Stomatal development is tightly connected with the overall plant growth, while changes in environmental conditions, like elevated temperature, affect negatively stomatal formation. Stomatal ontogenesis follows a well-defined series of cell developmental transitions in the cotyledon and leaf epidermis that finally lead to the production of mature stomata. YODA signaling cascade regulates stomatal development mainly through the phosphorylation and inactivation of SPEECHLESS (SPCH) transcription factor, while HSP90 chaperones have a central role in the regulation of YODA cascade. Here, we report that acute heat stress affects negatively stomatal differentiation, leads to high phosphorylation levels of MPK3 and MPK6, and alters the expression of SPCH and MUTE transcription factors. Genetic depletion of HSP90 leads to decreased stomatal differentiation rates. Thus, HSP90 chaperones safeguard the completion of distinct stomatal differentiation steps depending on these two transcription factors under normal and heat stress conditions.

Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Olomouc Olomouc Czech Republic

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Hetherington AM, Woodward FI.. The role of stomata in sensing and driving environmental change. Nature. 2003;424:1–5. PMID:12931178. doi:10.1038/nature01843. PubMed DOI

Zoulias N, Harrison EL, Casson SA, Gray JE.. Molecular control of stomatal development. Biochem J. 2018;475:441–454. doi:10.1042/BCJ20170413. PubMed DOI PMC

Gray JE. Plant development: three steps for stomata. Curr Biol. 2007;17:R213–R215. doi:10.1016/j.cub.2007.01.032. PubMed DOI

Pillitteri LJ, Sloan DB, Bogenschutz NL, Torii KU. Termination of asymmetric cell division and differentiation of stomata. Nature. 2007;445:501–505. PMID:17183267. doi:10.1038/nature05467. PubMed DOI

Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell. 2007;19:63–73. doi:10.1105/tpc.106.048298. PubMed DOI PMC

Bush SM, Krysan PJ. Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo development. J Exp Bot. 2007;58:2181–2191. doi:10.1093/jxb/erm092. PubMed DOI

Komis G, Šamajová O, Ovečka M, Šamaj J. Cell and developmental biology of plant mitogen-activated protein kinases. Annu Rev Plant Biol. 2018;69:237–265. doi:10.1146/annurev-arplant-042817-040314. PubMed DOI

Taipale M, Jarosz DF, Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Mol Cell Biol. 2010;11:515–528. PMID:20531426. doi:10.1038/nrm2918. PubMed DOI

Queitsch C, Sangster TA, Lindquist S. HSP90 as a capacitor of phenotypic variation. Nature. 2002;417:618–624. PMID:12050657. doi:10.1038/nature749. PubMed DOI

Samakovli D, Thanou A, Valmas C, Hatzopoulos P. HSP90 canalizes developmental perturbation. J Exp Bot. 2007;58:3513–3524. doi:10.1093/jxb/erm191. PubMed DOI

Samakovli D, Margaritopoulou T, Prassinos C, Milioni D, Hatzopoulos P. Brassinosteroid nuclear signaling recruits HSP90 activity. New Phytol. 2014;203:743–757. doi:10.1111/nph.12843. PubMed DOI

Samakovli D, Roka L, Plitsi PK, Kaltsa I, Daras G, Milioni D, Hatzopoulos, P. Active BR signaling adjusts the subcellular localization of BES1/HSP90 complex formation. Plant Biol. 2019. doi:10.1111/plb.13040. PubMed DOI

Jarosz DF, Taipale M, Lindquist S. Protein homeostasis and the phenotypic manifestation of genetic diversity: principles and mechanisms. Annu Rev Genet. 2010;44:189–216. PMID:21047258. doi:10.1146/annurev.genet.40.110405.090412. PubMed DOI

Margaritopoulou T, Kryovrysanaki N, Megkoula P, Prassinos C, Samakovli D, Milioni D, Hatzopoulos P. HSP90 canonical content organizes a molecular scaffold mechanism to progress flowering. Plant J. 2016;87:174–187. doi:10.1111/tpj.13191. PubMed DOI

Tichá T, Samakovli D, Kuchařová A, Vavrdová T, Šamaj J. Multifaceted roles of HEAT SHOCK PROTEIN 90 molecular chaperones in plant development. J Exp Bot. 2020. published online Apr 2020. doi:10.1093/jxb/eraa177. PubMed DOI

Samakovli D, Tichá T, Vavrdová T, Ovečka M, Luptovčiak I, Zapletalová V, Kuchařová A, Křenek P, Krasylenko Y, Margaritopoulou T, et al. YODA-HSP90 module regulates phosphorylation-dependent inactivation of SPEECHLESS to control stomatal development under acute heat stress in Arabidopsis. Mol Plant. 2020;13:612–633. doi:10.1016/j.molp.2020.01.001. PubMed DOI

Putarjunan A, Torii KU. Heat shocking the jedi master: HSP90’s role in regulating stomatal cell fate. Mol Plant. 2020;13:536–538. doi:10.1016/j.molp.2020.03.001. PubMed DOI

Vatèn A, Soyars CL, Tarr PT, Nimchuk ZL, Bergmann DC. Modulation of asymmetric division diversity through cytokinin and SPEECHLESS regulatory interactions in the arabidopsis stomatal lineage. Dev Cell. 2018;47:53–66. doi:10.1016/j.devcel.2018.08.007. PubMed DOI PMC

Han SK, Qi X, Sugihara K, Dang JH, Endo TA, Miller KL, Kim ED, Miura T, Torii KU. MUTE directly orchestrates cell-state switch and the single symmetric division to create stomata. Dev Cell. 2018;45:303–315. 10.1016/j.devcel.2018.04.010. PubMed DOI

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