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Transcriptional network regulation of the brassinosteroid signaling pathway by the BES1–TPL–HDA19 co-repressor complex

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Abstract

Main conclusion

The brassinosteroid-related BES1 and BZR1 transcription factors dynamically modulate downstream gene networks via the TPL–HDA19 co-repressor complex in BR-signaling pathways in Arabidopsis thaliana.

Abstract

Brassinosteroids (BRs) are plant steroid hormones that are essential for diverse growth and developmental processes across the whole life cycle of plants. In Arabidopsis thaliana, the BR-related transcription factors BRI1-EMS-SUPPRESSOR 1 (BES1) and BRASSINAZOLE-RESISTANT 1 (BZR1) regulate a range of global gene expression in response to BR and several external signaling cues; however, the molecular mechanisms by which they mediate the reprogramming of downstream transcription remain unclear. We here report that formation of a protein complex between BES1 and BZR1 and Histone Deacetylase 19 (HDA19) via the conserved ERF-associated amphiphilic repression (EAR) motif proved essential for regulation of BR-signaling-related gene expression. Defects in BR-related functions of BES1 and BZR1 proteins containing a mutated EAR motif were completely rescued by artificial fusion with EAR-repression domain (SRDX), TOPLESS (TPL), or HDA19 proteins. RNA-sequencing analysis of Arabidopsis plants over-expressing bes1-DmEAR or bes1-DmEAR-HDA19 revealed an essential role for HDA19 activity in regulation of BES1/BZR1-mediated BR signaling. In addition to BR-related gene expression, the BES1–HDA19 transcription factor complex was important for abiotic stress-related drought stress tolerance and organ boundary formation. These results suggested that integrating activation of BR-signaling pathways with the formation of the protein complex containing BES1/BZR1 and TPL–HDA19 via the EAR motif was important in fine-tuning BR-related gene networks in plants.

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Abbreviations

BR:

Brassinosteroid

EAR:

ERF-associated amphiphilic repression

TPL:

TOPLESS

HDA19:

Histone deacetylase 19

BES1:

BRI1-EMS-SUPPRESSOR 1

BZR1:

BRASSINAZOLE-RESISTANT 1

DEG:

Differentially expressed genes

GO:

Gene ontology

References

  • Bell EM, Lin WC, Husbands AY, Yu L, Jaganatha V, Jablonska B, Mangeon A, Neff MM, Girke T, Springer PS (2012) Arabidopsis lateral organ boundaries negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. Proc Natl Acad Sci USA 109:21146–21151

    Article  PubMed  Google Scholar 

  • Causier B, Ashworth M, Guo W, Davies B (2011) The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158:423–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Biol 49:427–451

    Article  CAS  Google Scholar 

  • Clouse SD, Langford M, McMorris TC (1996) A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111:671–678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Espinosa-Ruiz A, Martínez C, de Lucas M, Fàbregas N, Bosch N, Caño-Delgado AI, Prat S (2017) TOPLESS mediates brassinosteroid control of shoot boundaries and root meristem development in Arabidopsis thaliana. Development 144:1619–1628. https://doi.org/10.1242/dev.143214

    Article  CAS  PubMed  Google Scholar 

  • Fletcher JC (2002) Shoot and floral meristem maintenance in Arabidopsis. Annu Rev Plant Biol 53:45–66

    Article  CAS  PubMed  Google Scholar 

  • Gendron JM, Liu J-S, Fan M, Bai M-Y, Wenkel S, Springer PS, Barton MK, Wang Z-Y (2012) Brassinosteroids regulate organ boundary formation in the shoot apical meristem of Arabidopsis. Proc Natl Acad Sci USA 109:21152–21157

    Article  PubMed  Google Scholar 

  • González-García M-P, Vilarrasa-Blasi J, Zhiponova M, Divol F, Mora-García S, Russinova E, Caño-Delgado AI (2011) Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 138:849–859

    Article  CAS  PubMed  Google Scholar 

  • Greer CB, Tanaka Y, Kim YJ, Xie P, Zhang MQ, Park I-H, Kim TH (2015) Histone deacetylases positively regulate transcription through the elongation machinery. Cell Rep 13:1444–1455

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ha Y, Shang Y, Nam KH (2016) Brassinosteroids modulate ABA-induced stomatal closure in Arabidopsis. J Exp Bot 67:6297–6308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heyman J, Cools T, Vandenbussche F, Heyndrickx KS, Van Leene J, Vercauteren I, Vanderauwera S, Vandepoele K, De Jaeger G, Van Der Straeten D (2013) ERF115 controls root quiescent center cell division and stem cell replenishment. Science 342:860–863

    Article  CAS  PubMed  Google Scholar 

  • Jian W, Yan B, Huang S, Qiu Y (2017) Histone deacetylase 1 activates PU. 1 gene transcription through regulating TAF9 deacetylation and transcription factor IID assembly. FASEB J 31:4104–4116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kagale S, Rozwadowski K (2011) EAR motif-mediated transcriptional repression in plants: an underlying mechanism for epigenetic regulation of gene expression. Epigenetics 6:141–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kauschmann A, Jessop A, Koncz C, Szekeres M, Willmitzer L, Altmann T (1996) Genetic evidence for an essential role of brassinosteroids in plant development. Plant J 9:701–713

    Article  CAS  Google Scholar 

  • Kim T-W, Wang Z-Y (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61:681–704

    Article  CAS  PubMed  Google Scholar 

  • Lee H-S, Kim Y, Pham G, Kim JW, Song J-H, Lee Y, Hwang Y-S, Roux SJ, Kim S-H (2015) Brassinazole resistant 1 (BZR1)-dependent brassinosteroid signalling pathway leads to ectopic activation of quiescent cell division and suppresses columella stem cell differentiation. J Exp Bot 66:4835–4849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee J, Shim D, Moon S, Kim H, Bae W, Kim K, Kim Y-H, Rhee S-K, Hong CP, Hong S-Y (2018) Genome-wide transcriptomic analysis of BR-deficient Micro-Tom reveals correlations between drought stress tolerance and brassinosteroid signaling in tomato. Plant Physiol Biochem 127:553–560

    Article  CAS  PubMed  Google Scholar 

  • Li Q-F, Lu J, Yu J-W, Zhang C-Q, He J-X, Liu Q-Q (2018) The brassinosteroid-regulated transcription factors BZR1/BES1 function as a coordinator in multisignal-regulated plant growth. BBA Gene Regul Mech 1861:561–571

    CAS  Google Scholar 

  • Liu Z, Karmarkar V (2008) Groucho/Tup1 family co-repressors in plant development. Trends Plant Sci 13:137–144

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Yang S, Zhao M, Luo M, Yu C-W, Chen C-Y, Tai R, Wu K (2014) Transcriptional repression by histone deacetylases in plants. Mol Plant 7:764–772

    Article  CAS  PubMed  Google Scholar 

  • Mondragón-Palomino M, Stam R, John-Arputharaj A, Dresselhaus T (2017) Diversification of defensins and NLRs in Arabidopsis species by different evolutionary mechanisms. BMC Evol Biol 17:255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nolan T, Chen J, Yin Y (2017) Cross-talk of brassinosteroid signaling in controlling growth and stress responses. Biochem J 474:2641–2661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nusinzon I, Horvath CM (2005) Histone deacetylases as transcriptional activators? Role reversal in inducible gene regulation. Sci STKE 2005:re11. https://doi.org/10.1126/stke.2962005re11

    Article  PubMed  Google Scholar 

  • Oh E, Zhu J-Y, Ryu H, Hwang I, Wang Z-Y (2014) TOPLESS mediates brassinosteroid-induced transcriptional repression through interaction with BZR1. Nat Commun 5:4140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reddy GV, Heisler MG, Ehrhardt DW, Meyerowitz EM (2004) Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex of Arabidopsis thaliana. Development 131:4225–4237

    Article  CAS  PubMed  Google Scholar 

  • Ryu H, Cho Y-G (2015) Plant hormones in salt stress tolerance. J Plant Biol 58:147–155

    Article  CAS  Google Scholar 

  • Ryu H, Kim K, Cho H, Park J, Choe S, Hwang I (2007) Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling. Plant Cell 19:2749–2762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ryu H, Cho H, Bae W, Hwang I (2014) Control of early seedling development by BES1/TPL/HDA19-mediated epigenetic regulation of ABI3. Nat Commun 5:4138

    Article  CAS  PubMed  Google Scholar 

  • Vilarrasa-Blasi J, González-García M-P, Frigola D, Fàbregas N, Alexiou KG, López-Bigas N, Rivas S, Jauneau A, Lohmann JU, Benfey PN (2014) Regulation of plant stem cell quiescence by a brassinosteroid signaling module. Dev Cell 30:36–47

    Article  CAS  PubMed  Google Scholar 

  • Wang Z-Y, Nakano T, Gendron J, He J, Chen M, Vafeados D, Yang Y, Fujioka S, Yoshida S, Asami T (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2:505–513

    Article  CAS  PubMed  Google Scholar 

  • Ye H, Liu S, Tang B, Chen J, Xie Z, Nolan TM, Jiang H, Guo H, Lin H-Y, Li L (2017) RD26 mediates crosstalk between drought and brassinosteroid signalling pathways. Nat Commun 8:14573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin Y, Wang Z-Y, Mora-Garcia S, Li J, Yoshida S, Asami T, Chory J (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109:181–191

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J (2005) A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120:249–259

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was carried out with the support of the Basic Science Research Program through the National Research Foundation of Korea (2015R1A4A1041869), Korean Ministry of Science, ICT and Future Planning, and the Cooperative Research Program for Agriculture Science & Technology Development (Project No. PJ01283704 and PJ012805 for K. Kim), Rural Development Administration, Republic of Korea.

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  1. Hyemin Kim and Donghwan Shim contributed equally to this work as the first authors.

Authors and Affiliations

  1. Department of Biology, Chungbuk National University, Cheongju, 28644, Republic of Korea

    Hyemin Kim, Suyun Moon, Jinsu Lee, Wonsil Bae, Kyunghwan Kim & Hojin Ryu

  2. Department of Forest Bio-Resources, National Institute of Forest Science, Suwon, 16631, Republic of Korea

    Donghwan Shim & Hyunmo Choi

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  1. Hyemin Kim
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Correspondence to Hojin Ryu.

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Kim, H., Shim, D., Moon, S. et al. Transcriptional network regulation of the brassinosteroid signaling pathway by the BES1–TPL–HDA19 co-repressor complex. Planta 250, 1371–1377 (2019). https://doi.org/10.1007/s00425-019-03233-z

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