Skip to main content

Hormonal Signaling in Plants and Animals: An Epigenetics Viewpoint

  • Chapter
  • First Online:
Epigenetic Memory and Control in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 18))

Abstract

In the past 10 years, enormous progress has been made in elucidating the nature of plant hormone receptors. This has allowed much greater insight into the mechanisms underlying hormone-mediated effects on the level of gene expression, particularly for hormones whose main receptors are localized in the nucleus. Surprisingly, and in contrast to the case for intensively studied nuclear hormone receptors in animals, very little is known about the contribution of chromatin-based epigenetic mechanisms in conveying and integrating responses to plant hormones. Here, we examine the similarities and differences between plant and animal nuclear receptor systems with the aim of revealing analogies that could help identify possible intersections between plant hormone signaling and epigenetic mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Achard P, Vriezen WH, Van Der Straeten D, Harberd NP (2003) Ethylene regulates arabidopsis development via the modulation of DELLA protein growth repressor function. Plant Cell 15: 2816–2825

    Article  PubMed  CAS  Google Scholar 

  • Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94

    Article  PubMed  CAS  Google Scholar 

  • Aranda A, Pascual A (2001) Nuclear hormone receptors and gene expression. Physiol Rev 81:1269–1304

    PubMed  CAS  Google Scholar 

  • Archacki R, Buszewicz D, Sarnowski TJ, Sarnowska E, Rolicka AT, Tohge T, Fernie AR, Jikumaru Y, Kotlinski M, Iwanicka-Nowicka R, Kalisiak K, Patryn J, Halibart-Puzio J, Kamiya Y, Davis SJ, Koblowska MK, Jerzmanowski A (2013) BRAHMA ATPase of the SWI/SNF chromatin remodeling complex acts as a positive regulator of gibberellin-mediated responses in arabidopsis. PLoS ONE 8(3):e58588. doi: 10.1371/journal.pone.0058588

    Article  PubMed  CAS  Google Scholar 

  • Arya G, Maitra A, Grigoryev S (2010) A structural perspective on the where, how, why, and what of nucleosome positioning. J Biomol Struct Dyn 27:803–820

    Article  PubMed  CAS  Google Scholar 

  • Bai MY, Shang JX, Oh E, Fan M, Bai Y et al (2012) Brassinosteroid, gibberellin and phytochrome impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14:810–817

    Article  PubMed  CAS  Google Scholar 

  • Belandia B, Parker MG (2003) Nuclear receptors: a rendezvous for chromatin remodeling factors. Cell 114:277–280

    Article  PubMed  CAS  Google Scholar 

  • Belandia B, Orford RL, Hurst HC, Parker MG (2002) Targeting of SWI/SNF chromatin remodelling complexes to estrogen-responsive genes. EMBO J 21:4094–4103

    Article  PubMed  CAS  Google Scholar 

  • Bezhani S, Winter C, Hershman S, Wagner JD, Kennedy JF, Kwon CS, Pfluger J, Su Y, Wagner D (2007) Unique, shared, and redundant roles for the arabidopsis SWI/SNF chromatin remodeling ATPases BRAHMA and SPLAYED. Plant Cell 19:403–416

    Article  PubMed  CAS  Google Scholar 

  • Bishopp A, Mähönen AP, Helariutta Y (2006) Signs of change: hormone receptors that regulate plant development. Development 133:1857–1869

    Article  PubMed  CAS  Google Scholar 

  • Brogaard K, Xi L, Wang J-P, Widom J (2012) A map of nucleosome positions in yeast at base-pair resolution. Nature 486:496–501

    PubMed  CAS  Google Scholar 

  • Bryant GO, Prabhu V, Floer M, Wang X, Spagna D, Schreiber D, Ptashne M (2008) Activator control of nucleosome occupancy in activation and repression of transcription. PLoS Biol 6:2928–2939

    Article  PubMed  CAS  Google Scholar 

  • Carlberg C, Seuter S (2010) Dynamics of nuclear receptor target gene regulation. Chromosoma 119:479–484

    Article  PubMed  Google Scholar 

  • Chen J, Archer TK (2005) Regulating SWI/SNF subunit levels via protein-protein interactions and proteasomal degradation: BAF155 and BAF170 limit expression of BAF57. Mol Cell Biol 25:9016–9027

    Article  PubMed  CAS  Google Scholar 

  • Cho JN, Ryu JY, Jeong YM, Park J, Song JJ, Amasino RM, Noh B, Noh YS (2012) Control of seed germination by light-induced histone arginine demethylation activity. Dev Cell 22:736–748

    Article  PubMed  CAS  Google Scholar 

  • Chow B, McCourt P (2006) Plant hormone receptors: perception is everything. Genes Dev 20:1998–2008

    Article  PubMed  CAS  Google Scholar 

  • Clapier CR, Cairns BR (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78:273–304

    Article  PubMed  CAS  Google Scholar 

  • Cullen SJ, Ponnappan S, Ponnappan U (2009) Catalytic activity of the proteasome fine-tunes BRG1-mediated chromatin remodeling to regulate the expression of inflammatory genes. Mol Immunol 47:600–605

    Article  PubMed  CAS  Google Scholar 

  • Depuydt S, Hardtke CS (2011) Hormone signaling crosstalk in plant growth regulation. Curr Biol 21:R365–R373

    Article  PubMed  CAS  Google Scholar 

  • Dugardeyn J, Vandenbussche F, Van Der Straeten D (2008) To grow or not to grow: what can we learn on ethylene–gibberellin cross-talk by in silico gene expression analysis? J Exp Bot 59:1–16

    Article  PubMed  CAS  Google Scholar 

  • Euskirchen GM, Auerbach RK, Davidov E, Gianoulis TA, Zhong G, Rozowsky J, Bhardwaj N, Gerstein MB, Snyder M (2011) Diverse roles and interactions of the SWI/SNF chromatin remodeling complex revealed using global approaches. PLoS Genet 7:e1002008

    Article  PubMed  CAS  Google Scholar 

  • Fukazawa J, Nakata M, Ito T, Yamaguchi S, Takahashi Y (2010) The transcription factor RSG regulates negative feedback of NtGA20ox1 encoding GA 20-oxidase. Plant J 62:1035–1045

    PubMed  CAS  Google Scholar 

  • Gallego-Bartolomé J, Minguet EG, Grau-Enguix F, Abbas M, Locascio A et al (2012) Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc Natl Acad Sci USA 109:13446–13451

    Article  PubMed  Google Scholar 

  • Han SK, Sang Y, Rodrigues A, BIOL425 F2010, Wu MF, Rodriguez PL, Wagner D (2012) The SWI2/SNF2 Chromatin Remodeling ATPase BRAHMA Represses Abscisic Acid Responses in the Absence of the Stress Stimulus in Arabidopsis. Plant Cell doi: http://dx.doi.org/10.1105/tpc.112.105114

  • Hargreaves D, Crabtree GR (2011) ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res 21:398–420

    Article  Google Scholar 

  • Hauvermale AL, Ariizumi T, Steber CM (2012) Gibberellin signaling: a theme and variations on DELLA repression. Plant Physiol 160:83–92

    Article  PubMed  CAS  Google Scholar 

  • Hebbar PB, Archer TK (2003) Chromatin remodeling by nuclear receptors. Chromosoma 111:495–504

    Article  PubMed  Google Scholar 

  • Henderson JT, Li HC, Rider SD, Mordhorst AP, Romero-Severson J, Cheng JC, Robey J, Sung ZR, de Vries SC, Ogas J (2004) PICKLE acts throughout the plant to repress expression of embryonic traits and may play a role in gibberellin-dependent responses. Plant Physiol 134:995–1005

    Article  PubMed  CAS  Google Scholar 

  • Hou X, Lee LYC, Xia K, Yen Y, Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19:884–894

    Article  PubMed  CAS  Google Scholar 

  • Hsiao PW, Fryer CJ, Trotter KW, Wang W, Archer TK (2003) BAF60a mediates critical interactions between nuclear receptors and the BRG1 chromatin-remodeling complex for transactivation. Mol Cell Biol 23:6210–6220

    Article  PubMed  CAS  Google Scholar 

  • Hurtado L, Farrona S, Reyes JC (2006) The putative SWI/SNF complex subunit BRAHMA activates flower homeotic genes in Arabidopsis thaliana. Plant Mol Biol 62:291–304

    Article  PubMed  CAS  Google Scholar 

  • Iyer VR (2012) Nucleosome positioning: bringing order to the eukaryotic genome. Trends Cell Biol 22:250–56

    Article  PubMed  CAS  Google Scholar 

  • Jaillais Y, Chory J (2010) Unraveling the paradoxes of plant hormone signaling integration. Nat Struct Mol Biol 17:642–645

    Article  PubMed  CAS  Google Scholar 

  • Jeong H, Mason SP, Barabási AL, Oltvai ZN (2001) Lethality and centrality in protein networks. Nature 411:41–42

    Article  PubMed  CAS  Google Scholar 

  • Jerzmanowski A (2007) SWI/SNF remodeling and linker histones in plants. Biochim Biophys Acta 1769:330–345

    Article  PubMed  CAS  Google Scholar 

  • John S, Sabo PJ, Johnson TA, Sung MH, Biddie SC, Lightman SL, Voss TC, Davis SR, Meltzer PS, Stamatoyannopoulos JA, Hager GL (2008) Interaction of the glucocorticoid receptor with the chromatin landscape. Mol Cell 29:611–624

    Article  PubMed  CAS  Google Scholar 

  • Johnson TA, Elbi C, Parekh BS, Hager GL, John S (2008) Chromatin remodeling complexes interact dynamically with a glucocorticoid receptor-regulated promoter. Mol Biol Cell 19:3308–3322

    Article  PubMed  CAS  Google Scholar 

  • Kafri R, Dahan O, Levy J, Pilpel Y (2008) Preferential protection of protein interaction network hubs in yeast: Evolved functionality of genetic redundancy. Proc Natl Acad Sci USA 105:1243–1248

    Article  PubMed  CAS  Google Scholar 

  • Keppler BR, Archer TK (2010) Ubiquitin-dependent and ubiquitin-independent control of subunit stoichiometry in the SWI/SNF complex. J Biol Chem 285:35665–35674

    Article  PubMed  CAS  Google Scholar 

  • Keppler BR, Archer TK, Kinyamu HK (2011) Emerging roles of the 26S proteasome in nuclear hormone receptor-regulated transcription. Biochim Biophys Acta 1809:109–118

    Article  PubMed  CAS  Google Scholar 

  • Knizewski L, Ginalski K, Jerzmanowski A (2008) Snf2 proteins in plants: gene silencing and beyond. Trends Plant Sci 13:557–565

    Article  PubMed  CAS  Google Scholar 

  • Lehner B, Crombie C, Tischler J, Fortunato A, Fraser AG (2006) Systematic mapping of genetic interactions in Caenorhabditis elegans identifies common modifiers of diverse signaling pathways. Nat Genet 38:896–903

    Article  PubMed  CAS  Google Scholar 

  • Link KA, Burd CJ, William E, Marshall T, Rosson G, Henry E, Weissman B, Knudsen KE (2005) BAF57 governs androgen receptor action and androgen-dependent proliferation through SWI/SNF. Mol Cell Biol 25:2200–2215

    Article  PubMed  CAS  Google Scholar 

  • Maynard-Smith J, Szathmáry E (1995) The major transitions in evolution. Oxford University Press, Oxford

    Google Scholar 

  • Mellor J (2006) Dynamic nucleosomes and gene transcription. Trends Genet 22:320–329

    Article  PubMed  CAS  Google Scholar 

  • Nicolaides NC, Galata Z, Kino T, Chrousos GP, Charmandari E (2010) The human glucocorticoid receptor: molecular basis of biologic function. Steroids 75:1–28

    Article  PubMed  CAS  Google Scholar 

  • Nordstrom A, Tarkowski P, Tarkowska D, Norbaek R, Ã…stot C, Dolezal K, Sandberg G (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin–cytokinin-regulated development. Proc Natl Acad Sci USA 101:8039–8044

    Article  PubMed  Google Scholar 

  • Pham CD, Sims HI, Archer TK, Schnitzler GR (2011) Multiple distinct stimuli increase measured nucleosome occupancy around human promoters. PLoS One 6:e23490

    Article  PubMed  CAS  Google Scholar 

  • Rochette-Egly C (2005) Dynamic combinatorial networks in nuclear receptor-mediated transcription. J Biol Chem 280:32565–32568

    Article  PubMed  CAS  Google Scholar 

  • Rodrigo G, Jaramillo A, Blázquez MA (2011) Integral control of plant gravitropism through the interplay of hormone signaling and gene regulation. Biophys J 17:757–763

    Article  Google Scholar 

  • Saez A, Rodrigues A, Santiago J, Rubio S, Rodriguez PL (2008) HAB-1-SWI3B interaction reveals a link between abscisic acid signaling and putative SWI/SNF chromatin-remodeling complexes in Arabidopsis. Plant Cell 20:2972–2988

    Article  PubMed  CAS  Google Scholar 

  • Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signaling. Nat Rev 459:1071–1078

    CAS  Google Scholar 

  • Sarnowski TJ, Rios G, Jasik J, Swiezewski S, Kaczanowski S, Kwiatkowska A, Pawlikowska K, Kozbial M, Kozbial P, Koncz C, Jerzmanowski A (2005) SWI3 subunits of putative SWI/SNF chromatin remodeling complex play distinct roles during Arabidopsis development. Plant Cell 17:2454–2472

    Article  PubMed  CAS  Google Scholar 

  • Shivaswamy S, Iyer VR (2008) Stress-dependent dynamics of global chromatin remodeling in yeast: dual role for SWI/SNF in the heat shock stress response. Mol Cell Biol 28:2221–2234

    Article  PubMed  CAS  Google Scholar 

  • Sikder D, Johnston SA, Kodadek T (2006) Widespread, but non-identical, association of proteasomal 19 and 20 S proteins with yeast chromatin. J Biol Chem 281:27346–27355

    Article  PubMed  CAS  Google Scholar 

  • Sohn DH, Lee KY, Lee C, Oh J, Chung H, Jeon SH, Seong RH (2007) SRG3 interacts directly with the major components of the SWI/SNF chromatin remodeling complex and protects them from proteasomal degradation. J Biol Chem 282:10614–10624

    Article  PubMed  CAS  Google Scholar 

  • Spartz AK, Gray WM (2008) Plant hormone receptors: new perception. Genes Dev 22:2139–2148

    Article  PubMed  CAS  Google Scholar 

  • Stepanova AN, Yun Y, Likhacheva AV, Alonso JM (2007) Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 19:2169–2185

    Article  PubMed  CAS  Google Scholar 

  • Talbert PB, Henikoff S (2006) Spreading of silent chromatin: inaction at a distance. Nat Rev Genet 7:793–803

    Article  PubMed  CAS  Google Scholar 

  • Tang X, Hou A, Babu M, Nguyen V, Hurtado L, Lu Q, Reyes JC, Wang A, Keller WA, Harada JJ, Tsang EW, Cui Y (2008) The Arabidopsis BRAHMA chromatin-remodeling ATPase is involved in repression of seed maturation genes in leaves. Plant Physiol 147:1143–1157

    Article  PubMed  CAS  Google Scholar 

  • Tolkunov D, Zawadzki KA, Singer C, Elfving N, Morozov AV, Broach JR (2011) Chromatin remodelers clear nucleosomes from intrinsically unfavorable sites to establish nucleosome-depleted regions at promoters. Mol Biol Cell 22:2106–2118

    Article  PubMed  CAS  Google Scholar 

  • Trotter K, Archer TK (2008) The BRG1 transcriptional co-regulator. Nucl Recept Signal 6:e004

    PubMed  Google Scholar 

  • Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:821–839

    Article  Google Scholar 

  • Vert G, Walcher CL, Chory J, Nemhauser JL (2008) Integration of auxin and brassinosteroid pathways by Auxin Response Factor 2. Proc Natl Acad Sci USA 105:9829–9834

    Article  PubMed  CAS  Google Scholar 

  • Walley JW, Rowe HC, Xiao Y, Chehab EW, Kliebenstein DJ, Wagner D, Dehesh K (2008) The chromatin remodeler SPLAYED regulates specific stress signaling pathways. PLoS Pathog 4:e1000237

    Article  PubMed  Google Scholar 

  • Wang D, Xia X, Weiss RE, Refetoff S, Yen PM (2010) Distinct and histone-specific modifications mediate positive versus negative transcriptional regulation of TSH-alpha promoter. PLoS One 5:e9853

    Article  PubMed  Google Scholar 

  • Weiss D, Ori N (2007) Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol 144:1240–1246

    Article  PubMed  CAS  Google Scholar 

  • Williams ME (2011) Introduction to phytohormones. In: Teaching tools in plant biology. Plant Cell. Available via http://www.plantcell.org/cgi/doi/10.1105/tpc.110.tt0310

  • Wu MF, Sang Y, Bezhani S, Yamaguchi N, Han SK, Li Z, Su Y, Slewinski TL, Wagner D (2012) SWI2/SNF2 chromatin remodeling ATPases overcome polycomb repression and control floral organ identity with the LEAFY and SEPALLATA3 transcription factors. Proc Natl Acad Sci USA 109:3576–3581

    Article  PubMed  CAS  Google Scholar 

  • Yu X, Li L, Li L, Guo M, Chory J, Yin Y (2008) Modulation of brassinosteroid-regulated gene expression by Jumonji domain-containing proteins ELF6 and REF6 in Arabidopsis. Proc Natl Acad Sci USA 105:7618–7623

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Ogas J (2009) An epigenetic perspective on developmental regulation of seed genes. Mol Plant 2:610–627

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Rider SD Jr, Henderson JT, Fountain M, Chuang K, Kandachar V, Simons A, Edenberg HJ, Romero-Severson J, Muir WM, Ogas J (2008) The CHD3 remodeler PICKLE promotes trimethylation of histone H3 lysine 27. J Biol Chem 283:22637–22648

    Article  PubMed  CAS  Google Scholar 

  • Zhu YX (2010) The epigenetic involvement in plant hormone signaling. Chin Sci Bull 55:2198–2203

    Article  CAS  Google Scholar 

  • Zotenko E, Mestre J, O’Leary DP, Przytycka TM (2008) Why do hubs in the yeast protein interaction network tend to be essential: reexamining the connection between the network topology and essentiality. PLoS Comput Biol 4:e1000140

    Article  PubMed  Google Scholar 

  • Zraly CB, Middleton FA, Dingwall AK (2006) Hormone-response genes are direct in vivo regulatory targets of Brahma (SWI/SNF) complex function. J Biol Chem 281:35305–35315

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrzej Jerzmanowski .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Jerzmanowski, A., Archacki, R. (2013). Hormonal Signaling in Plants and Animals: An Epigenetics Viewpoint. In: Grafi, G., Ohad, N. (eds) Epigenetic Memory and Control in Plants. Signaling and Communication in Plants, vol 18. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-35227-0_6

Download citation

Publish with us

Policies and ethics