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• W2893142413 abstract "News & Views1 October 2018free access Epigenetically jump starting de novo shoot regeneration Ning Zhang BIOSS Centre for Biological Signaling Studies, Faculty of Biology, Albert-Ludwigs-Universität Freiburg, Freiburg, Germany Search for more papers by this author Thomas Laux [email protected] orcid.org/0000-0001-6659-0515 BIOSS Centre for Biological Signaling Studies, Faculty of Biology, Albert-Ludwigs-Universität Freiburg, Freiburg, Germany Sino-German Joint Research Center on Agricultural Biology, Shandong Agricultural University, Tai'an, Shandong, China Search for more papers by this author Ning Zhang BIOSS Centre for Biological Signaling Studies, Faculty of Biology, Albert-Ludwigs-Universität Freiburg, Freiburg, Germany Search for more papers by this author Thomas Laux [email protected] orcid.org/0000-0001-6659-0515 BIOSS Centre for Biological Signaling Studies, Faculty of Biology, Albert-Ludwigs-Universität Freiburg, Freiburg, Germany Sino-German Joint Research Center on Agricultural Biology, Shandong Agricultural University, Tai'an, Shandong, China Search for more papers by this author Author Information Ning Zhang1 and Thomas Laux1,2 1BIOSS Centre for Biological Signaling Studies, Faculty of Biology, Albert-Ludwigs-Universität Freiburg, Freiburg, Germany 2Sino-German Joint Research Center on Agricultural Biology, Shandong Agricultural University, Tai'an, Shandong, China EMBO J (2018)37:e100596https://doi.org/10.15252/embj.2018100596 See also: JY Kim et al (October 2018) PDFDownload PDF of article text and main figures. ToolsAdd to favoritesDownload CitationsTrack CitationsPermissions ShareFacebookTwitterLinked InMendeleyWechatReddit Figures & Info The ability to regenerate lost organs or tissues is a central requirement for animals and plants in order to cope with injury. Regeneration of a whole body is rare in animals but is more commonly found in plants where in vitro regeneration has become a widely used tool in plant research. In a new study, Kim et al find that epigenetic changes via the histone acetyltransferase HAG1 establish the competency for shoot regeneration from callus by promoting the expression of root stem cell factors. More than six decades ago, Skoog and Miller established a two-step process procedure that has become widely adapted to many plant species for in vitro regeneration of complete plants from excised tissue fragments. First, pieces of plant tissue are incubated on auxin-rich callus induction medium (CIM) to form a proliferating cell mass, the callus. Subsequent transfer to cytokinin-rich shoot induction medium (SIM) induces shoot formation, whereas transfer to only auxin-containing root-inducing medium (RIM) results in root formation. The ease of this procedure has made it a model to study the mechanisms underlying regeneration in plants. One outstanding finding of the recent years is that callus development shares many properties with lateral root initiation (Sugimoto et al, 2010). In the first step, xylem-associated pericycle cells in roots or pericycle-like cells in shoot organs enter mitosis and act as pluripotent founder cells for the callus very similar to their role as founder cells for lateral root primordia. In Arabidopsis, several regulators of the root meristem stem cells are upregulated during—and are required for—callus formation, regardless of whether shoot or root explants are used. These include members of the WUSCHEL-RELATED HOMEOBOX (WOX) family, PLETHORA 1 (PLT1), PLT2, and SCARECROW (SCR; Sugimoto et al, 2010; Lee & Seo, 2018; Sang et al, 2018). Recently, regeneration studies have focused on epigenetic mechanisms. In animals and plants, the epigenetic state of a cell is a key factor of its developmental potency (Lee & Seo, 2018). In pluripotent cells, many genes are maintained in an open chromatin state while cell differentiation genes are transcriptionally silenced. In differentiated cells, on the other hand, pluripotency genes are silenced by DNA methylation and histone modifications (Lee & Seo, 2018; Sang et al, 2018). In line with the pluripotent nature of callus cells, which can give rise to a complete plant including the germ cells, activating epigenetic marks are enriched and repressive marks are depleted compared to differentiated cells. Direct evidence for an important role for the epigenetic landscape in regeneration comes, for example, from mutations resulting in DNA hypomethylation that enable direct shoot regeneration from explants without a callus intermediate, indicating the presence of an epigenetic block for shoot formation in wild-type plants (Shemer et al, 2015). In order to better understand the role of epigenetic regulation in callus-derived shoot regeneration, Kim et al (2018) applied the Miller and Skoog protocol to a number of epigenetic mutants in the model plant Arabidopsis thaliana. They found that explants of loss-of-function mutants for the histone acetyltransferase HAG1 are able to form a somewhat enlarged callus on CIM (Fig 1). These calli are capable of giving rise to roots when cultured on RIM but fail to regenerate shoots when cultured on SIM. In yeast and humans, the HAG1 homolog GCN5 catalyzes acetylation of histone H3 and is part of different complexes that promote transcription with both broad and specific sets of target genes. Transcript profiling during wild-type Arabidopsis shoot regeneration revealed that a large number (7,067) of differentially expressed genes (DEGs) are detected after the transition from root explants to callus while fewer are changed between callus and the induced shoot. In hag1 mutants, however, the number of upregulated genes during callus induction is strongly reduced, indicating that despite their morphological similarity, wild-type and hag1 calli are very different in their gene expression profile. Among the DEGs that were not or less upregulated in hag1 are the root stem cell factors WOX5, WOX7, WOX14, SCR, PLT1, and PLT2. These genes displayed lower histone H3 acetylation levels in hag1 compared to wild type, and HAG1-HA protein directly binds to their promoters. Moreover, single and multiple mutants of these genes are defective in de novo shoot regeneration in a similar manner as the hag1 mutant and overexpression of WOX5 and/or SCR in hag1 plants can partially recover shoot regeneration. From these studies, the authors conclude that histone acetylation by HAG1 causes upregulation of root stem cell factors that are essential for the acquisition of pluripotency during callus formation (Fig 1). HAG1 would thus in part play a similar role in callus as it does in the root meristem by promoting stem cell maintenance via regulating PLT1 and PLT2 genes (Kornet & Scheres, 2009). Figure 1. Acquisition of shoot forming potential by HAG1In callus, HAG1 promotes transcription of WOX, SCR, and PLT root stem cell regulators by histone acetylation at their promoters. Subsequently, these root stem cell factors are essential for de novo shoot regeneration. A hypothetical DNA binding protein recruiting HAG1 to the correct target genes is indicated by a (?). Exposure of wild-type callus (left panel) on SIM causes localized expression of the WUS (light green) in cells peripheral to shoot meristem progenitor cells from which shoots arise. By contrast, hag1 callus gives dispersed WUS expression and defective shoot formation (right panel). Nucleosomes are shown as discs wrapped by the DNA; blue modifications indicate acetylation of histone H3. Download figure Download PowerPoint At first sight, the failure to upregulate root meristem regulators seems counterintuitive to the inability of calli to give rise to the shoot, while root regeneration is normal. Furthermore, expression of the shoot stem cell regulator WUS on SIM is induced to normal levels in the hag1 mutant. However, the authors notice that when hag1 calli are cultured on SIM, WUS expression is dispersed across the callus and not localized in foci as it is in wild type (Fig 1). Previous genes expression studies showed that wild-type callus becomes partitioned into regions of different cell identity after transfer to SIM, including patches of shoot meristem progenitor cells where WUS expression is localized at the periphery, and into regions of high auxin response that do not initiate shoots (Gordon et al, 2007). This indicates that one important outcome of HAG1/WOX/SCR function is the spatial patterning within callus exposed to high cytokinin. In line with this model, the authors find that WOX5 and SCR are required for a limited time during cultivation on SIM to make a shoot. This study by Kim et al (2018) not only offers significant novel insight into the mechanism of in vitro regeneration, but also provides entry points for important future studies. What are the first steps after treating explants with a high auxin/cytokinin hormone regime that eventually result in WOX and SCR gene upregulation? It appears likely that other components are necessary in addition to HAG1. HAG1 is expressed in various tissues that do not initiate upregulation of root meristem regulators nor any form of dedifferentiation (Hruz et al, 2008), indicating that its readout is modified by the cellular context. Identification of specific transcription factors that could target HAG1 to the appropriate genes for promoting shoot regeneration from callus is one of the promising future goals (Fig 1). One eye-catching question addressed by the authors is whether expression of the root regulators WOX5, SCR, PLT1, and PLT2 could be sufficient to convert differentiated cells into pluripotent stem cells, in analogy to how the mammalian OSKM factors (OCT4, SOX2, KFL4, and MYC) can reprogram somatic cells into induced pluripotent stem cells (iPSC; Takahashi & Yamanaka, 2006). As the authors point out, several recent findings support this hypothesis. Ectopic expression of WOX5 reprograms differentiated columella cells into stem cell-like cells, in part by repressing the differentiation gene CDF4 via histone deacetylation (Pi et al, 2015). Likewise, SCR, PLT1, and PLT2 are required to repress differentiation of root stem cells, in part redundantly with WOX5 (Sabatini et al, 2003; Sarkar et al, 2007). In line with this hypothesis, the authors find that increasing the expression levels of WOX5 and SCR can not only partially suppress the regeneration defects in hag1 calli, but also increase shoot regeneration efficiency of wild-type calli when submitted to SIM treatment. It will therefore be interesting to address whether expression of these transcription factors, or combinations with other stem cell regulators, can bypass the requirement for hormone treatment to produce plant iPSC and in which cells this is possible. References Gordon SP, Heisler MG, Reddy GV, Ohno C, Das P, Meyerowitz EM (2007) Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development 134: 3539–3548CrossrefCASPubMedWeb of Science®Google Scholar Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator v3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinformatics 2008: 420747CrossrefPubMedGoogle Scholar Kim JY, Yang W, Forner J, Lohmann JU, Noh B, Noh YS (2018) Epigenetic reprogramming by histone acetyltransferase HAG1/AtGCN5 is required for pluripotency acquisition in Arabidopsis. EMBO J 37: e98726Wiley Online LibraryGoogle Scholar Kornet N, Scheres B (2009) Members of the GCN5 histone acetyltransferase complex regulate PLETHORA-mediated root stem cell niche maintenance and transit amplifying cell proliferation in Arabidopsis. Plant Cell 21: 1070–1079CrossrefCASPubMedWeb of Science®Google Scholar Lee K, Seo PJ (2018) Dynamic epigenetic changes during plant regeneration. Trends Plant Sci 23: 235–247CrossrefCASPubMedWeb of Science®Google Scholar Pi L, Aichinger E, van der Graaff E, Llavata-Peris CI, Weijers D, Hennig L, Groot E, Laux T (2015) Organizer-derived WOX5 signal maintains root columella stem cells through chromatin-mediated repression of CDF4 expression. Dev Cell 33: 576–588CrossrefCASPubMedWeb of Science®Google Scholar Sabatini S, Heidstra R, Wildwater M, Scheres B (2003) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 17: 354–358CrossrefCASPubMedWeb of Science®Google Scholar Sang YL, Cheng ZJ, Zhang XS (2018) Plant stem cells and de novo organogenesis. New Phytol 218: 1334–1339Wiley Online LibraryPubMedWeb of Science®Google Scholar Sarkar A, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446: 811–814CrossrefCASPubMedWeb of Science®Google Scholar Shemer O, Landau U, Candela H, Zemach A, Williams LE (2015) Competency for shoot regeneration from Arabidopsis root explants is regulated by DNA methylation. Plant Sci 238: 251–261CrossrefCASPubMedWeb of Science®Google Scholar Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18: 463–471CrossrefCASPubMedWeb of Science®Google Scholar Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663–676CrossrefCASPubMedWeb of Science®Google Scholar Previous ArticleNext Article Read MoreAbout the coverClose modalView large imageVolume 37,Issue 20,15 October 2018Cover: A quantitative analysis of neuropeptide‐secreting dense‐core vesicles (DCVs) using super‐resolution and electron microscopy provides insight into DCV distribution, abundance and release probability. From Claudia M Persoon, Ruud F Toonen, Matthijs Verhage and colleagues: Pool size estimations for dense‐core vesicles in mammalian CNS neurons. (Collage of micrographs from the article by Uta Mackensen) Volume 37Issue 2015 October 2018In this issue FiguresReferencesRelatedDetailsLoading ..." @default.
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