HEAT SHOCK PROTEIN 90 proteins and YODA regulate main body axis formation during early embryogenesis

. 2021 Jul 06 ; 186 (3) : 1526-1544.

Jazyk angličtina Země Spojené státy americké Médium print

Typ dokumentu srovnávací studie, časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33856486

The YODA (YDA) kinase pathway is intimately associated with the control of Arabidopsis (Arabidopsis thaliana) embryo development, but little is known regarding its regulators. Using genetic analysis, HEAT SHOCK PROTEIN 90 (HSP90) proteins emerge as potent regulators of YDA in the process of embryo development and patterning. This study is focused on the characterization and quantification of early embryonal traits of single and double hsp90 and yda mutants. HSP90s genetic interactions with YDA affected the downstream signaling pathway to control the development of both basal and apical cell lineage of embryo. Our results demonstrate that the spatiotemporal expression of WUSCHEL-RELATED HOMEOBOX 8 (WOX8) and WOX2 is changed when function of HSP90s or YDA is impaired, suggesting their essential role in the cell fate determination and possible link to auxin signaling during early embryo development. Hence, HSP90s together with YDA signaling cascade affect transcriptional networks shaping the early embryo development.

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Armenta-Medina A, Gillmor CS. (2019) Genetic, molecular and parent-of-origin regulation of early embryogenesis in flowering plants. Curr Top Dev Biol 131: 497–543 PubMed

Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W. (2009) Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323: 1485–1488 PubMed

Beck M, Komis G, Müller J, Menzel D, Šamaj J. (2010) Arabidopsis homologs of nucleus- and phragmoplast-localized kinase 2 and 3 and mitogen-activated protein kinase 4 are essential for microtubule organization. Plant Cell 22: 755–771 PubMed PMC

Bergmann DC, Sack FD. (2007) Stomatal development. Ann Rev Plant Biol 58: 163–181 PubMed

Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T. (2008) Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo .Dev Cell 14: 867–876 PubMed

Bush SM, Krysan PJ. (2007). Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo development. J Exp Bot 58: 2181–2191 PubMed

Costa LM, Marshall E, Tesfaye M, Silverstein KA, Mori M, Umetsu Y, Otterbach SL, Papareddy R, Dickinson HG, Boutiller K, et al. (2014) Central cell-derived peptides regulate early embryo patterning in flowering plants. Science 344: 168–172 PubMed

D’Alessandro S, Golin S, Hardtke CS, Lo Schiavo F, Zottini M. (2015) The co-chaperone p23 controls root development through the modulation of auxin distribution in the Arabidopsis root meristem. J Exp Bot 66: 5113–5122 PubMed PMC

Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B. (1993) Cellular organisation of the Arabidopsis thaliana root. Development 119: 71–84 PubMed

Dong J, MacAlister CA, Bergmann DC. (2009) BASL controls asymmetric cell division in Arabidopsis. Cell 137: 1320–1330 PubMed PMC

Feng J, Fan P, Jiang P, Lv S, Chen X, Li Y. (2014) Chloroplast-targeted Hsp90 plays essential roles in plastid development and embryogenesis in Arabidopsis possibly linking with VIPP1. Physiol Plant 150: 292–307 PubMed

Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426: 147–153 PubMed

Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T. (2004) Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131: 657–668 PubMed

Haralampidis K, Milioni D, Rigas S, Hatzopoulos P. (2002) Combinatorial interaction of cis elements specifies the expression of the Arabidopsis AtHsp90-1gene. Plant Physiol 129: 1138–1149 PubMed PMC

Hartman JL, Garvik B, Hartwell L. (2001) Principles for the buffering of genetic variation. Science 291: 1001–1004 PubMed

Hofmann F, Schon MA, Nodine MD. (2019) The embryonic transcriptome of Arabidopsis thaliana. Plant Reprod 32: 77–91 PubMed

Hubert DA, He Y, McNulty BC, Tornero P, Dangl JL. (2009) Specific Arabidopsis HSP90.2 alleles recapitulate RAR1 cochaperone function in plant NB-LRR disease resistance protein regulation. Proc Natl Acad Sci USA 106: 9556–9563 PubMed PMC

Jarosz DF, Taipale M, Lindquist S. (2010) Protein homeostasis and the phenotypic manifestation of genetic diversity: principles and mechanisms. Ann Rev Genet 44: 189–216 PubMed

Jeong S, Palmer TM, Lukowitz W. (2011) The RWP-RK factor GROUNDED promotes embryonic polarity by facilitating YODA MAP kinase signaling. Curr Biol 21: 1268–1276 PubMed

Jia W, Li B, Li S, Liang Y, Wu X, Ma M, Wang J, Gao J, Cai Y, Zhang Y, et al. (2016) Mitogen-activated protein kinase cascade MKK7-MPK6 plays important roles in plant development and regulates shoot branching by phosphorylating PIN1 in Arabidopsis .PLoS Biol 14: e1002550. PubMed PMC

Jürgens G, Mayer U. (1994) Arabidopsis. In Bard J, ed, A Colour Atlas of Developing Embryos. Wolfe Publishing, London, pp 7–21

Kamphausen T, Fanghänel J, Neumann D, Schulz B, Rahfeld JU. (2002) Characterization of Arabidopsis thaliana AtFKBP42 that is membrane-bound and interacts with Hsp90. Plant J 32: 263–276 PubMed

Khurana N, Bhattacharyya S. (2015) Hsp90, the concertmaster: tuning transcription. Front Oncol 5: 100. PubMed PMC

Klepikova AV, Kasianov AS, Gerasimov ES, Logacheva MD, Penin AA. (2016) A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA‐seq profiling. Plant J 88: 1058–1070 PubMed

Komis G, Šamajová O, Ovečka M, Šamaj J. (2018) Cell and developmental biology of plant mitogen-activated protein kinases. Ann Rev Plant Biol 69: 237–265 PubMed

Lau S, Slane D, Herud O, Kong J, Jürgens G. (2012) Early embryogenesis in flowering plants: setting up the basic body pattern. Ann Rev Plant Biol 63: 483–506 PubMed

Li B, Tang M, Nelson A, Caligagan H, Zhou X, Clark-Wiest C, Ngo R, Brady SM, Kliebenstein DJ (2018) Network-guided discovery of extensive epistasis between transcription factors involved in aliphatic glucosinolate biosynthesis. Plant Cell 30: 178–195 PubMed PMC

Lukowitz W, Roeder A, Parmenter D, Somerville C. (2004) A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116: 109–119 PubMed

Mansfield SG, Briarty LG. (1991) Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can J Bot 69: 461–476

Margaritopoulou T, Kryovrysanaki N, Megkoula P, Prassinos C, Samakovli D, Milioni D, Hatzopoulos P. (2016) HSP90 canonical content organizes a molecular scaffold mechanism to progress flowering. Plant J 87: 174–187 PubMed

Meng LS, Li YQ, Liu MQ, Jiang JH. (2016) The Arabidopsis ANGUSTIFOLIA3-YODA gene cascade induces anthocyanin accumulation by regulating sucrose levels. Front Plant Sci 7: 1728. PubMed PMC

Meng X, Wang H, He Y, Liu Y, Walker JC, Torii KU, Zhang S. (2012) A MAPK cascade downstream of ERECTA receptor-like protein kinase regulates Arabidopsis inflorescence architecture by promoting localized cell proliferation. Plant Cell 24: 4948–4960 PubMed PMC

Miao Y, Smykowski A, Zentgraf U. (2008). A novel upstream regulator of WRKY53 transcription during leaf senescence in Arabidopsis thaliana. Plant Biol 10: 110–120 PubMed

Milioni D, Hatzopoulos P. (1997) Genomic organization of HSP90 gene family in Arabidopsis. Plant Mol Biol 35: 955–961 PubMed

Möller B, Weijers D. (2009) Auxin control of embryo patterning. Cold Spring Harbor Perspect Biol 1: a001545 PubMed PMC

Müller J, Beck M, Mettbach U, Komis G, Hause G, Menzel D, Samaj J. (2010) Arabidopsis MPK6 is involved in cell division plane control during early root development, and localizes to the pre-prophase band, phragmoplast, trans-Golgi network and plasma membrane. Plant J 61: 234–248 PubMed

Musielak TJ, Schenkel L, Kolb M, Henschen A, Bayer M. (2015) A simple and versatile cell wall staining protocol to study plant reproduction. Plant Reprod 28: 161–169 PubMed PMC

Neckers L, Mollapour M, Tsutsumi S. (2009) The complex dance of the molecular chaperone Hsp90. Trend Biochem Sci 34: 223–226 PubMed PMC

Neu A, Eilbert E, Asseck LY, Slane D, Henschen A, Wang K, Bürgel P, Hildebrandt M, Musielak TJ, Kolb M, et al. (2019) Constitutive signaling activity of a receptor-associated protein links fertilization with embryonic patterning in Arabidopsis thaliana. Proc Natl Acad Sci USA 116: 5795–5804 PubMed PMC

Prasinos C, Krampis K, Samakovli D, Hatzopoulos P. (2005) Tight regulation of expression of two Arabidopsis cytosolic Hsp90 genes during embryo development. J Exp Bot 56: 633–644 PubMed

Queitsch C, Sangster TA, Lindquist S. (2002) HSP90 as a capacitor of phenotypic variation. Nature 417: 618–624 PubMed

Rutherford SL, Lindquist S. (1998) HSP90 as a capacitor for morphological evolution. Nature 396: 336–342 PubMed

Samakovli D, Margaritopoulou T, Prassinos C, Milioni D, Hatzopoulos P. (2014) Brassinosteroid nuclear signaling recruits HSP90 activity. New Phytol 203: 743–757 PubMed

Samakovli D, Roka L, Plitsi PK, Kaltsa I, Daras G, Milioni D, Hatzopoulos P. (2020a). Active BR signaling adjusts the subcellular localization of BES1/HSP90 complex formation. Plant Biol 22: 129–133 PubMed

Samakovli D, Thanou A, Valmas C, Hatzopoulos P. (2007) HSP90 canalizes developmental perturbation. J Exp Bot 58: 3513–3524 PubMed

Samakovli D, Tichá T, Šamaj J. (2020c) HSP90 chaperones regulate stomatal differentiation under normal and heat stress conditions. Plant Signal Behav 15: 1789817. PubMed PMC

Samakovli D, Tichá T, Vavrdová T, Ovečka M, Luptovčiak I, Zapletalová V, Kuchařová A, Křenek P, Krasylenko Y, Margaritopoulou T, et al. (2020b) YODA-HSP90 module regulates phosphorylation-dependent inactivation of SPEECHLESS to control stomatal development under acute heat stress in Arabidopsis. Mol Plant 13: 612–633 PubMed

Sangster TA, Bahrami A, Wilczek A, Watanabe E, Schellenberg K, McLellan C, Kelley A, Kong SW, Queitsch C, Lindquist S. (2007) Phenotypic diversity and altered environmental plasticity in Arabidopsis thaliana with reduced Hsp90 levels. PLoS One 2: e648. PubMed PMC

Schneider CA, Rasband WS, Eliceiri KW. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675 PubMed PMC

Segrè D, Deluna A, Church GM, Kishony R. (2005) Modular epistasis in yeast metabolism. Nat Genet 37: 77–83 PubMed

Shigeta T, Zaizen Y, Sugimoto Y, Nakamura Y, Matsuo T, Okamoto S. (2015) Heat shock protein 90 acts in brassinosteroid signaling through interaction with BES1/BZR1 transcription factor .J Plant Physiol 178: 69–73 PubMed

Smékalová V, Luptovčiak I, Komis G, Šamajová O, Ovečka M, Doskočilová A, Takáč T, Vadovič P, Novák O, Pechan T, et al. (2014) Involvement of YODA and mitogen activated protein kinase 6 in Arabidopsis post-embryogenic root development through auxin up-regulation and cell division plane orientation. New Phytol 203: 1175–1193 PubMed PMC

Taipale M, Jarosz DF, Lindquist S. (2010) HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 11: 515–528 PubMed

Tejos RI, Mercado AV, Meisel LA. (2010) Analysis of chlorophyll fluorescence reveals stage specific patterns of chloroplast-containing cells during Arabidopsis embryogenesis. Biol Res 43: 99–111 PubMed

ten Hove CA, Lu KJ, Weijers D. (2015) Building a plant: cell fate specification in the early Arabidopsis embryo. Development 142: 420–430 PubMed

Tichá T, Samakovli D, Kuchařová A, Vavrdová T, Šamaj J. (2020) Multifaceted roles of HEAT SHOCK PROTEIN 90 molecular chaperones in plant development. J Exp Bot 71: 3966–3985 PubMed

Truernit E, Bauby H, Dubreucq B, Grandjean O, Runions J, Barthélémy J, Palauqui JC. (2008) High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of phloem development and structure in Arabidopsis. Plant Cell 20: 1494–1503 PubMed PMC

Ueda M, Aichinger E, Gong W, Groot E, Verstraeten I, Vu LD, De Smet I, Higashiyama T, Umeda M, Laux T (2017) Transcriptional integration of paternal and maternal factors in the Arabidopsis zygote. Genes Dev 31: 617–627 PubMed PMC

Ueda M, Zhang Z, Laux T. (2011) Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev Cell 20: 264–270 PubMed

Waki T, Hiki T, Watanabe R, Hashimoto T, Nakajima K. (2011) The Arabidopsis RWP-RK protein RKD4 triggers gene expression and pattern formation in early embryogenesis. Curr Biol 21: 1277–1281 PubMed

Wandinger SK, Richter K, Buchner J. (2008) The Hsp90 chaperone machinery. J Biol Chem 283: 18473–18477 PubMed

Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S. (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19: 63–73 PubMed PMC

Wang R, Zhang Y, Kieffer M, Yu H, Kepinski S, Estelle M. (2016) HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1. Nat Commun 7: 10269. PubMed PMC

Watanabe E, Mano S, Nomoto M, Tada Y, Hara-Nishimura I, Nishimura M, Yamada K. (2016) HSP90 stabilizes auxin-responsive phenotypes by masking a mutation in the auxin receptor TIR1. Plant Cell Physiol 57: 2245–2254 PubMed

Wei Y, Liu W, Hu W, Yan Y, Shi H. (2019) The chaperone MeHSP90 recruits MeWRKY20 and MeCatalase1 to regulate drought stress resistance in cassava. New Phytol 226: 476–491 PubMed

Wei Y, Zhu B, Liu W, Cheng X, Lin D, He C, Shi H. (2021) Heat shock protein 90 co-chaperone modules fine-tune the antagonistic interaction between salicylic acid and auxin biosynthesis in cassava. Cell Rep 34: 108717. PubMed

Wu G, Otegui MS, Spalding EP. (2010) The ER-localized TWD1 immunophilin is necessary for localization of multidrug resistance-like proteins required for polar auxin transport in Arabidopsis roots. Plant Cell 22: 3295–3304 PubMed PMC

Wu X, Chory J, Weigel D. (2007) Combinations of WOX activities regulate tissue proliferation during Arabidopsis embryonic development. Dev Biol 309: 306–316 PubMed PMC

Yoshida S, Barbier de Reuille P, Lane B, Bassel GW, Prusinkiewicz P, Smith RS, Weijers D. (2014) Genetic control of plant development by overriding a geometric division rule. Dev Cell 29: 75–87 PubMed

Zhang Y, Wang P, Shao W, Zhu JK, Dong J. (2015) The BASL polarity protein controls a MAPK signaling feedback loop in asymmetric cell division. Dev Cell 33: 136–149 PubMed PMC

Zhang Z, Tucker E, Hermann M, Laux T. (2017) A molecular framework for the embryonic initiation of shoot meristem stem cells. Dev Cell 40: 264–277 PubMed

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