efficiency of <em>in vitro</em> embryogenesis systems, even in recalcitrant species.</p><p class="chapter-para">Two crop species, the monocot <em>Hordeum vulgare</em> (barley) and the eudicot <em>Brassica napus</em> (rapeseed), have been used as models for studying the celular and molecular basis of microspore embryogenesis. In these two species, there are efficient and well-established <em>in vitro</em> systems of stress-induced microspore embryogenesis using isolated microspores cultures (<span class="xrefLink" id="jumplink-CIT0093"></span><a href="javascript:;" reveal-id="CIT0093" data-open="CIT0093" class="link link-ref link-reveal xref-bibr">Pechan and Keller, 1988</a>; <span class="xrefLink" id="jumplink-CIT0066"></span><a href="javascript:;" reveal-id="CIT0066" data-open="CIT0066" class="link link-ref link-reveal xref-bibr">Kumlehn <em>et al.</em>, 2006</a>; <span class="xrefLink" id="jumplink-CIT0105"></span><a href="javascript:;" reveal-id="CIT0105" data-open="CIT0105" class="link link-ref link-reveal xref-bibr">Prem <em>et al.</em>, 2012</a>; <span class="xrefLink" id="jumplink-CIT0112"></span><a href="javascript:;" reveal-id="CIT0112" data-open="CIT0112" class="link link-ref link-reveal xref-bibr">Rodríguez-Serrano <em>et al.</em>, 2012</a>). Anther culture, on the other hand, is especially useful in biotechnological applications of many herbaceous crops and some woody species, including several fruit and forest trees, in which long regeneration times and strong inbreeding depression make traditional breeding methods impractical (<span class="xrefLink" id="jumplink-CIT0054"></span><a href="javascript:;" reveal-id="CIT0054" data-open="CIT0054" class="link link-ref link-reveal xref-bibr">Jain <em>et al</em>., 1996<em>a</em></a>, <em>b</em>, <em>c</em>, <em>d</em>, <em>e</em>; <span class="xrefLink" id="jumplink-CIT0018"></span><a href="javascript:;" reveal-id="CIT0018" data-open="CIT0018" class="link link-ref link-reveal xref-bibr">Touraev <em>et al.</em>, 2009</a>). <em>Citrus clementina</em> is one of the best examples of a fruit tree in which the regeneration of DHs by anther culture has been successful (<span class="xrefLink" id="jumplink-CIT0040"></span><a href="javascript:;" reveal-id="CIT0040" data-open="CIT0040" class="link link-ref link-reveal xref-bibr">Germanà, 2009</a>). Also, in cork oak (<em>Quercus suber</em> L.), successful microspore embryogenesis using anther cultures and embryo production protocols has been reported and later optimized (<span class="xrefLink" id="jumplink-CIT0016"></span><a href="javascript:;" reveal-id="CIT0016" data-open="CIT0016" class="link link-ref link-reveal xref-bibr">Bueno <em>et al.</em>, 1997</a>; <span class="xrefLink" id="jumplink-CIT0140"></span><a href="javascript:;" reveal-id="CIT0140" data-open="CIT0140" class="link link-ref link-reveal xref-bibr">Testillano <em>et al.</em>, 2018</a>). After induction and culture initiation, responsive microspores divide and produce multicellular structures or proembryos, still confined within the microspore wall (exine) (<span class="xrefLink" id="jumplink-F2"></span><a href="javascript:;" data-modal-source-id="F2" class="link xref-fig">Fig. 2B</a>). Such structures are considered to be an early sign of initiation of embryogenesis. As embryogenesis progresses, the exine breaks down, and embryos develop following a similar pathway to zygotic embryogenesis, producing globular, heart, torpedo (<span class="xrefLink" id="jumplink-F2"></span><a href="javascript:;" data-modal-source-id="F2" class="link xref-fig">Fig. 2C</a>), and cotyledonary embryos (<span class="xrefLink" id="jumplink-F2"></span><a href="javascript:;" data-modal-source-id="F2" class="link xref-fig">Fig. 2D</a>) in the case of dicot species, and globular, transitional, scutellar, and coleoptilar embryos in the case of monocot plants. Microspore-derived embryos can germinate under appropriate culture conditions and further regenerate plants which can be acclimatized and grown in soil. Haploid plants grow normally and produce flowers that are completely sterile and often show malformations (<span class="xrefLink" id="jumplink-CIT0089"></span><a href="javascript:;" reveal-id="CIT0089" data-open="CIT0089" class="link link-ref link-reveal xref-bibr">Murovec and Bohanec, 2012</a>). Depending on the species, spontaneous diploidization can occur in a proportion of regenerated plants. In cereals, the rate of spontaneous diploidization is high, whereas in vegetables and trees it is much lower, and chemical treatments with drugs, such as colchicine, oryzalin, amiprophosmethyl, trifluralin, or pronamide, should be applied during DH production (<span class="xrefLink" id="jumplink-CIT0054"></span><a href="javascript:;" reveal-id="CIT0054" data-open="CIT0054" class="link link-ref link-reveal xref-bibr">Jain <em>et al</em>., 1996<em>a</em></a>; <span class="xrefLink" id="jumplink-CIT0010"></span><a href="javascript:;" reveal-id="CIT0010" data-open="CIT0010" class="link link-ref link-reveal xref-bibr">Barnabás <em>et al.</em>, 1999</a>; <span class="xrefLink" id="jumplink-CIT0101"></span><a href="javascript:;" reveal-id="CIT0101" data-open="CIT0101" class="link link-ref link-reveal xref-bibr">Pintos <em>et al.</em>, 2007</a>; <span class="xrefLink" id="jumplink-CIT0089"></span><a href="javascript:;" reveal-id="CIT0089" data-open="CIT0089" class="link link-ref link-reveal xref-bibr">Murovec and Bohanec, 2012</a>). The frequency of spontaneous genome doubling has been reported to be up to 40–50% in <em>Brassica napus</em>, 40% in maize, 60% in rice, and 90% in barley and rye (<span class="xrefLink" id="jumplink-CIT0018"></span><a href="javascript:;" reveal-id="CIT0018" data-open="CIT0018" class="link link-ref link-reveal xref-bibr">Castillo <em>et al.</em>, 2009</a>; <span class="xrefLink" id="jumplink-CIT0105"></span><a href="javascript:;" reveal-id="CIT0105" data-open="CIT0105" class="link link-ref link-reveal xref-bibr">Prem <em>et al.</em>, 2012</a>; <span class="xrefLink" id="jumplink-CIT0107"></span><a href="javascript:;" reveal-id="CIT0107" data-open="CIT0107" class="link link-ref link-reveal xref-bibr">Ren <em>et al.</em>, 2017</a>), with nuclear fusion as the main mechanism for spontaneous diploidization in cereal species (<span class="xrefLink" id="jumplink-CIT0061"></span><a href="javascript:;" reveal-id="CIT0061" data-open="CIT0061" class="link link-ref link-reveal xref-bibr">Kasha <em>et al</em>., 2001</a>, <span class="xrefLink" id="jumplink-CIT0062"></span><a href="javascript:;" reveal-id="CIT0062" data-open="CIT0062" class="link link-ref link-reveal xref-bibr">2005</a>; <span class="xrefLink" id="jumplink-CIT0136"></span><a href="javascript:;" reveal-id="CIT0136" data-open="CIT0136" class="link link-ref link-reveal xref-bibr">Testillano <em>et al.</em>, 2004</a>; <span class="xrefLink" id="jumplink-CIT0046"></span><a href="javascript:;" reveal-id="CIT0046" data-open="CIT0046" class="link link-ref link-reveal xref-bibr">González-Melendi <em>et al.</em>, 2005</a>).</p><p class="chapter-para">Our understanding of the cellular and molecular basis of induction of microspore embryogenesis has improved in recent years; however, the mechanism underlying the change in microspore cell fate is still largely unknown. Advances in this area have been hampered by several factors such as: (i) the difficulty involved in applying genetic approaches (genotypes that are responsive to embryogenesis cannot be efficiently transformed, lack of transformation procedures, lack of mutants in many crop species, etc.); (ii) recalcitrance of the model plant Arabidopsis to induction of microspore embryogenesis; and (iii) the difficulty in dissecting early developmental stages of the process for analyses by molecular and biochemical approaches. After induction, a high proportion of non-responsive microspores co-exist in the <em>in vitro</em> culture, with a much lower percentage of responsive microspores that start to divide, producing multicellular microspores/proembryos, and separation of these early embryogenic structures is technically very difficult at the onset of initiation of embryogenesis. Cellular approaches using <em>in situ</em> molecular identification techniques have provided unique information by localizing key molecules and differential gene expression in microspore embryogenic structures from the very initial stages, by advanced imaging microscopy technologies (<span class="xrefLink" id="jumplink-CIT0142"></span><a href="javascript:;" reveal-id="CIT0142" data-open="CIT0142" class="link link-ref link-reveal xref-bibr">Testillano and Risueño, 2009</a>; <span class="xrefLink" id="jumplink-CIT0143"></span><a href="javascript:;" reveal-id="CIT0143" data-open="CIT0143" class="link link-ref link-reveal xref-bibr">Testillano and Rodríguez, 2012</a>; <span class="xrefLink" id="jumplink-CIT0111"></span><a href="javascript:;" reveal-id="CIT0111" data-open="CIT0111" class="link link-ref link-reveal xref-bibr">Rodríguez-Sanz <em>et al</em>., 2015</a>)—methodologies that permit very early embryogenic structures (2–3 cells) to be distinguished from non-embryogenic structures. Changes in various cell activities and rearrangements in the structural organization of subcellular compartments have been shown to accompany the microspore reprogramming process in several herbaceous and woody species (<span class="xrefLink" id="jumplink-CIT0135"></span><a href="javascript:;" reveal-id="CIT0135" data-open="CIT0135" class="link link-ref link-reveal xref-bibr">Telmer <em>et al.</em>, 1995</a>; <span class="xrefLink" id="jumplink-CIT0137"></span><a href="javascript:;" reveal-id="CIT0137" data-open="CIT0137" class="link link-ref link-reveal xref-bibr">Testillano <em>et al.</em>, 2000</a>, 2002; <span class="xrefLink" id="jumplink-CIT0008"></span><a href="javascript:;" reveal-id="CIT0008" data-open="CIT0008" class="link link-ref link-reveal xref-bibr">Bárány <em>et al.</em>, 2005</a>; <span class="xrefLink" id="jumplink-CIT0118"></span><a href="javascript:;" reveal-id="CIT0118" data-open="CIT0118" class="link link-ref link-reveal xref-bibr">Seguí-Simarro <em>et al.</em>, 2006</a>; <span class="xrefLink" id="jumplink-CIT0127"></span><a href="javascript:;" reveal-id="CIT0127" data-open="CIT0127" class="link link-ref link-reveal xref-bibr">Solís <em>et al.</em>, 2008</a>), and some common features in the developmental pattern among species have been identified, as well as species-specific features of woody plants (<span class="xrefLink" id="jumplink-CIT0109"></span><a href="javascript:;" reveal-id="CIT0109" data-open="CIT0109" class="link link-ref link-reveal xref-bibr">Rodríguez-Sanz <em>et al</em>., 2014<em>a</em></a>; <span class="xrefLink" id="jumplink-CIT0023"></span><a href="javascript:;" reveal-id="CIT0023" data-open="CIT0023" class="link link-ref link-reveal xref-bibr">Chiancone <em>et al.</em>, 2015</a>).</p><p class="chapter-para">Here, we will review recent findings regarding the determinant factors that underlie stress-induced initiation and progression of microspore embryogenesis, with special emphasis on the role of autophagy, cell death, endogenous auxin, chromatin modifications, and cell wall remodelling. Information gained over the last few years has also shown that the modulation of these determinant factors by small bioactive molecules affects the process yield, emerging as a promising strategy to improve the efficiency of microspore embryogenesis (<span class="xrefLink" id="jumplink-CIT0126"></span><a href="javascript:;" reveal-id="CIT0126" data-open="CIT0126" class="link link-ref link-reveal xref-bibr">Solís <em>et al</em>., 2015</a>; <span class="xrefLink" id="jumplink-CIT0012"></span><a href="javascript:;" reveal-id="CIT0012" data-open="CIT0012" class="link link-ref link-reveal xref-bibr">Berenguer <em>et al.</em>, 2017</a>; <span class="xrefLink" id="jumplink-CIT0005"></span><a href="javascript:;" reveal-id="CIT0005" data-open="CIT0005" class="link link-ref link-reveal xref-bibr">Bárány <em>et al</em>., 2018</a>; <span class="xrefLink" id="jumplink-CIT0097"></span><a href="javascript:;" reveal-id="CIT0097" data-open="CIT0097" class="link link-ref link-reveal xref-bibr">Pérez-Pérez <em>et al.</em>, 2019<em>a</em></a>). This has opened up a completely new intervention pathway to increase the efficiency of the <em>in vitro</em> production of embryos and DH plants in crop and forest species, especially recalcitrant species, with the aim being their application in breeding programmes.</p> <h2 scrollto-destination=136423280 id="136423280" class="section-title js-splitscreen-section-title" data-legacy-id=s2>Stress-induced cell death, autophagy, and proteases</h2> <p class="chapter-para">Stress treatments are necessary to produce the embryogenic response of microspores. Cold and mild heat treatments are the most frequently used conditions to induce microspore embryogenesis in many plant species (<span class="xrefLink" id="jumplink-CIT0077"></span><a href="javascript:;" reveal-id="CIT0077" data-open="CIT0077" class="link link-ref link-reveal xref-bibr">Maluszynski <em>et al</em>., 2003</a>; <span class="xrefLink" id="jumplink-CIT0115"></span><a href="javascript:;" reveal-id="CIT0115" data-open="CIT0115" class="link link-ref link-reveal xref-bibr">Shariatpanahi <em>et al.</em>, 2006</a>). In the model systems of <em>B. napus</em> (rapeseed) and <em>H. vulgare</em> (barley), the inductive stress treatments are 32 °C and 4 °C, respectively. The expression of some stress-related proteins, such as heat-shock proteins HSP70 and HSP90, has been reported in microspore embryogenesis cultures of <em>B. napus</em> and <em>Capsicum annum</em> (<span class="xrefLink" id="jumplink-CIT0021"></span><a href="javascript:;" reveal-id="CIT0021" data-open="CIT0021" class="link link-ref link-reveal xref-bibr">Cordewener <em>et al.</em>, 1995</a>, <span class="xrefLink" id="jumplink-CIT0020"></span><a href="javascript:;" reveal-id="CIT0020" data-open="CIT0020" class="link link-ref link-reveal xref-bibr">2000</a>; <span class="xrefLink" id="jumplink-CIT0009"></span><a href="javascript:;" reveal-id="CIT0009" data-open="CIT0009" class="link link-ref link-reveal xref-bibr">Bárány <em>et al.</em>, 2001</a>; <span class="xrefLink" id="jumplink-CIT0120"></span><a href="javascript:;" reveal-id="CIT0120" data-open="CIT0120" class="link link-ref link-reveal xref-bibr">Seguí-Simarro <em>et al.</em>, 2003</a>); although a protective role for these chaperones in response to stress has been suggested, their role in microspore embryogenesis is not clear.</p><p class="chapter-para">Analyses of cell viability have shown that there is a marked increase in cell death levels after stress treatment in several microspore embryogenesis systems (<span class="xrefLink" id="jumplink-CIT0112"></span><a href="javascript:;" reveal-id="CIT0112" data-open="CIT0112" class="link link-ref link-reveal xref-bibr">Rodríguez-Serrano <em>et al.</em>, 2012</a>; <span class="xrefLink" id="jumplink-CIT0097"></span><a href="javascript:;" reveal-id="CIT0097" data-open="CIT0097" class="link link-ref link-reveal xref-bibr">Pérez-Pérez <em>et al.</em>, 2019<em>a</em></a>). The inductive stress for microspore embryogenesis also leads to oxidative stress, with the production of reactive oxygen species (ROS; <span class="xrefLink" id="jumplink-CIT0163"></span><a href="javascript:;" reveal-id="CIT0163" data-open="CIT0163" class="link link-ref link-reveal xref-bibr">Zur <em>et al.</em>, 2009</a>; <span class="xrefLink" id="jumplink-CIT0112"></span><a href="javascript:;" reveal-id="CIT0112" data-open="CIT0112" class="link link-ref link-reveal xref-bibr">Rodríguez-Serrano <em>et al.</em>, 2012</a>). The balance between ROS-producing and ROS-scavenging endogenous mechanisms determines the level of oxidative stress and damage in the cell, leading to cell death when it surpasses a certain threshold (<span class="xrefLink" id="jumplink-CIT0019"></span><a href="javascript:;" reveal-id="CIT0019" data-open="CIT0019" class="link link-ref link-reveal xref-bibr">Clarke <em>et al.</em>, 2000</a>). The ability to control oxidative stress to prevent cellular oxidative damage and maintain cell homeostasis is a key factor for stress-induced microspore embryogenesis. In this sense, several enzymes of the antioxidative machinery of the cell have been found to increase their activity/expression in microspore cultures, with a protective role being suggested for these stress-related proteins (<span class="xrefLink" id="jumplink-CIT0078"></span><a href="javascript:;" reveal-id="CIT0078" data-open="CIT0078" class="link link-ref link-reveal xref-bibr">Maraschin <em>et al.</em>, 2006</a>; <span class="xrefLink" id="jumplink-CIT0088"></span><a href="javascript:;" reveal-id="CIT0088" data-open="CIT0088" class="link link-ref link-reveal xref-bibr">Muñoz-Amatriain <em>et al.</em>, 2006</a>; <span class="xrefLink" id="jumplink-CIT0163"></span><a href="javascript:;" reveal-id="CIT0163" data-open="CIT0163" class="link link-ref link-reveal xref-bibr">Zur <em>et al.</em>, 2009</a>; <span class="xrefLink" id="jumplink-CIT0149"></span><a href="javascript:;" reveal-id="CIT0149" data-open="CIT0149" class="link link-ref link-reveal xref-bibr">Uvácková <em>et al.</em>, 2012</a>).</p><p class="chapter-para">Autophagy, which is a major catabolic pathway for recycling cell materials, has many different functions under stress conditions or during specific developmental processes (reviewed in <span class="xrefLink" id="jumplink-CIT0053"></span><a href="javascript:;" reveal-id="CIT0053" data-open="CIT0053" class="link link-ref link-reveal xref-bibr">Hofius <em>et al.</em>, 2017</a>; <span class="xrefLink" id="jumplink-CIT0080"></span><a href="javascript:;" reveal-id="CIT0080" data-open="CIT0080" class="link link-ref link-reveal xref-bibr">Masclaux-Daubresse <em>et al.</em>, 2017</a>; <span class="xrefLink" id="jumplink-CIT0001"></span><a href="javascript:;" reveal-id="CIT0001" data-open="CIT0001" class="link link-ref link-reveal xref-bibr">Avin-Wittenberg <em>et al.</em>, 2018</a>). In plants, autophagy has been shown to have a role in promoting cell survival under starvation and stress conditions, as well as in cell death initiation and/or execution (<span class="xrefLink" id="jumplink-CIT0083"></span><a href="javascript:;" reveal-id="CIT0083" data-open="CIT0083" class="link link-ref link-reveal xref-bibr">Minina <em>et al.</em>, 2013</a>, 2014; <span class="xrefLink" id="jumplink-CIT0001"></span><a href="javascript:;" reveal-id="CIT0001" data-open="CIT0001" class="link link-ref link-reveal xref-bibr">Avin-Wittenberg, 2018</a>; <span class="xrefLink" id="jumplink-CIT0001"></span><a href="javascript:;" reveal-id="CIT0001" data-open="CIT0001" class="link link-ref link-reveal xref-bibr">Avin-Wittenberg <em>et al.</em>, 2018</a>). Increasing evidence has connected ROS and autophagy in plants and algae (<span class="xrefLink" id="jumplink-CIT0096"></span><a href="javascript:;" reveal-id="CIT0096" data-open="CIT0096" class="link link-ref link-reveal xref-bibr">Pérez-Pérez <em>et al</em>., 2012</a>). Induction of autophagy has been shown in response to ROS treatments (<span class="xrefLink" id="jumplink-CIT0095"></span><a href="javascript:;" reveal-id="CIT0095" data-open="CIT0095" class="link link-ref link-reveal xref-bibr">Pérez-Pérez <em>et al</em>., 2010</a>). A recent study on barley microspore embryogenesis reported the activation of autophagy after an inductive stress at 4 °C (<span class="xrefLink" id="jumplink-CIT0011"></span><a href="javascript:;" reveal-id="CIT0011" data-open="CIT0011" class="link link-ref link-reveal xref-bibr">Bárány <em>et al.</em>, 2018</a>). Stress-treated microspores showed up-regulation of autophagy genes <em>HvATG5</em> and <em>HvATG6</em>, and an increase in the number of autophagosomes which were labelled by ATG5 and ATG8 antibodies (<span class="xrefLink" id="jumplink-F3"></span><a href="javascript:;" data-modal-source-id="F3" class="link xref-fig">Fig. 3</a>), and exhibited the typical ultrastructure of autophagosomes under electron microscopy (<span class="xrefLink" id="jumplink-CIT0011"></span><a href="javascript:;" reveal-id="CIT0011" data-open="CIT0011" class="link link-ref link-reveal xref-bibr">Bárány <em>et al.</em>, 2018</a>).</p> <a id="136423284" scrollto-destination="136423284"></a> <div data-id="f3" data-content-id="f3" class="fig fig-section js-fig-section" swap-content-for-modal="true"><div class="graphic-wrap"><img class="content-image" src="https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/jxb/70/11/10.1093_jxb_ery464/1/m_exbotj_ery464_f0003.jpeg?Expires=1735137917&Signature=bDYNbJweccccaHacyEBldeqIawafdhh7EYAaOV0Xgmhg~s33kZAcSN3rfMp265lqRNnMhynnjRpgLA2nauALgz37EKItA9uyBpBWptOH~c-pTQ--pC4i~rZxc9-mi0WCJULu84f6anYjctDfO0zskAHfYSrBAXKBg5hB5MlKxm35d5cP4EPdIJE~7SlLpBDIY-i55h8q1CRx-bVBAuUVdItoKea80zn9Mkv-H08FdHmstcuyKWXdEIfQy1iycESbUAlGQi9QDTEYX0ZA42wm4g80QSYHNpP1G3J9WmOoZc9I0B2WRLIjQllyUe66rKo6oLtIr4MzJ70jSS5SGyDSFQ__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA" alt="Autophagy induction in stress-induced microspore embryogenesis of Hordeum vulgare. Confocal microscopy merged images of localization of ATG8 protein in autophagosomes (green) by immunofluorescence with ATG8 antibodies (Abcam) and nuclei stained with DAPI (blue). (A) Microspore before the stress treatment, with no ATG8 signal. (B) Stress-treated microspore showing ATG8 labelling on numerous small cytoplasmic spots, corresponding to autophagosomes. Scale bars=20 µm." data-path-from-xml="exbotj_ery464_f0003.jpg" /><div class="graphic-bottom"><div class="label fig-label" id="label-136423284">Fig. 3.</div><div class="caption fig-caption"><p class="chapter-para">Autophagy induction in stress-induced microspore embryogenesis of <em>Hordeum vulgare</em>. Confocal microscopy merged images of localization of ATG8 protein in autophagosomes (green) by immunofluorescence with ATG8 antibodies (Abcam) and nuclei stained with DAPI (blue). (A) Microspore before the stress treatment, with no ATG8 signal. (B) Stress-treated microspore showing ATG8 labelling on numerous small cytoplasmic spots, corresponding to autophagosomes. Scale bars=20 µm.</p></div><div class="ajax-articleAbstract-exclude-regex fig-orig original-slide figure-button-wrap"><a class="fig-view-orig js-view-large at-figureViewLarge openInAnotherWindow" role="button" aria-describedby="label-136423284" href="/view-large/figure/136423284/exbotj_ery464_f0003.jpg" data-path-from-xml="exbotj_ery464_f0003.jpg" target="_blank">Open in new tab</a><a class="download-slide" role="button" aria-describedby="label-136423284" data-section="136423284" href="/DownloadFile/DownloadImage.aspx?image=https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/jxb/70/11/10.1093_jxb_ery464/1/exbotj_ery464_f0003.jpeg?Expires=1735137917&Signature=mdC~xEmpQJjtvwxEYGxyxeGNfeC9KYrj9bG8c9hKdYH6U4FRZV4rb-ginq9ffl3MEn580b240xzmqqoWTUxRkcdS8X3iVZUPKPnyNUBAG-XwuuPMz0G~MAJXe20MuDyAnHEuclOeZwpTcl78slYTv8HIhL6loDwQ8n1PaIgKBMtUxf9eSSrBsqBAcYqdqfFxJgWXLWlOxDppAFyYDHags2q~9u7hUpD-mgxy94Ec25GPHMDOEgTCdXQp5o-plqU-76RQ9lTirCE~SoN5r~K8~6hzTT01X0fKzimuovCQvPmKCFPTQymxADKMgvkr6TgjKxn5sKuJRVVg82oUFYBGWA__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA&sec=136423284&ar=5310108&xsltPath=~/UI/app/XSLT&imagename=&siteId=5304" data-path-from-xml="exbotj_ery464_f0003.jpg">Download slide</a></div></div></div></div><p class="chapter-para">The plant proteolytic machinery comprises a large number of proteases that regulate cell homeostasis, and many of them have been shown to play key roles in both autophagy and cell death processes (<span class="xrefLink" id="jumplink-CIT0150"></span><a href="javascript:;" reveal-id="CIT0150" data-open="CIT0150" class="link link-ref link-reveal xref-bibr">van Der Hoorn and Jones, 2004</a>; <span class="xrefLink" id="jumplink-CIT0151"></span><a href="javascript:;" reveal-id="CIT0151" data-open="CIT0151" class="link link-ref link-reveal xref-bibr">van der Hoorn and Rivas, 2018</a>). Papain-like C1A cysteine proteases (PLCPs or cathepsins) are the most abundant enzymes with a role in plant senescence, programmed cell death (PCD), and proteolysis mediated by stress (<span class="xrefLink" id="jumplink-CIT0027"></span><a href="javascript:;" reveal-id="CIT0027" data-open="CIT0027" class="link link-ref link-reveal xref-bibr">Díaz-Mendoza <em>et al.</em>, 2016</a>; <span class="xrefLink" id="jumplink-CIT0154"></span><a href="javascript:;" reveal-id="CIT0154" data-open="CIT0154" class="link link-ref link-reveal xref-bibr">Velasco-Arroyo <em>et al.</em>, 2016</a>). In animals, cathepsins are well known lysosomal proteases with a role in autophagy and cell death (<span class="xrefLink" id="jumplink-CIT0148"></span><a href="javascript:;" reveal-id="CIT0148" data-open="CIT0148" class="link link-ref link-reveal xref-bibr">Turk and Stoka, 2007</a>), although in plants PLCP function in autophagy has not yet been demonstrated directly. Studies on cell death-related proteases involved in the stress response of barley microspores have revealed that cathepsin L/F-, B-, and H-like activities were induced after stress, and cathepsin-like genes <em>HvPap-1</em> and <em>HvPap-6</em> were up-regulated (<span class="xrefLink" id="jumplink-CIT0005"></span><a href="javascript:;" reveal-id="CIT0005" data-open="CIT0005" class="link link-ref link-reveal xref-bibr">Bárány <em>et al.</em>, 2018</a>). Caspases are another important group of cell death proteases. Despite the fact that plant genomes do not contain structural homologues of caspases, caspase-like activities have been detected in many plant species, and are required for PCD execution (<span class="xrefLink" id="jumplink-CIT0082"></span><a href="javascript:;" reveal-id="CIT0082" data-open="CIT0082" class="link link-ref link-reveal xref-bibr">Minina <em>et al.</em>, 2017</a>). Plant metacaspases constitute a major protease group of the large C14B family of proteases with relevant roles in PCD and autophagy (<span class="xrefLink" id="jumplink-CIT0083"></span><a href="javascript:;" reveal-id="CIT0083" data-open="CIT0083" class="link link-ref link-reveal xref-bibr">Minina <em>et al.</em>, 2013</a>, 2017). Preliminary results regarding <em>B. napus</em> microspore embryogenesis have revealed that the stress treatment of 32 °C, used to induce embryogenesis, leads to activation of autophagy, and induction of metacaspase enzymatic activity and gene expression (<span class="xrefLink" id="jumplink-CIT0005"></span><a href="javascript:;" reveal-id="CIT0005" data-open="CIT0005" class="link link-ref link-reveal xref-bibr">Berenguer <em>et al.</em>, 2018</a>).</p><p class="chapter-para">Interestingly, pharmacological treatments with inhibitors of ROS (MnCl<sub>2</sub> and ascorbate), autophagy [3-methyladenine (3-MA) and concanamycin A], and protease activities, particularly PLCP, caspase 3-like, and metacaspase activities (E64, Ac-DEVD-CHO, and Ac-VRPR-FMK), lead to the reduction of cell death levels, and consequently an increase in the embryogenesis initiation rate in stress-induced microspore embryogenesis cultures of rapeseed and barley (<span class="xrefLink" id="jumplink-CIT0005"></span><a href="javascript:;" reveal-id="CIT0005" data-open="CIT0005" class="link link-ref link-reveal xref-bibr">Bárány <em>et al</em>., 2018</a>; <span class="xrefLink" id="jumplink-CIT0097"></span><a href="javascript:;" reveal-id="CIT0097" data-open="CIT0097" class="link link-ref link-reveal xref-bibr">Pérez-Pérez <em>et al.</em>, 2019<em>a</em></a>). These findings reveal the implication of autophagy in cell death of microspores after the inductive stress, as well as the participation of cathepsin and caspase 3-like proteolytic activities. Further work will be necessary to explore whether autophagy can also play a role in promoting cell viability in response to stress in a certain population of microspores, as is the case in other plant cells (<span class="xrefLink" id="jumplink-CIT0001"></span><a href="javascript:;" reveal-id="CIT0001" data-open="CIT0001" class="link link-ref link-reveal xref-bibr">Avin-Wittenberg, 2018</a>), a possibility that cannot be ruled out. These findings also open up new intervention pathways to reduce stress-induced cell death levels at early stages of microspore embryogenesis by modulating autophagy and protease activities.</p> <h2 scrollto-destination=136423287 id="136423287" class="section-title js-splitscreen-section-title" data-legacy-id=s3>Endogenous auxin</h2> <p class="chapter-para">Among plant growth regulators, auxin is the most significant hormone in plant development and it is the key regulator of cell division and differentiation (<span class="xrefLink" id="jumplink-CIT0134"></span><a href="javascript:;" reveal-id="CIT0134" data-open="CIT0134" class="link link-ref link-reveal xref-bibr">Teale <em>et al.</em>, 2006</a>; <span class="xrefLink" id="jumplink-CIT0156"></span><a href="javascript:;" reveal-id="CIT0156" data-open="CIT0156" class="link link-ref link-reveal xref-bibr">Weijers <em>et al.</em>, 2018</a>). The induction of most somatic embryogenesis systems, from cells other than microspores, is mostly triggered by exogenous hormones, and this is commonly achieved using the synthetic auxin 2,4-dichlorophenoxyacetic acid (2,4-D), as well as via stress treatments (<span class="xrefLink" id="jumplink-CIT0036"></span><a href="javascript:;" reveal-id="CIT0036" data-open="CIT0036" class="link link-ref link-reveal xref-bibr">Feher, 2015</a>). On the contrary, the majority of microspore embryogenesis systems do not require exogenous auxin as an inducer, whereas a transient physical (thermal) or chemical stress is essential to trigger the change of developmental cell fate, probably as a response guided by endogenous hormones. In the case of anther culture, some protocols include growth regulators in their media composition. In this sense, microspore embryogenesis using isolated microspore cultures represents a convenient system for analysing the endogenous hormone function during <em>in vitro</em> initiation and progression of embryogenesis, since the process is induced and the embryo is differentiated <em>in vitro</em> from individual isolated cells without the addition of auxin or other hormones at any stage.</p><p class="chapter-para">Auxin action depends on its local biosynthesis and differential distribution within plant tissues, mainly regulated by its polar transport among cells (<span class="xrefLink" id="jumplink-CIT0100"></span><a href="javascript:;" reveal-id="CIT0100" data-open="CIT0100" class="link link-ref link-reveal xref-bibr">Petrasek and Friml, 2009</a>). Different pathways leading from auxin perception to gene expression and to non-transcriptional responses have been identified in recent decades, although many aspects of the complex mechanisms of signalling and action involved remain elusive (<span class="xrefLink" id="jumplink-CIT0156"></span><a href="javascript:;" reveal-id="CIT0156" data-open="CIT0156" class="link link-ref link-reveal xref-bibr">Weijers <em>et al.</em>, 2018</a>). The key components of auxin biosynthesis, transport, and signalling have been elucidated (reviewed in <span class="xrefLink" id="jumplink-CIT0070"></span><a href="javascript:;" reveal-id="CIT0070" data-open="CIT0070" class="link link-ref link-reveal xref-bibr">Li <em>et al.</em>, 2016</a>; <span class="xrefLink" id="jumplink-CIT0085"></span><a href="javascript:;" reveal-id="CIT0085" data-open="CIT0085" class="link link-ref link-reveal xref-bibr">Mironova <em>et al.</em>, 2017</a>); among them, the genes of auxin biosynthesis <em>TAA1</em> and <em>YUC</em>, the efflux carrier <em>PIN1</em> gene, and the auxin response factor (<em>ARF</em>) genes are all crucial elements in the control of auxin action (<span class="xrefLink" id="jumplink-CIT0070"></span><a href="javascript:;" reveal-id="CIT0070" data-open="CIT0070" class="link link-ref link-reveal xref-bibr">Li <em>et al.</em>, 2016</a>). During zygotic embryogenesis <em>in planta</em>, the major form of auxin, indole acetic acid (IAA), has demonstrated key functions, particularly in embryo patterning, polarization, and differentiation (<span class="xrefLink" id="jumplink-CIT0086"></span><a href="javascript:;" reveal-id="CIT0086" data-open="CIT0086" class="link link-ref link-reveal xref-bibr">Moller and Weijers, 2009</a>; <span class="xrefLink" id="jumplink-CIT0106"></span><a href="javascript:;" reveal-id="CIT0106" data-open="CIT0106" class="link link-ref link-reveal xref-bibr">Rademacher <em>et al.</em>, 2012</a>).</p><p class="chapter-para">Several studies have shown endogenous auxin accumulation in early microspore embryo cells of <em>B. napus</em> and <em>Quercus suber</em> (<span class="xrefLink" id="jumplink-CIT0105"></span><a href="javascript:;" reveal-id="CIT0105" data-open="CIT0105" class="link link-ref link-reveal xref-bibr">Prem <em>et al.</em>, 2012</a>; <span class="xrefLink" id="jumplink-CIT0111"></span><a href="javascript:;" reveal-id="CIT0111" data-open="CIT0111" class="link link-ref link-reveal xref-bibr">Rodríguez-Sanz <em>et al</em>., 2015</a>), as well as in <em>H. vulgare</em> (<span class="xrefLink" id="jumplink-CIT0032"></span><a href="javascript:;" reveal-id="CIT0032" data-open="CIT0032" class="link link-ref link-reveal xref-bibr">El-Tantawy, 2016</a>); other studies have localized auxin response in microspore embryos of <em>B. napus</em> (<span class="xrefLink" id="jumplink-CIT0029"></span><a href="javascript:;" reveal-id="CIT0029" data-open="CIT0029" class="link link-ref link-reveal xref-bibr">Dubas <em>et al.</em>, 2014</a>; <span class="xrefLink" id="jumplink-CIT0130"></span><a href="javascript:;" reveal-id="CIT0130" data-open="CIT0130" class="link link-ref link-reveal xref-bibr">Soriano <em>et al.</em>, 2014</a>) by expression of the DR5-auxin reporter. In addition, various reports have documented that abiotic stress factors can impact on auxin homeostasis, leading to a wide range of plant cell responses (<span class="xrefLink" id="jumplink-CIT0103"></span><a href="javascript:;" reveal-id="CIT0103" data-open="CIT0103" class="link link-ref link-reveal xref-bibr">Potters <em>et al.</em>, 2007</a>; <span class="xrefLink" id="jumplink-CIT0145"></span><a href="javascript:;" reveal-id="CIT0145" data-open="CIT0145" class="link link-ref link-reveal xref-bibr">Tognetti <em>et al.</em>, 2012</a>; <span class="xrefLink" id="jumplink-CIT0025"></span><a href="javascript:;" reveal-id="CIT0025" data-open="CIT0025" class="link link-ref link-reveal xref-bibr">da Costa <em>et al.</em>, 2013</a>). Interactions between stress signalling and hormones, particularly auxin, have been proposed to lead to induction of somatic embryogenesis (<span class="xrefLink" id="jumplink-CIT0036"></span><a href="javascript:;" reveal-id="CIT0036" data-open="CIT0036" class="link link-ref link-reveal xref-bibr">Feher, 2015</a>). Recent studies have revealed the involvement of endogenous auxin in microspore reprogramming and <em>in vitro</em> embryo formation in <em>B. napus</em>. After induction of microspore embryogenesis, <em>de novo</em> endogenous auxin biosynthesis and early accumulation of IAA in proembryo cells are detected, from the first embryogenic divisions (<span class="xrefLink" id="jumplink-CIT0111"></span><a href="javascript:;" reveal-id="CIT0111" data-open="CIT0111" class="link link-ref link-reveal xref-bibr">Rodríguez-Sanz <em>et al</em>., 2015</a>). Moreover, expression of both <em>BnTAA1</em> and <em>BnPIN1</em> is up-regulated throughout initiation and progression of microspore embryogenesis, correlating with the increase in IAA concentration. Pharmacological treatments with inhibitors of auxin action, <em>p</em>-chloroiodobenzene (PCIB); polar transport, 1-<em>N</em>-naphthylphthalamic acid (NPA) (<span class="xrefLink" id="jumplink-CIT0109"></span><a href="javascript:;" reveal-id="CIT0109" data-open="CIT0109" class="link link-ref link-reveal xref-bibr">Rodríguez-Sanz <em>et al</em>., 2014<em>a</em></a>; <span class="xrefLink" id="jumplink-CIT0111"></span><a href="javascript:;" reveal-id="CIT0111" data-open="CIT0111" class="link link-ref link-reveal xref-bibr">, 2015</a>); and biosynthesis, kynurenin (Y. Pérez-Pérez and P.S. Testillano, unpublished) severely disturb initiation and progression of microspore embryogenesis, resulting in a significant reduction in embryo production yield (<span class="xrefLink" id="jumplink-CIT0111"></span><a href="javascript:;" reveal-id="CIT0111" data-open="CIT0111" class="link link-ref link-reveal xref-bibr">Rodríguez-Sanz <em>et al</em>., 2015</a>). These findings clearly indicate that auxin biosynthesis, activity, and transport are required for stress-induced microspore embryogenesis.</p><p class="chapter-para">Together with auxin, cytokinin is a key regulator of plant growth and development. The balance of these two hormones, which usually act antagonistically, controls cell division and differentiation. In recent years, several studies have revealed the inter-relationship of auxin and cytokinin signalling pathways, and the importance of their concentration balance and antagonistic effects as key factors for cell fate, proliferation, and differentiation (<span class="xrefLink" id="jumplink-CIT0099"></span><a href="javascript:;" reveal-id="CIT0099" data-open="CIT0099" class="link link-ref link-reveal xref-bibr">Periañez-Rodríguez <em>et al.</em>, 2014</a>). In comparison with auxin, less is known about the biosynthesis, signalling pathway, and transport of cytokinins (Durán-Medina <em>et al.</em>, 2017). Recent studies have shown that establishment of the spatiotemporal distribution of auxin and cytokinin response signals is central for the control of early somatic embryogenesis and meristem initiation in Arabidopsis (<span class="xrefLink" id="jumplink-CIT0131"></span><a href="javascript:;" reveal-id="CIT0131" data-open="CIT0131" class="link link-ref link-reveal xref-bibr">Su <em>et al.</em>, 2014</a>). Supplementation with exogenous cytokinins has been tested in some anther culture systems, with variable results (<span class="xrefLink" id="jumplink-CIT0164"></span><a href="javascript:;" reveal-id="CIT0164" data-open="CIT0164" class="link link-ref link-reveal xref-bibr">Zur <em>et al.</em>, 2015</a>); however, the involvement of endogenous cytokinin in microspore embryogenesis remains to be analysed. Preliminary results of our group show that auxin and cytokinin have opposite patterns of distribution in microspore-derived developing embryos, suggesting a defined spatiotemporal localization of auxin and cytokinin responses during microspore embryogenesis.</p><p class="chapter-para">Further work will be necessary to explore the hormonal crosstalk and signalling pathways that regulate induction of microspore embryogenesis, and to determine how the inductor stress signalling interacts with auxin and cytokinin signalling pathways to drive the switching of cell fate.</p> <h2 scrollto-destination=136423293 id="136423293" class="section-title js-splitscreen-section-title" data-legacy-id=s4>Epigenetic modifications and chromatin remodelling</h2> <p class="chapter-para">The reprogramming of somatic cells and initiation of embryogenesis involve genome-wide changes of gene expression that allow the old cell fate programme to be halted and the activation of a new developmental programme. These changes in gene expression are characterized by the change in global genome organization and the remodelling of chromatin, in both plants and animals (<span class="xrefLink" id="jumplink-CIT0064"></span><a href="javascript:;" reveal-id="CIT0064" data-open="CIT0064" class="link link-ref link-reveal xref-bibr">Kouzarides, 2007</a>). Increasing evidence has indicated the involvement of epigenetic mechanisms in the regulation of plant <em>in vitro</em> morphogenic processes, including organogenesis and somatic embryogenesis (<span class="xrefLink" id="jumplink-CIT0081"></span><a href="javascript:;" reveal-id="CIT0081" data-open="CIT0081" class="link link-ref link-reveal xref-bibr">Miguel and Marum, 2011</a>; <span class="xrefLink" id="jumplink-CIT0036"></span><a href="javascript:;" reveal-id="CIT0036" data-open="CIT0036" class="link link-ref link-reveal xref-bibr">Feher, 2015</a>), as well as in response to environmental cues and to stress (<span class="xrefLink" id="jumplink-CIT0051"></span><a href="javascript:;" reveal-id="CIT0051" data-open="CIT0051" class="link link-ref link-reveal xref-bibr">Gutzat and Mittelsten Scheid, 2012</a>; <span class="xrefLink" id="jumplink-CIT0074"></span><a href="javascript:;" reveal-id="CIT0074" data-open="CIT0074" class="link link-ref link-reveal xref-bibr">Luo <em>et al.</em>, 2012</a>). DNA methylation and histone modifications, mainly methylation and acetylation, are the most important epigenetic marks controlling chromatin organization.</p><p class="chapter-para">DNA methylation constitutes a prominent epigenetic modification of the chromatin fibre which is locked in a transcriptionally inactive conformation, leading to gene silencing (<span class="xrefLink" id="jumplink-CIT0155"></span><a href="javascript:;" reveal-id="CIT0155" data-open="CIT0155" class="link link-ref link-reveal xref-bibr">Wang and Kohler, 2017</a>). Commonly, open chromatin increases the accessibility of the genome to the transcription machinery, while closed chromatin represses gene expression by limiting accessibility (<span class="xrefLink" id="jumplink-CIT0108"></span><a href="javascript:;" reveal-id="CIT0108" data-open="CIT0108" class="link link-ref link-reveal xref-bibr">Reyes, 2006</a>; <span class="xrefLink" id="jumplink-CIT0064"></span><a href="javascript:;" reveal-id="CIT0064" data-open="CIT0064" class="link link-ref link-reveal xref-bibr">Kouzarides, 2007</a>). Several reports have related totipotency of cells to an open chromatin conformation characterized by large nuclei and homogenous euchromatin (<span class="xrefLink" id="jumplink-CIT0047"></span><a href="javascript:;" reveal-id="CIT0047" data-open="CIT0047" class="link link-ref link-reveal xref-bibr">Grafi <em>et al.</em>, 2011</a>). During microspore embryogenesis, changes in global DNA methylation levels have been observed in various herbaceous and woody species (<span class="xrefLink" id="jumplink-CIT0128"></span><a href="javascript:;" reveal-id="CIT0128" data-open="CIT0128" class="link link-ref link-reveal xref-bibr">Solís <em>et al</em>., 2012</a>; <span class="xrefLink" id="jumplink-CIT0034"></span><a href="javascript:;" reveal-id="CIT0034" data-open="CIT0034" class="link link-ref link-reveal xref-bibr">El-Tantawy <em>et al.</em>, 2014</a>; <span class="xrefLink" id="jumplink-CIT0110"></span><a href="javascript:;" reveal-id="CIT0110" data-open="CIT0110" class="link link-ref link-reveal xref-bibr">Rodríguez-Sanz <em>et al</em>., 2014<em>b</em></a>; <span class="xrefLink" id="jumplink-CIT0026"></span><a href="javascript:;" reveal-id="CIT0026" data-open="CIT0026" class="link link-ref link-reveal xref-bibr">De-la-Peña <em>et al</em>., 2015</a>; <span class="xrefLink" id="jumplink-CIT0070"></span><a href="javascript:;" reveal-id="CIT0070" data-open="CIT0070" class="link link-ref link-reveal xref-bibr">Li <em>et al.</em>, 2016</a>; <span class="xrefLink" id="jumplink-CIT0022"></span><a href="javascript:;" reveal-id="CIT0022" data-open="CIT0022" class="link link-ref link-reveal xref-bibr">Corredoira <em>et al.</em>, 2017</a>). Using quantitative biochemical assays and immunolocalization of 5-methyl-deoxy-cytosine (5mdC), these studies demonstrated that microspore reprogramming and initiation of embryogenesis involve a global DNA hypomethylation.</p><p class="chapter-para">The change in the developmental programme and initiation of embryogenesis affected the functional organization of the nuclear domains, including the chromatin condensation state (<span class="xrefLink" id="jumplink-CIT0137"></span><a href="javascript:;" reveal-id="CIT0137" data-open="CIT0137" class="link link-ref link-reveal xref-bibr">Testillano <em>et al.</em>, 2000</a>, 2005; <span class="xrefLink" id="jumplink-CIT0118"></span><a href="javascript:;" reveal-id="CIT0118" data-open="CIT0118" class="link link-ref link-reveal xref-bibr">Seguí-Simarro <em>et al.</em>, 2006</a>, 2011; <span class="xrefLink" id="jumplink-CIT0026"></span><a href="javascript:;" reveal-id="CIT0026" data-open="CIT0026" class="link link-ref link-reveal xref-bibr">De-la-Peña <em>et al</em>., 2015</a>). After induction, early microspore proembryos are characterized by a decondensed chromatin pattern that exhibits low DNA methylation, as revealed by 5mdC labelling (<span class="xrefLink" id="jumplink-CIT0128"></span><a href="javascript:;" reveal-id="CIT0128" data-open="CIT0128" class="link link-ref link-reveal xref-bibr">Solís <em>et al</em>., 2012</a>; <span class="xrefLink" id="jumplink-CIT0034"></span><a href="javascript:;" reveal-id="CIT0034" data-open="CIT0034" class="link link-ref link-reveal xref-bibr">El-Tantawy <em>et al.</em>, 2014</a>). In contrast, further embryo development is characterized by a progressive increase in global methylation of embryo cells, associated with the heterochromatization that accompanies cellular differentiation. In <em>B. napus</em>, expression of the DNA methyltransferase gene <em>MET1</em> is up-regulated during progression of microspore embryogenesis, as well as in advanced stages of zygotic embryogenesis, suggesting that MET1 activity contributes to the increase in global DNA methylation of differentiating embryo cells (<span class="xrefLink" id="jumplink-CIT0128"></span><a href="javascript:;" reveal-id="CIT0128" data-open="CIT0128" class="link link-ref link-reveal xref-bibr">Solís <em>et al</em>., 2012</a>). Experiments by modulation of global DNA methylation levels using inhibitors of methylation, such as 5-azacytidine (azaC) or 5-aza-2'-deoxycytidine (azadC), have been used in various <em>in vitro</em> systems of somatic embryogenesis and organogenesis, with variable results due to high dose response effects and cell toxicity. However, when azaC or azadC are applied at early stages and at a low concentration, they produced DNA hypomethylation and promoted initiation of embryogenesis, as reported in Arabidopsis somatic embryogenesis with azadC (<span class="xrefLink" id="jumplink-CIT0035"></span><a href="javascript:;" reveal-id="CIT0035" data-open="CIT0035" class="link link-ref link-reveal xref-bibr">Elhiti <em>et al.</em>, 2010</a>) and in microspore embryogenesis of <em>B. napus</em> and <em>H. vulgare</em> with azaC (<span class="xrefLink" id="jumplink-CIT0126"></span><a href="javascript:;" reveal-id="CIT0126" data-open="CIT0126" class="link link-ref link-reveal xref-bibr">Solís <em>et al</em>., 2015</a>). The reduction of global DNA methylation by azaC treatment during advanced embryogenesis stages results in an impairment of embryo development and indicates that <em>de novo</em> DNA methylation is required for progression of microspore embryogenesis (<span class="xrefLink" id="jumplink-CIT0126"></span><a href="javascript:;" reveal-id="CIT0126" data-open="CIT0126" class="link link-ref link-reveal xref-bibr">Solís <em>et al</em>., 2015</a>). The way in which differentiating plant cells reprogramme and acquire cell totipotency is a central question that involves remodelling of genome-wide expression programmes and large-scale chromatin reorganization. In this regard, these recent findings support the idea that DNA hypomethylation is critical for the regulation of chromatin remodelling and the switching of the gene expression programme in induction of microspore embryogenesis.</p><p class="chapter-para">Together with DNA methylation, histone modifications—mainly methylation and acetylation—participate by driving changes in chromatin conformation and condensation (<span class="xrefLink" id="jumplink-CIT0157"></span><a href="javascript:;" reveal-id="CIT0157" data-open="CIT0157" class="link link-ref link-reveal xref-bibr">Yang <em>et al.</em>, 2010</a>; <span class="xrefLink" id="jumplink-CIT0031"></span><a href="javascript:;" reveal-id="CIT0031" data-open="CIT0031" class="link link-ref link-reveal xref-bibr">Eichten <em>et al.</em>, 2014</a>), controlling gene expression during plant development and in response to the environment. Chromatin-modifying enzymes, including histone lysine methyltransferases (HKMTs) and demethylases (LSD1 and JmjC families), as well as histone acetyltransferases (HATs) and deacetylases (HDACs), have all been proposed as modulators of cell reprogramming that act by changing the genome-wide distribution of repressive and permissive histone marks and promoting open/closed chromatin states (<span class="xrefLink" id="jumplink-CIT0091"></span><a href="javascript:;" reveal-id="CIT0091" data-open="CIT0091" class="link link-ref link-reveal xref-bibr">Onder <em>et al.</em>, 2012</a>). Methylation of histones can occur on different lysine residues in histones H3 and H4. H3 methylation at positions K9 and K27 is generally related to gene silencing, while active genes are associated with methylation at K4 and K36 (Liu <em>et al</em>., 2010). Among these epigenetic marks, H3K9 methylation is one of the major histone modifications with central roles in the epigenetic control of diverse developmental processes. In plants, H3K9 methylation is associated with DNA methylation and small RNAs, which are both essential drivers for heterochromatin formation (<span class="xrefLink" id="jumplink-CIT0117"></span><a href="javascript:;" reveal-id="CIT0117" data-open="CIT0117" class="link link-ref link-reveal xref-bibr">Saze <em>et al.</em>, 2012</a>). H3K27 methyltransferases of POLYCOMB REPRESSIVE COMPLEX 2 (PRC2) have been associated with the prevention of pluripotency during differentiation in Arabidopsis (<span class="xrefLink" id="jumplink-CIT0123"></span><a href="javascript:;" reveal-id="CIT0123" data-open="CIT0123" class="link link-ref link-reveal xref-bibr">She <em>et al.</em>, 2013</a>; <span class="xrefLink" id="jumplink-CIT0039"></span><a href="javascript:;" reveal-id="CIT0039" data-open="CIT0039" class="link link-ref link-reveal xref-bibr">Gentry and Hennig, 2014</a>; <span class="xrefLink" id="jumplink-CIT0048"></span><a href="javascript:;" reveal-id="CIT0048" data-open="CIT0048" class="link link-ref link-reveal xref-bibr">Gu <em>et al.</em>, 2014</a>; <span class="xrefLink" id="jumplink-CIT0036"></span><a href="javascript:;" reveal-id="CIT0036" data-open="CIT0036" class="link link-ref link-reveal xref-bibr">Feher, 2015</a>), and PRC2 activity has been reported to block hormone-mediated reprogramming towards somatic embryogenesis in Arabidopsis (<span class="xrefLink" id="jumplink-CIT0087"></span><a href="javascript:;" reveal-id="CIT0087" data-open="CIT0087" class="link link-ref link-reveal xref-bibr">Mozgova <em>et al</em>., 2017</a>).</p><p class="chapter-para">A recent report has shown that microspore reprogramming and the initiation of embryogenesis are associated with low levels of H3K9 methylation, while embryo differentiation progresses with increasing levels of this histone mark (<span class="xrefLink" id="jumplink-CIT0110"></span><a href="javascript:;" reveal-id="CIT0110" data-open="CIT0110" class="link link-ref link-reveal xref-bibr">Rodríguez-Sanz <em>et al</em>., 2014<em>b</em></a>; <span class="xrefLink" id="jumplink-CIT0012"></span><a href="javascript:;" reveal-id="CIT0012" data-open="CIT0012" class="link link-ref link-reveal xref-bibr">Berenguer <em>et al.</em>, 2017</a>), as demonstrated by biochemical and H3K9me2 immunofluorescence assays (<span class="xrefLink" id="jumplink-F4"></span><a href="javascript:;" data-modal-source-id="F4" class="link xref-fig">Fig. 4</a>). Interestingly, the temporal profile of bulk H3K9 methylation during microspore embryogenesis correlates with the gene expression patterns of <em>BnHKMT SUVR4-like</em> and <em>BnLSD1-like</em> genes, ‘writer’ and ‘eraser’ enzymes of H3K9me2 (<span class="xrefLink" id="jumplink-CIT0012"></span><a href="javascript:;" reveal-id="CIT0012" data-open="CIT0012" class="link link-ref link-reveal xref-bibr">Berenguer <em>et al.</em>, 2017</a>), providing additional evidence of the developmental regulation of this histone modification during the process of microspore embryogenesis. Moreover, treatment of microspore cultures with the small molecule BIX-01294, a known inhibitor of H3K9 methylation in mammalian cells (<span class="xrefLink" id="jumplink-CIT0132"></span><a href="javascript:;" reveal-id="CIT0132" data-open="CIT0132" class="link link-ref link-reveal xref-bibr">Tachibana <em>et al.</em>, 2002</a>; <span class="xrefLink" id="jumplink-CIT0065"></span><a href="javascript:;" reveal-id="CIT0065" data-open="CIT0065" class="link link-ref link-reveal xref-bibr">Kubicek <em>et al.</em>, 2007</a>), promotes microspore reprogramming and embryogenesis initiation, in rapeseed and barley (<span class="xrefLink" id="jumplink-CIT0012"></span><a href="javascript:;" reveal-id="CIT0012" data-open="CIT0012" class="link link-ref link-reveal xref-bibr">Berenguer <em>et al.</em>, 2017</a>). Conversely, BIX-01294 treatment at advanced stages impairs embryo formation, showing that initiation of embryogenesis involves low H3K9 methylation but embryo differentiation requires high levels of this repressive mark.</p> <a id="136423299" scrollto-destination="136423299"></a> <div data-id="f4" data-content-id="f4" class="fig fig-section js-fig-section" swap-content-for-modal="true"><div class="graphic-wrap"><img class="content-image" src="https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/jxb/70/11/10.1093_jxb_ery464/1/m_exbotj_ery464_f0004.jpeg?Expires=1735137917&Signature=kSHZf4okqzOKG~g8J3Bb8XYV1tyO7C-hrINDf2qhL~aHg0qgEBgVfxUiotT-a-f3N7au-NMXz14m7z2e~AMHhI6LVsq0dfBVlAAwn1jmRvSMTvdmk5V~uf9MNANIhM-laT2g5voUwAF8jnXYrCvOVL7YSxt4ZXk7AhG95UdnB9MnmfGgT0oh9gT6Pcyxpf9QqQmI2ICowIu7JfqejUf03oTzbg19VW39juZUCd6DnQQTXuUR3Xk1JXjV3Rrg4Vx4AyRIbh4xyWdsmCQJr3fJRI00c6tdqnHWVGeTZsSSzEqEXK0HVeYeEDo3DJtaRoQWBPIFlW8mnyYt6wLbyV4jJA__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA" alt="Localization of H3K9me2 during microspore embryogenesis of Hordeum vulgare. Confocal microscopy images of H3K9me2 immunofluorescence (green, A', B', C') and DAPI-stained nuclei (blue, A, B, C). Pairs of images A–A', B–B', and C–C' correspond to the same structures. (A, A') Vacuolated microspore before induction showing mid intense labelling on the nucleus. (B, B') Proembryo with several large and rounded nuclei exhibiting lower immunofluorescence for H3K9me2. (C, C') Region of a cotyledonary embryo with numerous nuclei intensely labelled by H3K9me2 antibodies. Scale bars in A, A', B, B': 20 µm; in C, C': 75 µm." data-path-from-xml="exbotj_ery464_f0004.jpg" /><div class="graphic-bottom"><div class="label fig-label" id="label-136423299">Fig. 4.</div><div class="caption fig-caption"><p class="chapter-para">Localization of H3K9me2 during microspore embryogenesis of <em>Hordeum vulgare</em>. Confocal microscopy images of H3K9me2 immunofluorescence (green, A', B', C') and DAPI-stained nuclei (blue, A, B, C). Pairs of images A–A', B–B', and C–C' correspond to the same structures. (A, A') Vacuolated microspore before induction showing mid intense labelling on the nucleus. (B, B') Proembryo with several large and rounded nuclei exhibiting lower immunofluorescence for H3K9me2. (C, C') Region of a cotyledonary embryo with numerous nuclei intensely labelled by H3K9me2 antibodies. Scale bars in A, A', B, B': 20 µm; in C, C': 75 µm.</p></div><div class="ajax-articleAbstract-exclude-regex fig-orig original-slide figure-button-wrap"><a class="fig-view-orig js-view-large at-figureViewLarge openInAnotherWindow" role="button" aria-describedby="label-136423299" href="/view-large/figure/136423299/exbotj_ery464_f0004.jpg" data-path-from-xml="exbotj_ery464_f0004.jpg" target="_blank">Open in new tab</a><a class="download-slide" role="button" aria-describedby="label-136423299" data-section="136423299" href="/DownloadFile/DownloadImage.aspx?image=https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/jxb/70/11/10.1093_jxb_ery464/1/exbotj_ery464_f0004.jpeg?Expires=1735137917&Signature=lRMAxPvCCMdrVed1o97HPkkYshtZZKdwbX0pT-Y0-UiMQokOwrZDMow6stCisE1e~cK-0zljFWEyTtdJTBsVqX2au2i8Twp0vc4fDCufX3qwWVxqsUaHLhT9KFasiMtoG~nXiLe4vC~S9J6l6UAh4OAvQV9s8qFwPfngVqbM1uaVGDzSl~BhAAWDIsnon0~Cr02ELuKfkEFHGMntqb2FAHc~WawJ1rKdCshOORTYPInSzVWcg2p5J9V6CeqciXddFwwpgAvWDL6GYj7xINIimTj8tbAyUli1xtzK2z-fdaC0elh9A-RkPi~ljmFb8qkHtb668-A61FGwYN9yjR2-ug__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA&sec=136423299&ar=5310108&xsltPath=~/UI/app/XSLT&imagename=&siteId=5304" data-path-from-xml="exbotj_ery464_f0004.jpg">Download slide</a></div></div></div></div><p class="chapter-para">It has been shown that the acetylation of lysine residues within the N-terminal tail of histones H3 and H4 is also involved in initiation and progression of microspore embryogenesis, and increasing acetylation has been related to cell totipotency ( <span class="xrefLink" id="jumplink-CIT0069"></span><a href="javascript:;" reveal-id="CIT0069" data-open="CIT0069" class="link link-ref link-reveal xref-bibr">Li <em>et al.</em>, 2014</a>; <span class="xrefLink" id="jumplink-CIT0110"></span><a href="javascript:;" reveal-id="CIT0110" data-open="CIT0110" class="link link-ref link-reveal xref-bibr">Rodríguez-Sanz <em>et al</em>., 2014<em>b</em></a>). Histone H3 and H4 acetylation is mainly associated with actively transcribed genes and promotes the open chromatin states (<span class="xrefLink" id="jumplink-CIT0091"></span><a href="javascript:;" reveal-id="CIT0091" data-open="CIT0091" class="link link-ref link-reveal xref-bibr">Onder <em>et al.</em>, 2012</a>). The application of histone deacetylase inhibitors—such as trichostatin A or suberoylanilide hydroxamic acid (SAHA), which lead to increased levels of histone acetylation—produce an increase in the rate of induction of microspore embryogenesis ( <span class="xrefLink" id="jumplink-CIT0069"></span><a href="javascript:;" reveal-id="CIT0069" data-open="CIT0069" class="link link-ref link-reveal xref-bibr">Li <em>et al.</em>, 2014</a>; <span class="xrefLink" id="jumplink-CIT0161"></span><a href="javascript:;" reveal-id="CIT0161" data-open="CIT0161" class="link link-ref link-reveal xref-bibr">Zhang <em>et al.</em>, 2016</a>; <span class="xrefLink" id="jumplink-CIT0059"></span><a href="javascript:;" reveal-id="CIT0059" data-open="CIT0059" class="link link-ref link-reveal xref-bibr">Jiang <em>et al.</em>, 2017</a>; <span class="xrefLink" id="jumplink-CIT0092"></span><a href="javascript:;" reveal-id="CIT0092" data-open="CIT0092" class="link link-ref link-reveal xref-bibr">Pandey <em>et al.</em>, 2017</a>; E. Berenguer <em>et al</em>., unpublished results), demonstrating that histone acetylation plays a crucial role in promoting microspore reprogramming and totipotency.</p><p class="chapter-para">Increasing evidence points to the existence of a complex crosstalk between DNA methylation and histone methylation/acetylation in the regulation of the plant developmental processes (<span class="xrefLink" id="jumplink-CIT0117"></span><a href="javascript:;" reveal-id="CIT0117" data-open="CIT0117" class="link link-ref link-reveal xref-bibr">Saze <em>et al.</em>, 2012</a>). Evidence obtained to date shows that a genome-wide chromatin remodelling is required for microspore reprogramming, totipotency, and initiation of embryogenesis; global hypomethylation of DNA and H3K9, and increasing histone acetylation would presumably mainly contribute to this chromatin remodelling by increasing both chromatin decondensation and the access of transcription factors regulating the switch of the developmental programme.</p> <h2 scrollto-destination=136423302 id="136423302" class="section-title js-splitscreen-section-title" data-legacy-id=s5>Cell wall remodelling: pectins and AGPs</h2> <p class="chapter-para">A growing number of studies support the crucial role of cell wall components such as pectins and arabinogalactan proteins (AGPs) during somatic and zygotic embryogenesis in plants (<span class="xrefLink" id="jumplink-CIT0153"></span><a href="javascript:;" reveal-id="CIT0153" data-open="CIT0153" class="link link-ref link-reveal xref-bibr">van Hengel <em>et al.</em>, 2002</a>; <span class="xrefLink" id="jumplink-CIT0114"></span><a href="javascript:;" reveal-id="CIT0114" data-open="CIT0114" class="link link-ref link-reveal xref-bibr">Samaj <em>et al.</em>, 2005</a>; <span class="xrefLink" id="jumplink-CIT0033"></span><a href="javascript:;" reveal-id="CIT0033" data-open="CIT0033" class="link link-ref link-reveal xref-bibr">El-Tantawy <em>et al.</em>, 2013</a>; <span class="xrefLink" id="jumplink-CIT0109"></span><a href="javascript:;" reveal-id="CIT0109" data-open="CIT0109" class="link link-ref link-reveal xref-bibr">Rodríguez-Sanz <em>et al</em>., 2014<em>a</em></a>). Plant cell walls are dynamic and complex structures that play important roles in the regulation of plant growth, development, and the determination of cell shape and fate (<span class="xrefLink" id="jumplink-CIT0129"></span><a href="javascript:;" reveal-id="CIT0129" data-open="CIT0129" class="link link-ref link-reveal xref-bibr">Somerville <em>et al.</em>, 2004</a>). Modifications in cell wall components have been reported as being crucial in relation to cell fate and development. Plant growth and differentiation require controlled remodelling of cell wall polymer networks, producing changes in their mechanical properties to permit cell division and expansion (<span class="xrefLink" id="jumplink-CIT0152"></span><a href="javascript:;" reveal-id="CIT0152" data-open="CIT0152" class="link link-ref link-reveal xref-bibr">van Hengel <em>et al.</em>, 2001</a>; <span class="xrefLink" id="jumplink-CIT0003"></span><a href="javascript:;" reveal-id="CIT0003" data-open="CIT0003" class="link link-ref link-reveal xref-bibr">Baluska <em>et al.</em>, 2002</a>, 2005; <span class="xrefLink" id="jumplink-CIT0153"></span><a href="javascript:;" reveal-id="CIT0153" data-open="CIT0153" class="link link-ref link-reveal xref-bibr">Van Hengel <em>et al.</em>, 2002</a>; <span class="xrefLink" id="jumplink-CIT0004"></span><a href="javascript:;" reveal-id="CIT0004" data-open="CIT0004" class="link link-ref link-reveal xref-bibr">Samaj <em>et al.</em>, 2005</a>; <span class="xrefLink" id="jumplink-CIT0121"></span><a href="javascript:;" reveal-id="CIT0121" data-open="CIT0121" class="link link-ref link-reveal xref-bibr">Seifert and Roberts, 2007</a>; <span class="xrefLink" id="jumplink-CIT0044"></span><a href="javascript:;" reveal-id="CIT0044" data-open="CIT0044" class="link link-ref link-reveal xref-bibr">Geshi <em>et al.</em>, 2013</a>; <span class="xrefLink" id="jumplink-CIT0124"></span><a href="javascript:;" reveal-id="CIT0124" data-open="CIT0124" class="link link-ref link-reveal xref-bibr">Smertenko and Bozhkov, 2014</a>). Cell differentiation requires remodelling of wall polysaccharide networks during development and in response to external signals (<span class="xrefLink" id="jumplink-CIT0011"></span><a href="javascript:;" reveal-id="CIT0011" data-open="CIT0011" class="link link-ref link-reveal xref-bibr">Barnes and Anderson, 2018</a>). Among cell wall polymers, pectins are major components of the primary wall and represent one of the most complex families of polysaccharides. Pectins are exported to the cell wall in a highly methylesterified form and their level of methylesterification is controlled <em>in muro</em> by pectin methylesterases (PMEs) and PME inhibitors (PMEIs) (<span class="xrefLink" id="jumplink-CIT0094"></span><a href="javascript:;" reveal-id="CIT0094" data-open="CIT0094" class="link link-ref link-reveal xref-bibr">Pelloux <em>et al.</em>, 2007</a>). The de-methylesterified residues of pectins can form Ca<sup>2+</sup> bonds which may promote cell wall strengthening or become a target for pectin-degrading enzymes, such as polygalacturonases, affecting the texture and rigidity of the cell wall (<span class="xrefLink" id="jumplink-CIT0094"></span><a href="javascript:;" reveal-id="CIT0094" data-open="CIT0094" class="link link-ref link-reveal xref-bibr">Pelloux <em>et al.</em>, 2007</a>). The change in the developmental programme of the microspore and the progression of embryo development involve changes in pectin esterification that are associated with proliferation and differentiation events, as demonstrated by highly sensitive immunocytochemical and immunodot-blot assays with specific antibodies (<span class="xrefLink" id="jumplink-CIT0006"></span><a href="javascript:;" reveal-id="CIT0006" data-open="CIT0006" class="link link-ref link-reveal xref-bibr">Bárány <em>et al.</em>, 2010<em>a</em>, <em>b</em></a>; <span class="xrefLink" id="jumplink-CIT0125"></span><a href="javascript:;" reveal-id="CIT0125" data-open="CIT0125" class="link link-ref link-reveal xref-bibr">Solís <em>et al</em>., 2016</a>). These modifications in the esterification status of pectins may cause cell wall remodelling during the process. At early embryogenic stages, high levels of methylesterified pectins have been found (<span class="xrefLink" id="jumplink-F5"></span><a href="javascript:;" data-modal-source-id="F5" class="link xref-fig">Fig. 5A</a>, <span class="xrefLink" id="jumplink-F5"></span><a href="javascript:;" data-modal-source-id="F5" class="link xref-fig">B</a>) as a differential feature of the cell wall after cell reprogramming in the stress-induced microspore embryogenesis of several species (<span class="xrefLink" id="jumplink-CIT0127"></span><a href="javascript:;" reveal-id="CIT0127" data-open="CIT0127" class="link link-ref link-reveal xref-bibr">Solís <em>et al.</em>, 2008</a>, 2016; <span class="xrefLink" id="jumplink-CIT0109"></span><a href="javascript:;" reveal-id="CIT0109" data-open="CIT0109" class="link link-ref link-reveal xref-bibr">Rodríguez-Sanz <em>et al.</em>, 2014<em>a</em></a>; <span class="xrefLink" id="jumplink-CIT0022"></span><a href="javascript:;" reveal-id="CIT0022" data-open="CIT0022" class="link link-ref link-reveal xref-bibr">Corredoira <em>et al.</em>, 2017</a>). As embryogenesis proceeds, decreasing methylesterification levels have been reported in cell walls of differentiating embryos, in agreement with observations in other developmental pathways from proliferating to differentiating tissues of various plant species (<span class="xrefLink" id="jumplink-CIT0060"></span><a href="javascript:;" reveal-id="CIT0060" data-open="CIT0060" class="link link-ref link-reveal xref-bibr">Jolie <em>et al.</em>, 2010</a>). Changes in pectin esterification levels correlate with temporal expression patterns of <em>PME</em> and <em>PMEI</em> genes in microspore embryogenesis of <em>B. napus</em> (<span class="xrefLink" id="jumplink-CIT0125"></span><a href="javascript:;" reveal-id="CIT0125" data-open="CIT0125" class="link link-ref link-reveal xref-bibr">Solís <em>et al</em>., 2016</a>; unpublished results) and somatic embryogenesis of <em>Q. suber</em> (<span class="xrefLink" id="jumplink-CIT0098"></span><a href="javascript:;" reveal-id="CIT0098" data-open="CIT0098" class="link link-ref link-reveal xref-bibr">Pérez-Pérez <em>et al.</em>, 2019<em>b</em></a>). For example, differentiating embryos (such as torpedo and cotyledonary embryos) show cell walls rich in de-methylesterified pectins, together with high expression levels of <em>PME</em> (<span class="xrefLink" id="jumplink-F5"></span><a href="javascript:;" data-modal-source-id="F5" class="link xref-fig">Fig. 5C</a>, <span class="xrefLink" id="jumplink-F5"></span><a href="javascript:;" data-modal-source-id="F5" class="link xref-fig">D</a>). Moreover, inhibition of PME activity by catechin (<span class="xrefLink" id="jumplink-CIT0068"></span><a href="javascript:;" reveal-id="CIT0068" data-open="CIT0068" class="link link-ref link-reveal xref-bibr">Lewis <em>et al.</em>, 2008</a>) impairs somatic embryogenesis in <em>Q. suber</em> (<span class="xrefLink" id="jumplink-CIT0098"></span><a href="javascript:;" reveal-id="CIT0098" data-open="CIT0098" class="link link-ref link-reveal xref-bibr">Pérez-Pérez <em>et al.</em>, 2019<em>b</em></a>), indicating that pectin esterification and cell wall configuration play a relevant role in induction and/or progression of embryogenesis (<span class="xrefLink" id="jumplink-CIT0125"></span><a href="javascript:;" reveal-id="CIT0125" data-open="CIT0125" class="link link-ref link-reveal xref-bibr">Solís <em>et al</em>., 2016</a>; <span class="xrefLink" id="jumplink-CIT0098"></span><a href="javascript:;" reveal-id="CIT0098" data-open="CIT0098" class="link link-ref link-reveal xref-bibr">Pérez-Pérez <em>et al.</em>, 2019<em>b</em></a>). Taken together, these findings support the idea that PME-mediated configuration of pectins could be a crucial factor for microspore embryo differentiation, acting via the promotion of cell wall remodelling during the process. Auxin has been related to the regulation of cell wall remodelling during initiation of organogenesis in Arabidopsis, exerting its effect by reducing the cell wall stiffness through a process that requires de-methylesterification of pectins (<span class="xrefLink" id="jumplink-CIT0015"></span><a href="javascript:;" reveal-id="CIT0015" data-open="CIT0015" class="link link-ref link-reveal xref-bibr">Braybrook and Peaucelle, 2013</a>; <span class="xrefLink" id="jumplink-CIT0067"></span><a href="javascript:;" reveal-id="CIT0067" data-open="CIT0067" class="link link-ref link-reveal xref-bibr">Lewis <em>et al.</em>, 2013</a>). Further work will be necessary to determine the exact role of auxin in pectin-related cell wall remodelling during stress-induced microspore embryogenesis.</p> <a id="136423304" scrollto-destination="136423304"></a> <div data-id="f5" data-content-id="f5" class="fig fig-section js-fig-section" swap-content-for-modal="true"><div class="graphic-wrap"><img class="content-image" src="https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/jxb/70/11/10.1093_jxb_ery464/1/m_exbotj_ery464_f0005.jpeg?Expires=1735137917&Signature=S7hwJMTvBRqCSrJFHACOC31bAiKhJW31LsT8e149Jh2q1MoPAe-k7herOdMFcl0Y~fXAEFOJlP8NWLA5d0VvuHQm69DDrEURFxjIgUcU-nBpARYhtNfEMPMI73WwlIxITfzZXtgZXPU0iyfSSX8Q9f0IAiT~hVnlAgUHqtQPIzzu6gvEurweDN0F8SYZisRZDHn8~hGzFYmQaQx7TmCsP9p29EaQcTTdxXXF2emDKueI2aZpnPmBEYXXrYJOd1m3zW9qoovPYu4eKQ~G6Cqfw0xxPUpIP~k7rY~Tz5aCneR0kMjj~tYCeO-0KX~qo2apMMEDiY0rUNXeipLCVcndrA__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA" alt="Changes in pectin methylesterification of the cell wall during microspore embryogenesis in Brassica napus. Confocal microscopy merged images of immunofluorescence (A, B) or FISH, fluorescence in situ hybridization (C, D) (green) and DAPI-stained nuclei (blue). (A, B) Proembryos, early stage after embryogenesis induction. (A) Localization of highly esterified pectins (by JIM7 antibody) showing intense signal on cell walls of proembryos. (B) Localization of de-esterified pectins (by JIM5 antibody); cell walls of proembryos show much less immunofluorescence signal. (C) FISH of BnPME1 in torpedo embryo showing an intense signal corresponding to high expression in cytoplasm. (D) Negative control of FISH assay with the sense probe, in torpedo embryo. Scale bars=20 µm." data-path-from-xml="exbotj_ery464_f0005.jpg" /><div class="graphic-bottom"><div class="label fig-label" id="label-136423304">Fig. 5.</div><div class="caption fig-caption"><p class="chapter-para">Changes in pectin methylesterification of the cell wall during microspore embryogenesis in <em>Brassica napus</em>. Confocal microscopy merged images of immunofluorescence (A, B) or FISH, fluorescence <em>in situ</em> hybridization (C, D) (green) and DAPI-stained nuclei (blue). (A, B) Proembryos, early stage after embryogenesis induction. (A) Localization of highly esterified pectins (by JIM7 antibody) showing intense signal on cell walls of proembryos. (B) Localization of de-esterified pectins (by JIM5 antibody); cell walls of proembryos show much less immunofluorescence signal. (C) FISH of <em>BnPME1</em> in torpedo embryo showing an intense signal corresponding to high expression in cytoplasm. (D) Negative control of FISH assay with the sense probe, in torpedo embryo. Scale bars=20 µm.</p></div><div class="ajax-articleAbstract-exclude-regex fig-orig original-slide figure-button-wrap"><a class="fig-view-orig js-view-large at-figureViewLarge openInAnotherWindow" role="button" aria-describedby="label-136423304" href="/view-large/figure/136423304/exbotj_ery464_f0005.jpg" data-path-from-xml="exbotj_ery464_f0005.jpg" target="_blank">Open in new tab</a><a class="download-slide" role="button" aria-describedby="label-136423304" data-section="136423304" href="/DownloadFile/DownloadImage.aspx?image=https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/jxb/70/11/10.1093_jxb_ery464/1/exbotj_ery464_f0005.jpeg?Expires=1735137917&Signature=j~Q-bzoHr9aGlyO6ekitTyfiaV578x2RD0QcpzUQMydwvD7MsWXfBM17oPxBnFWjh0eXDwudwXoHWYnN2LRQHQz-9wvEPmuAa58RYZBg7YtLBrMLg-uGV2DRubWoL598K7NuPSZ90c6hglsJVuNZ-jRqUh55dZuTPiM26bf5wSV4dhs3JfDjxH5JmT5tMeq9P7-5dR~gz5ByceLD11HjZ9YKL~w0JQDcbw8PD4-bcjl5zBA0nlF0u7eK~vjnHgPGzZ0am8~8eZGqtp5cwEU4~CdnPIUCQjZXxxrYT3AjT8f9YC9nr-WbCrpHOu6bIuLaJ~6vKszCOS~3~r7yZauBUA__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA&sec=136423304&ar=5310108&xsltPath=~/UI/app/XSLT&imagename=&siteId=5304" data-path-from-xml="exbotj_ery464_f0005.jpg">Download slide</a></div></div></div></div><p class="chapter-para">Plant cell walls also contain structural proteins such as AGPs. AGPs are a large family of highly glycosylated hydroxyproline-rich proteins that are present in cell walls, plasma membranes, and extracellular secretions. Various lines of evidence have shown that AGPs play key roles in many plant developmental processes, including embryo development (<span class="xrefLink" id="jumplink-CIT0121"></span><a href="javascript:;" reveal-id="CIT0121" data-open="CIT0121" class="link link-ref link-reveal xref-bibr">Seifert and Roberts, 2007</a>; <span class="xrefLink" id="jumplink-CIT0162"></span><a href="javascript:;" reveal-id="CIT0162" data-open="CIT0162" class="link link-ref link-reveal xref-bibr">Zhong <em>et al.</em>, 2011</a>; <span class="xrefLink" id="jumplink-CIT0044"></span><a href="javascript:;" reveal-id="CIT0044" data-open="CIT0044" class="link link-ref link-reveal xref-bibr">Geshi <em>et al.</em>, 2013</a>). They have also been proposed as modulators of cell wall mechanics (<span class="xrefLink" id="jumplink-CIT0121"></span><a href="javascript:;" reveal-id="CIT0121" data-open="CIT0121" class="link link-ref link-reveal xref-bibr">Seifert and Roberts, 2007</a>). Many AGPs contain a glycosylphosphatidylinositol (GPI) anchor, which tethers them to the plasma membrane and allows them to be positioned over the surface of the plasma membrane and into the cell wall (<span class="xrefLink" id="jumplink-CIT0121"></span><a href="javascript:;" reveal-id="CIT0121" data-open="CIT0121" class="link link-ref link-reveal xref-bibr">Seifert and Roberts, 2007</a>). Moreover, like other signalling molecules, AGPs can also be exported into the cell wall, with them then being spread to the surrounding cells and secreted into the culture medium. Supplementing culture medium with exogenous AGPs (commonly Arabic gum containing an AGP mixture) promotes somatic embryogenesis in several plant species (<span class="xrefLink" id="jumplink-CIT0144"></span><a href="javascript:;" reveal-id="CIT0144" data-open="CIT0144" class="link link-ref link-reveal xref-bibr">Thompson and Knox, 1998</a>; <span class="xrefLink" id="jumplink-CIT0160"></span><a href="javascript:;" reveal-id="CIT0160" data-open="CIT0160" class="link link-ref link-reveal xref-bibr">Yuan <em>et al.</em>, 2012</a>; <span class="xrefLink" id="jumplink-CIT0124"></span><a href="javascript:;" reveal-id="CIT0124" data-open="CIT0124" class="link link-ref link-reveal xref-bibr">Smertenko and Bozhkov, 2014</a>). The secretion of endogenous AGPs from cultured cells into the medium has been shown to stimulate embryo development in microspore and zygote cultures of maize (<span class="xrefLink" id="jumplink-CIT0013"></span><a href="javascript:;" reveal-id="CIT0013" data-open="CIT0013" class="link link-ref link-reveal xref-bibr">Borderies <em>et al.</em>, 2004</a>; <span class="xrefLink" id="jumplink-CIT0138"></span><a href="javascript:;" reveal-id="CIT0138" data-open="CIT0138" class="link link-ref link-reveal xref-bibr">Testillano <em>et al.</em>, 2010</a>), carrot embryogenic suspension cultures (<span class="xrefLink" id="jumplink-CIT0152"></span><a href="javascript:;" reveal-id="CIT0152" data-open="CIT0152" class="link link-ref link-reveal xref-bibr">van Hengel <em>et al.</em>, 2001</a>), and somatic embryogenesis cultures of cotton (<span class="xrefLink" id="jumplink-CIT0102"></span><a href="javascript:;" reveal-id="CIT0102" data-open="CIT0102" class="link link-ref link-reveal xref-bibr">Poon <em>et al.</em>, 2012</a>). Several reports have also shown the differential presence of AGPs in various <em>in vitro</em> embryogenic systems (<span class="xrefLink" id="jumplink-CIT0114"></span><a href="javascript:;" reveal-id="CIT0114" data-open="CIT0114" class="link link-ref link-reveal xref-bibr">Samaj <em>et al.</em>, 2005</a>) and during microspore embryogenesis (<span class="xrefLink" id="jumplink-CIT0076"></span><a href="javascript:;" reveal-id="CIT0076" data-open="CIT0076" class="link link-ref link-reveal xref-bibr">Malik <em>et al.</em>, 2007</a>; <span class="xrefLink" id="jumplink-CIT0033"></span><a href="javascript:;" reveal-id="CIT0033" data-open="CIT0033" class="link link-ref link-reveal xref-bibr">El-Tantawy <em>et al.</em>, 2013</a>). The localization of AGPs in cell walls and secretory vesicles has also been demonstrated, as revealed by immunofluorescence with a battery of highly specific monoclonal antibodies against AGP epitopes (<span class="xrefLink" id="jumplink-CIT0063"></span><a href="javascript:;" reveal-id="CIT0063" data-open="CIT0063" class="link link-ref link-reveal xref-bibr">Knox, 1997</a>) at early stages of microspore embryogenesis (<span class="xrefLink" id="jumplink-CIT0033"></span><a href="javascript:;" reveal-id="CIT0033" data-open="CIT0033" class="link link-ref link-reveal xref-bibr">El-Tantawy <em>et al.</em>, 2013</a>). Information regarding the expression of AGP genes in <em>in vitro</em> embryogenesis is very scarce. Some studies have shown up-regulation of some AGP genes associated with the initiation of somatic embryogenesis in <em>Picea balfouriana</em> ( <span class="xrefLink" id="jumplink-CIT0071"></span><a href="javascript:;" reveal-id="CIT0071" data-open="CIT0071" class="link link-ref link-reveal xref-bibr">Li <em>et al.</em>, 2014</a>) and microspore embryogenesis in <em>B. napus</em> (<span class="xrefLink" id="jumplink-CIT0076"></span><a href="javascript:;" reveal-id="CIT0076" data-open="CIT0076" class="link link-ref link-reveal xref-bibr">Malik <em>et al.</em>, 2007</a>; <span class="xrefLink" id="jumplink-CIT0033"></span><a href="javascript:;" reveal-id="CIT0033" data-open="CIT0033" class="link link-ref link-reveal xref-bibr">El-Tantawy <em>et al.</em>, 2013</a>).</p><p class="chapter-para">Studies with Yariv reagents (<span class="xrefLink" id="jumplink-CIT0159"></span><a href="javascript:;" reveal-id="CIT0159" data-open="CIT0159" class="link link-ref link-reveal xref-bibr">Yariv <em>et al.</em>, 1962</a>, 1967), which block AGPs, have revealed that the inactivation of AGPs inhibited embryogenesis in several <em>in vitro</em> systems and in microspore embryogenesis cultures of <em>B. napus</em> (<span class="xrefLink" id="jumplink-CIT0133"></span><a href="javascript:;" reveal-id="CIT0133" data-open="CIT0133" class="link link-ref link-reveal xref-bibr">Tang <em>et al.</em>, 2006</a>). AGPs can be trapped by pectins and may modulate the mechanical properties of the pectic matrix (<span class="xrefLink" id="jumplink-CIT0121"></span><a href="javascript:;" reveal-id="CIT0121" data-open="CIT0121" class="link link-ref link-reveal xref-bibr">Seifert and Roberts, 2007</a>; <span class="xrefLink" id="jumplink-CIT0073"></span><a href="javascript:;" reveal-id="CIT0073" data-open="CIT0073" class="link link-ref link-reveal xref-bibr">Liao <em>et al.</em>, 2011</a>). AGPs are up-regulated and required in microspore embryogenesis; they might contribute to cell wall remodelling either by structural interaction with pectins or other wall polymers, or by directly stiffening the cell wall by oxidative cross-linking—a proposed mechanical role for AGPs in cell walls (<span class="xrefLink" id="jumplink-CIT0121"></span><a href="javascript:;" reveal-id="CIT0121" data-open="CIT0121" class="link link-ref link-reveal xref-bibr">Seifert and Roberts, 2007</a>). These findings indicated a role for both pectins and AGPs in the cell wall remodelling that takes place and is required in microspore embryogenesis, with pectin de-esterification and AGP expression being necessary for embryo formation.</p> <h2 scrollto-destination=136423307 id="136423307" class="section-title js-splitscreen-section-title" data-legacy-id=s6>Concluding remarks</h2> <p class="chapter-para">The knowledge gained in recent years has revealed that initiation and progression of microspore embryogenesis involve a complex network of determinant factors, whose roles are not yet well understood. Stress-induced cell death and low rates of cell reprogramming are major factors that greatly reduce the process yield at the initial stages. Autophagy and cell death proteases (metacaspases and cathepsins) have emerged as crucial players in the response of microspores to the inductive stress, leading to cell death, while cell reprogramming and acquisition of totipotency by responsive microspores are mainly regulated by hormonal and epigenetic mechanisms. Activation of endogenous auxin biosynthesis, as well as its polar transport and action, probably in combination with an appropriate cytokinin/auxin balance, are required for microspore embryogenesis, with initial stages involving global epigenetic changes such as hypomethylation of DNA, H3K9 demethylation, and H3/H4 acetylation. Supplementing the culture medium with specific modulators that induce these global epigenetic changes (such as azaC, azadC, BIX-01294, trichostatin A, or SAHA) leads to higher rates of initiation of embryogenesis, indicating the crucial role of epigenetic reprogramming in induction of microspore embryogenesis. Furthermore, after induction of embryogenesis, the remodelling of the cell wall—with increasing pectin de-methylesterification and AGP expression—is necessary for embryo development. Increasing evidence has revealed the involvement of auxin in signalling processes of chromatin remodelling by epigenetic mechanisms leading to the activation of specific gene expression programmes. Additionally, auxin has been reported to control cell wall remodelling during various plant developmental processes. All these factors might be interconnected in the regulation of microspore reprogramming, and embryogenesis initiation and progression, although future studies will be necessary to determine the signalling pathways involved.</p><p class="chapter-para">Recent reports of pharmacological treatments with autophagy, proteases, and epigenetic modulators are very promising in terms of enhancing <em>in vitro</em> embryo production yield. These modulators have shown similar beneficial effects in stress-induced microspore embryogenesis in various crop species, monocots, and eudicots, independently of the inductive stress applied (cold or heat), which suggests that common mechanisms may operate in other plants and that a similar pharmacological strategy could be extended to other species to increase the microspore viability, reprogramming, and embryogenesis induction rate. Recently, rapid advances have been reported in mammalian cell reprogramming by using small bioactive molecules which have been demonstrated to efficiently induce reprogramming and formation of pluripotent stem cells for various therapeutic applications (reviewed in (<span class="xrefLink" id="jumplink-CIT0075"></span><a href="javascript:;" reveal-id="CIT0075" data-open="CIT0075" class="link link-ref link-reveal xref-bibr">Ma <em>et al.</em>, 2017</a>). Although the mechanisms by which these small compounds induce reprogramming are unknown, they have shown activity as epigenetic modulators, autophagy modulators, and inhibitors of various signalling pathways. The potential of the screening of chemical libraries of small molecules in plant biology research has been reported, although its efficient application in plants is still quite limited (<span class="xrefLink" id="jumplink-CIT0052"></span><a href="javascript:;" reveal-id="CIT0052" data-open="CIT0052" class="link link-ref link-reveal xref-bibr">Hicks and Raikhel, 2012</a>; <span class="xrefLink" id="jumplink-CIT0024"></span><a href="javascript:;" reveal-id="CIT0024" data-open="CIT0024" class="link link-ref link-reveal xref-bibr">Chuprov-Netochin <em>et al.</em>, 2016</a>). Furthermore, increasing evidence has revealed that stem cells in plants and animals behave similarly (<span class="xrefLink" id="jumplink-CIT0090"></span><a href="javascript:;" reveal-id="CIT0090" data-open="CIT0090" class="link link-ref link-reveal xref-bibr">Olariu <em>et al.</em>, 2017</a>).</p><p class="chapter-para">The recent findings reported here support the hypothesis that treatments with modulators of the recently identified key regulating processes—or with novel small molecules with reported cell reprogramming activity—will increase the efficiency of <em>in vitro</em> microspore embryogenesis, by reducing cell death levels and enhancing cell reprogramming and initiation of embryogenesis. Future studies to identify new elements of the regulatory hormonal and epigenetic pathways controlling plant cell reprogramming, together with the screening of chemical libraries of novel small bioactive molecules (including autophagy, and epigenetic and enzymatic activity modulators), will pave the way for new biotechnological strategies, by using small cell-permeable synthetic molecules—which are easy to apply and remove from cultures— to enhance cell reprogramming. This will open up new possibilities for improving the efficiency of <em>in vitro</em> microspore embryogenesis systems for DH plant production in breeding and conservation programmes, even in recalcitrant crops.</p> <h2 scrollto-destination=136423311 id="136423311" class="backacknowledgements-title js-splitscreen-backacknowledgements-title" data-legacy-id=A1>Acknowledgements</h2> <p class="chapter-para">Research at Testillano’s laboratory is supported by projects (AGL2014-52028-R and AGL2017-82447-R) funded by the Spanish Ministry of Economy and Competitiveness (MINECO) and the European Regional Development Fund (ERDF/FEDER). Support of TRANSAUTOPHAGY COST action, European Network of Multidisciplinary Research and Translation of Autophagy Knowledge (CA15138), is acknowledged. The author thanks M.C. Risueño for helpful scientific discussions, and M.T. Solís, I. Bárány, E. Berenguer, Y. Pérez-Pérez, E. Carneros, and A. 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