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The converging path of protein SUMOylation in phytohormone signalling: highlights and new frontiers

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Abstract

Key message

The intersection of phytohormone signalling pathways with SUMOylation, a key post-translational modification, offers an additional layer of control to the phytohormone signalling for sophisticated regulation of plant development.

Abstract

Plants live in a constantly changing environment that are often challenging for the growth and development of plants. Phytohormones play a critical role in modulating molecular-level changes for enabling plants to resist climatic aberrations. The orchestration of such effective molecular responses entails rapid regulation of phytohormone signalling at transcriptional, translational and post-translational levels. Post-translational modifications have emerged as a key player in modulating hormonal pathways. The current review lays emphasis on the role of SUMOylation, a key post-translational modification, in manipulating individual hormone signalling pathways for better plant adaptability. Here, we discuss the recent advancement in the field and highlights how SUMO targets key signalling intermediates including transcription factors to provide a quick response to different biotic or abiotic stresses, sometimes even prior to changes in hormone levels. The understanding of the convergence of SUMOylation and hormonal pathways will offer an additional layer of control to the phytohormone signalling for an intricate and sophisticated regulation of plant development and can be utilised as a tool to generate climate-resilient crops.

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References

  • Achard P, Genschik P (2009) Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J Exp Bot 60:1085–1092

    Article  CAS  PubMed  Google Scholar 

  • Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S, Coppens F, Beemster GT, Genschik P (2009) Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr Biol 19:1188–1193

    Article  CAS  PubMed  Google Scholar 

  • An C, Mou Z (2011) Salicylic acid and its function in plant immunity. J Integr Plant Biol 53:412–428

    Article  CAS  PubMed  Google Scholar 

  • Attaran E, He SY (2012) The long-sought-after salicylic acid receptors. Mol Plant 5:971–973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey D, O’Hare P (2004) Characterization of the localization and proteolytic activity of the SUMO-specific protease, SENP1. J Biol Chem 279:692–703

    Article  CAS  PubMed  Google Scholar 

  • Bailey M, Srivastava A, Conti L, Nelis S, Zhang C, Florance H, Love A, Milner J, Napier R, Grant M, Sadanandom A (2016) Stability of small ubiquitin-like modifier (SUMO) proteases OVERLY TOLERANT TO SALT1 and -2 modulates salicylic acid signalling and SUMO1/2 conjugation in Arabidopsis thaliana. J Exp Bot 67:353–363

    Article  CAS  PubMed  Google Scholar 

  • Blanco-Tourinan N, Serrano-Mislata A, Alabadi D (2020) Regulation of DELLA proteins by post-translational modifications. Plant Cell Physiol. https://doi.org/10.1093/pcp/pcaa113

    Article  PubMed  Google Scholar 

  • Briones-Moreno A, Hernandez-Garcia J, Vargas-Chavez C, Romero-Campero FJ, Romero JM, Valverde F, Blazquez MA (2017) Evolutionary analysis of DELLA-associated transcriptional networks. Front Plant Sci 8:626

    Article  PubMed  PubMed Central  Google Scholar 

  • Calderon Villalobos LI, Lee S, De Oliveira C, Ivetac A, Brandt W, Armitage L, Sheard LB, Tan X, Parry G, Mao H, Zheng N, Napier R, Kepinski S, Estelle M (2012) A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin. Nat Chem Biol 8:477–485

    Article  CAS  PubMed  Google Scholar 

  • Campanaro A, Battaglia R, Galbiati M, Sadanandom A, Tonelli C, Conti L (2016) SUMO proteases OTS1 and 2 control filament elongation through a DELLA-dependent mechanism. Plant Reprod 29:287–290

    Article  CAS  PubMed  Google Scholar 

  • Castano-Miquel L, Segui J, Manrique S, Teixeira I, Carretero-Paulet L, Atencio F, Lois LM (2013) Diversification of SUMO-activating enzyme in Arabidopsis: implications in SUMO conjugation. Mol Plant 6:1646–1660

    Article  CAS  PubMed  Google Scholar 

  • Castro PH, Tavares RM, Bejarano ER, Azevedo H (2012) SUMO, a heavyweight player in plant abiotic stress responses. Cell Mol Life Sci 69:3269–3283

    Article  CAS  PubMed  Google Scholar 

  • Castro PH, Couto D, Freitas S, Verde N, Macho AP, Huguet S, Botella MA, Ruiz-Albert J, Tavares RM, Bejarano ER, Azevedo H (2016) SUMO proteases ULP1c and ULP1d are required for development and osmotic stress responses in Arabidopsis thaliana. Plant Mol Biol 92:143–159

    Article  CAS  PubMed  Google Scholar 

  • Castro PH, Santos MA, Freitas S, Cana-Quijada P, Lourenco T, Rodrigues MAA, Fonseca F, Ruiz-Albert J, Azevedo JE, Tavares RM, Castillo AG, Bejarano ER, Azevedo H (2018) Arabidopsis thaliana SPF1 and SPF2 are nuclear-located ULP2-like SUMO proteases that act downstream of SIZ1 in plant development. J Exp Bot 69:4633–4649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Catala R, Ouyang J, Abreu IA, Hu Y, Seo H, Zhang X, Chua NH (2007) The Arabidopsis E3 SUMO ligase SIZ1 regulates plant growth and drought responses. Plant Cell 19:2952–2966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43:265–285

    Article  CAS  PubMed  Google Scholar 

  • Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671

    Article  CAS  PubMed  Google Scholar 

  • Chung CD, Liao J, Liu B, Rao X, Jay P, Berta P, Shuai K (1997) Specific inhibition of Stat3 signal transduction by PIAS3. Science 278:1803–1805

    Article  CAS  PubMed  Google Scholar 

  • Coleman D, Kawamura A, Ikeuchi M, Favero DS, Lambolez A, Rymen B, Iwase A, Suzuki T, Sugimoto K (2020) The SUMO E3 ligase SIZ1 negatively regulates shoot regeneration. Plant Physiol 184:330–344

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conti L, Price G, O’Donnell E, Schwessinger B, Dominy P, Sadanandom A (2008) Small ubiquitin-like modifier proteases OVERLY TOLERANT TO SALT1 and -2 regulate salt stress responses in Arabidopsis. Plant Cell 20:2894–2908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conti L, Nelis S, Zhang C, Woodcock A, Swarup R, Galbiati M, Tonelli C, Napier R, Hedden P, Bennett M, Sadanandom A (2014) Small ubiquitin-like modifier protein SUMO enables plants to control growth independently of the phytohormone gibberellin. Dev Cell 28:102–110

    Article  CAS  PubMed  Google Scholar 

  • Dai B, Rasmussen TP (2007) Global epiproteomic signatures distinguish embryonic stem cells from differentiated cells. Stem Cells 25:2567–2574

    Article  CAS  PubMed  Google Scholar 

  • Dai C, Xue HW (2010) Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. EMBO J 29:1916–1927

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Zelicourt A, Colcombet J, Hirt H (2016) The role of MAPK modules and ABA during abiotic stress signaling. Trends Plant Sci 21:677–685

    Article  PubMed  CAS  Google Scholar 

  • Dempsey DA, Klessig DF (2012) SOS—too many signals for systemic acquired resistance? Trends Plant Sci 17:538–545

    Article  CAS  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005a) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  CAS  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jurgens G, Estelle M (2005b) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119

    Article  CAS  PubMed  Google Scholar 

  • Dong X (2004) NPR1, all things considered. Curr Opin Plant Biol 7:547–552

    Article  CAS  PubMed  Google Scholar 

  • Elrouby N (2015) Analysis of small ubiquitin-like modifier (SUMO) targets reflects the essential nature of protein SUMOylation and provides insight to elucidate the role of SUMO in plant development. Plant Physiol 169:1006–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elrouby N, Coupland G (2010) Proteome-wide screens for small ubiquitin-like modifier (SUMO) substrates identify Arabidopsis proteins implicated in diverse biological processes. Proc Natl Acad Sci U S A 107:17415–17420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • FAO (2017) The future of food and agriculture—trends and challenges. FAO, Rome

    Google Scholar 

  • Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Chen L, Yu L, Iglesias-Pedraz JM, Kircher S, Schafer E, Fu X, Fan LM, Deng XW (2008) Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451:475–479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • French M, Swanson K, Shih SC, Radhakrishnan I, Hicke L (2005) Identification and characterization of modular domains that bind ubiquitin. Methods Enzymol 399:135–157

    Article  CAS  PubMed  Google Scholar 

  • Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annu Rev Plant Biol 64:839–863

    Article  CAS  PubMed  Google Scholar 

  • Fu X, Richards DE, Ait-Ali T, Hynes LW, Ougham H, Peng J, Harberd NP (2002) Gibberellin-mediated proteasome-dependent degradation of the barley DELLA protein SLN1 repressor. Plant Cell 14:3191–3200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu X, Richards DE, Fleck B, Xie D, Burton N, Harberd NP (2004) The Arabidopsis mutant sleepy1gar2-1 protein promotes plant growth by increasing the affinity of the SCFSLY1 E3 ubiquitin ligase for DELLA protein substrates. Plant Cell 16:1406–1418

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garrido E, Srivastava AK, Sadanandom A (2018) Exploiting protein modification systems to boost crop productivity: SUMO proteases in focus. J Exp Bot 69:4625–4632

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goncalves NM, Fernandes T, Nunes C, Rosa MTG, Matiolli CC, Rodrigues MAA, Oliveira MM, Abreu IA (2020) SUMOylation of rice DELLA SLR1 modulates transcriptional responses and improves yield under salts stress. Biorxiv. https://doi.org/10.1101/2020.03.10.986224

    Article  PubMed  PubMed Central  Google Scholar 

  • Gray WM (2004) Hormonal regulation of plant growth and development. PLoS Biol 2:E311

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guo R, Sun W (2017) Sumoylation stabilizes RACK1B and enhance its interaction with RAP2.6 in the abscisic acid response. Sci Rep 7:44090

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanania U, Furman-Matarasso N, Ron M, Avni A (1999) Isolation of a novel SUMO protein from tomato that suppresses EIX-induced cell death. Plant J 19:533–541

    Article  CAS  PubMed  Google Scholar 

  • Hashiguchi A, Komatsu S (2016) Impact of post-translational modifications of crop proteins under abiotic stress. Proteomes 4:42

    Article  PubMed Central  CAS  Google Scholar 

  • He JX, Gendron JM, Yang Y, Li J, Wang ZY (2002) The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc Natl Acad Sci U S A 99:10185–10190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hecker CM, Rabiller M, Haglund K, Bayer P, Dikic I (2006) Specification of SUMO1- and SUMO2-interacting motifs. J Biol Chem 281:16117–16127

    Article  CAS  PubMed  Google Scholar 

  • Hermkes R, Fu YF, Nurrenberg K, Budhiraja R, Schmelzer E, Elrouby N, Dohmen RJ, Bachmair A, Coupland G (2011) Distinct roles for Arabidopsis SUMO protease ESD4 and its closest homolog ELS1. Planta 233:63–73

    Article  CAS  PubMed  Google Scholar 

  • Hernandez-Garcia J, Briones-Moreno A, Blazquez MA (2020) Origin and evolution of gibberellin signaling and metabolism in plants. Semin Cell Dev Biol. https://doi.org/10.1016/j.semcdb.2020.04.009

    Article  PubMed  Google Scholar 

  • Hicke L, Schubert HL, Hill CP (2005) Ubiquitin-binding domains. Nat Rev Mol Cell Biol 6:610–621

    Article  CAS  PubMed  Google Scholar 

  • Higuchi M, Pischke MS, Mahonen AP, Miyawaki K, Hashimoto Y, Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S, Helariutta Y, Sussman MR, Kakimoto T (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci U S A 101:8821–8826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ho CW, Chen HT, Hwang J (2011) UBC9 autosumoylation negatively regulates sumoylation of septins in Saccharomyces cerevisiae. J Biol Chem 286:21826–21834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    Article  CAS  PubMed  Google Scholar 

  • Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, Kato T, Tabata S, Shinozaki K, Kakimoto T (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409:1060–1063

    Article  CAS  PubMed  Google Scholar 

  • Itoh H, Ueguchi-Tanaka M, Sato Y, Ashikari M, Matsuoka M (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14:57–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson ES, Gupta AA (2001) An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106:735–744

    Article  CAS  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Keating BA, Carberry PS (2010) Sustainable production food security and supply chain implications. Asp Appl Biol 102:7–20

    Google Scholar 

  • Kepinski S, Leyser O (2005a) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  CAS  PubMed  Google Scholar 

  • Kepinski S, Leyser O (2005b) Plant development: auxin in loops. Curr Biol 15:R208-210

    Article  CAS  PubMed  Google Scholar 

  • Kerscher O (2007) SUMO junction-what’s your function? New insights through SUMO-interacting motifs. EMBO Rep 8:550–555

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan M, Rozhon W, Unterholzner SJ, Chen T, Eremina M, Wurzinger B, Bachmair A, Teige M, Sieberer T, Isono E, Poppenberger B (2014) Interplay between phosphorylation and SUMOylation events determines CESTA protein fate in brassinosteroid signalling. Nat Commun 5:4687

    Article  CAS  PubMed  Google Scholar 

  • Kim SI, Park BS, Kim DY, Yeu SY, Song SI, Song JT, Seo HS (2015) E3 SUMO ligase AtSIZ1 positively regulates SLY1-mediated GA signalling and plant development. Biochem J 469:299–314

    Article  CAS  PubMed  Google Scholar 

  • King KE, Moritz T, Harberd NP (2001) Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159:767–776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klessig DF, Choi HW, Dempsey DA (2018) Systemic acquired resistance and salicylic acid: past, present, and future. Mol Plant Microbe Interact 31:871–888

    Article  CAS  PubMed  Google Scholar 

  • Knipscheer P, Flotho A, Klug H, Olsen JV, van Dijk WJ, Fish A, Johnson ES, Mann M, Sixma TK, Pichler A (2008) Ubc9 sumoylation regulates SUMO target discrimination. Mol Cell 31:371–382

    Article  CAS  PubMed  Google Scholar 

  • Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Sung DY, Vierstra RD (2003) The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and -2 conjugates is increased by stress. J Biol Chem 278:6862–6872

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC, Kim D, Lee SY, Salt DE, Mengiste T, Gong Q, Ma S, Bohnert HJ, Kwak SS, Bressan RA, Hasegawa PM, Yun DJ (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79–90

    Article  CAS  PubMed  Google Scholar 

  • Leyser O (2006) Dynamic integration of auxin transport and signalling. Curr Biol 16:R424-433

    Article  CAS  PubMed  Google Scholar 

  • Li SJ, Hochstrasser M (1999) A new protease required for cell-cycle progression in yeast. Nature 398:246–251

    Article  CAS  PubMed  Google Scholar 

  • Li SJ, Hochstrasser M (2000) The yeast ULP2 (SMT4) gene encodes a novel protease specific for the ubiquitin-like Smt3 protein. Mol Cell Biol 20:2367–2377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu B, Liao J, Rao X, Kushner SA, Chung CD, Chang DD, Shuai K (1998) Inhibition of Stat1-mediated gene activation by PIAS1. Proc Natl Acad Sci U S A 95:10626–10631

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu G, Holub EB, Alonso JM, Ecker JR, Fobert PR (2005) An Arabidopsis NPR1-like gene, NPR4, is required for disease resistance. Plant J 41:304–318

    Article  CAS  PubMed  Google Scholar 

  • Lofke C, Luschnig C, Kleine-Vehn J (2013) Posttranslational modification and trafficking of PIN auxin efflux carriers. Mech Dev 130:82–94

    Article  PubMed  CAS  Google Scholar 

  • Lois LM, Lima CD (2005) Structures of the SUMO E1 provide mechanistic insights into SUMO activation and E2 recruitment to E1. EMBO J 24:439–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lois LM, Lima CD, Chua NH (2003) Small ubiquitin-like modifier modulates abscisic acid signaling in Arabidopsis. Plant Cell 15:1347–1359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lothrop AP, Torres MP, Fuchs SM (2013) Deciphering post-translational modification codes. FEBS Lett 587:1247–1257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068

    Article  CAS  PubMed  Google Scholar 

  • Malamy J, Carr JP, Klessig DF, Raskin I (1990) Salicylic Acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002–1004

    Article  CAS  PubMed  Google Scholar 

  • Mann M, Jensen ON (2003) Proteomic analysis of post-translational modifications. Nat Biotechnol 21:255–261

    Article  CAS  PubMed  Google Scholar 

  • Miller WA, Dinesh-Kumar SP (2019) A new mechanism for translational control in plants. FEBS J 286:3775–3777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miller MJ, Barrett-Wilt GA, Hua Z, Vierstra RD (2010) Proteomic analyses identify a diverse array of nuclear processes affected by small ubiquitin-like modifier conjugation in Arabidopsis. Proc Natl Acad Sci U S A 107:16512–16517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miura K, Hasegawa PM (2009) Sumoylation and abscisic acid signaling. Plant Signal Behav 4:1176–1178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miura K, Lee J, Jin JB, Yoo CY, Miura T, Hasegawa PM (2009) Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proc Natl Acad Sci U S A 106:5418–5423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miura K, Lee J, Gong Q, Ma S, Jin JB, Yoo CY, Miura T, Sato A, Bohnert HJ, Hasegawa PM (2011) SIZ1 regulation of phosphate starvation-induced root architecture remodeling involves the control of auxin accumulation. Plant Physiol 155:1000–1012

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Okamoto H, Okuma E, Shiba H, Kamada H, Hasegawa PM, Murata Y (2013) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. Plant J 73:91–104

    Article  CAS  PubMed  Google Scholar 

  • Morrell R, Sadanandom A (2019) Dealing with stress: a review of plant SUMO proteases. Front Plant Sci 10:1122

    Article  PubMed  PubMed Central  Google Scholar 

  • Mukhopadhyay D, Dasso M (2007) Modification in reverse: the SUMO proteases. Trends Biochem Sci 32:286–295

    Article  CAS  PubMed  Google Scholar 

  • Mukhtar MS, Nishimura MT, Dangl J (2009) NPR1 in plant defense: it’s not over ’til it’s turned over. Cell 137:804–806

    Article  CAS  PubMed  Google Scholar 

  • Murtas G, Reeves PH, Fu YF, Bancroft I, Dean C, Coupland G (2003) A nuclear protease required for flowering-time regulation in Arabidopsis reduces the abundance of SMALL UBIQUITIN-RELATED MODIFIER conjugates. Plant Cell 15:2308–2319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nam KH, Li J (2002) BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling. Cell 110:203–212

    Article  CAS  PubMed  Google Scholar 

  • Nemhauser JL, Mockler TC, Chory J (2004) Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biol 2:E258

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16:1365–1377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu LXL, Kong X, Qu GP, Cai B, Lee J, Jin JB (2019) SIZ1-mediated SUMOylation of TPR1 suppresses plant immunity in Arabidopsis. Mol Plant 12:215–228

    Article  CAS  PubMed  Google Scholar 

  • Novatchkova M, Tomanov K, Hofmann K, Stuible HP, Bachmair A (2012) Update on sumoylation: defining core components of the plant SUMO conjugation system by phylogenetic comparison. New Phytol 195:23–31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olsen SK, Capili AD, Lu X, Tan DS, Lima CD (2010) Active site remodelling accompanies thioester bond formation in the SUMO E1. Nature 463:906–912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orosa B, Yates G, Verma V, Srivastava AK, Srivastava M, Campanaro A, De Vega D, Fernandes A, Zhang C, Lee J, Bennett MJ, Sadanandom A (2018) SUMO conjugation to the pattern recognition receptor FLS2 triggers intracellular signalling in plant innate immunity. Nat Commun 9:5185

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Orosa-Puente B, Leftley N, von Wangenheim D, Banda J, Srivastava AK, Hill K, Truskina J, Bhosale R, Morris E, Srivastava M, Kumpers B, Goh T, Fukaki H, Vermeer JEM, Vernoux T, Dinneny JR, French AP, Bishopp A, Sadanandom A, Bennett MJ (2018) Root branching toward water involves posttranslational modification of transcription factor ARF7. Science 362:1407–1410

    Article  CAS  PubMed  Google Scholar 

  • Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295

    Article  CAS  PubMed  Google Scholar 

  • Peng P, Yan Z, Zhu Y, Li J (2008) Regulation of the Arabidopsis GSK3-like kinase BRASSINOSTEROID-INSENSITIVE 2 through proteasome-mediated protein degradation. Mol Plant 1:338–346

    Article  CAS  PubMed  Google Scholar 

  • Pichler A, Fatouros C, Lee H, Eisenhardt N (2017) SUMO conjugation—a mechanistic view. Biomol Concepts 8:13–36

    Article  CAS  PubMed  Google Scholar 

  • Qin Q, Wang W, Guo X, Yue J, Huang Y, Xu X, Li J, Hou S (2014) Arabidopsis DELLA protein degradation is controlled by a type-one protein phosphatase, TOPP4. PLoS Genet 10:e1004464

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Reed JM, Dervinis C, Morse AM, Davis JM (2010) The SUMO conjugation pathway in Populus: genomic analysis, tissue-specific and inducible SUMOylation and in vitro de-SUMOylation. Planta 232:51–59

    Article  CAS  PubMed  Google Scholar 

  • Reeves PH, Murtas G, Dash S, Coupland G (2002) early in short days 4, a mutation in Arabidopsis that causes early flowering and reduces the mRNA abundance of the floral repressor FLC. Development 129:5349–5361

    Article  CAS  PubMed  Google Scholar 

  • Russinova E, Borst JW, Kwaaitaal M, Cano-Delgado A, Yin Y, Chory J, de Vries SC (2004) Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16:3216–3229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sadanandom A, Bailey M, Ewan R, Lee J, Nelis S (2012) The ubiquitin-proteasome system: central modifier of plant signalling. New Phytol 196:13–28

    Article  CAS  PubMed  Google Scholar 

  • Saleh A, Withers J, Mohan R, Marques J, Gu Y, Yan S, Zavaliev R, Nomoto M, Tada Y, Dong X (2015) Posttranslational modifications of the master transcriptional regulator NPR1 enable dynamic but tight control of plant immune responses. Cell Host Microbe 18:169–182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saracco SA, Miller MJ, Kurepa J, Vierstra RD (2007) Genetic analysis of SUMOylation in Arabidopsis: conjugation of SUMO1 and SUMO2 to nuclear proteins is essential. Plant Physiol 145:119–134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasaki A, Itoh H, Gomi K, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Jeong DH, An G, Kitano H, Ashikari M, Matsuoka M (2003) Accumulation of phosphorylated repressor for gibberellin signaling in an F-box mutant. Science 299:1896–1898

    Article  CAS  PubMed  Google Scholar 

  • Schulz S, Chachami G, Kozaczkiewicz L, Winter U, Stankovic-Valentin N, Haas P, Hofmann K, Urlaub H, Ovaa H, Wittbrodt J, Meulmeester E, Melchior F (2012) Ubiquitin-specific protease-like 1 (USPL1) is a SUMO isopeptidase with essential, non-catalytic functions. EMBO Rep 13:930–938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo J, Lee KJ (2004) Post-translational modifications and their biological functions: proteomic analysis and systematic approaches. J Biochem Mol Biol 37:35–44

    CAS  PubMed  Google Scholar 

  • Silverstone AL, Jung HS, Dill A, Kawaide H, Kamiya Y, Sun TP (2001) Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13:1555–1566

    CAS  PubMed  PubMed Central  Google Scholar 

  • Song J, Durrin LK, Wilkinson TA, Krontiris TG, Chen Y (2004) Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc Natl Acad Sci U S A 101:14373–14378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song J, Zhang Z, Hu W, Chen Y (2005) Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif: a reversal of the bound orientation. J Biol Chem 280:40122–40129

    Article  CAS  PubMed  Google Scholar 

  • Srivastava M, Sadanandom A (2020) An insight into the factors influencing specificity of the SUMO system in plants. Plants 9:1788

    Article  CAS  PubMed Central  Google Scholar 

  • Srivastava AK, Zhang C, Sadanandom A (2016a) Rice OVERLY TOLERANT TO SALT 1 (OTS1) SUMO protease is a positive regulator of seed germination and root development. Plant Signal Behav 11:e1173301

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Srivastava AK, Zhang C, Yates G, Bailey M, Brown A, Sadanandom A (2016b) SUMO is a critical regulator of salt stress responses in rice. Plant Physiol 170:2378–2391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava AK, Zhang C, Caine RS, Gray J, Sadanandom A (2017) Rice SUMO protease overly tolerant to salt 1 targets the transcription factor, OsbZIP23 to promote drought tolerance in rice. Plant J 92:1031–1043

    Article  CAS  PubMed  Google Scholar 

  • Srivastava AK, Orosa B, Singh P, Cummins I, Walsh C, Zhang C, Grant M, Roberts MR, Anand GS, Fitches E, Sadanandom A (2018) SUMO suppresses the activity of the jasmonic acid receptor CORONATINE INSENSITIVE1. Plant Cell 30:2099–2115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava M, Sadanandom A, Srivastava AK (2020a) Towards understanding the multifaceted role of SUMOylation in plant growth and development. Physiol Plant. https://doi.org/10.1111/ppl.13204

    Article  PubMed  Google Scholar 

  • Srivastava M, Srivastava AK, Orosa-Puente B, Campanaro A, Zhang C, Sadanandom A (2020b) SUMO conjugation to BZR1 enables brassinosteroid signaling to integrate environmental cues to shape plant growth. Curr Biol 30:1410-1423.e1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Oh E, Patil S, Kim TW, Ji H, Wong WH, Rhee SY, Wang ZY (2010) Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Dev Cell 19:765–777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448:661–665

    Article  CAS  PubMed  Google Scholar 

  • Tomanov K, Zeschmann A, Hermkes R, Eifler K, Ziba I, Grieco M, Novatchkova M, Hofmann K, Hesse H, Bachmair A (2014) Arabidopsis PIAL1 and 2 promote SUMO chain formation as E4-type SUMO ligases and are involved in stress responses and sulfur metabolism. Plant Cell 26:4547–4560

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ubeda-Tomas S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster GT, Hedden P, Bhalerao R, Bennett MJ (2008) Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat Cell Biol 10:625–628

    Article  CAS  PubMed  Google Scholar 

  • van den Burg HA, Kini RK, Schuurink RC, Takken FL (2010) Arabidopsis small ubiquitin-like modifier paralogs have distinct functions in development and defense. Plant Cell 22:1998–2016

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Verma V, Croley F, Sadanandom A (2018) Fifty shades of SUMO: its role in immunity and at the fulcrum of the growth-defence balance. Mol Plant Pathol 19:1537–1544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verma V, Srivastava AK, Gough C, Campanaro A, Srivastava M, Morrell R, Joyce J, Bailey M, Zhang C, Krysan PJ, Sadanandom A (2021) SUMO enables substrate selectivity by mitogen-activated protein kinases to regulate immunity in plants. Proc Natl Acad Sci U S A 118:e2021351118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogt B, Hofmann K (2012) Bioinformatical detection of recognition factors for ubiquitin and SUMO. Methods Mol Biol 832:249–261

    Article  CAS  PubMed  Google Scholar 

  • Voss U, Bishopp A, Farcot E, Bennett MJ (2014) Modelling hormonal response and development. Trends Plant Sci 19:311–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Weits DA, Giuntoli B, Kosmacz M, Parlanti S, Hubberten HM, Riegler H, Hoefgen R, Perata P, van Dongen JT, Licausi F (2014) Plant cysteine oxidases control the oxygen-dependent branch of the N-end-rule pathway. Nat Commun 5:3425

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson KA, Henley JM (2010) Mechanisms, regulation and consequences of protein SUMOylation. Biochem J 428:133–145

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Despres C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep 1:639–647

    Article  CAS  PubMed  Google Scholar 

  • Xie DX, Feys BF, James S, Nieto-Rostro M, Turner JG (1998) COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280:1091–1094

    Article  CAS  PubMed  Google Scholar 

  • Yates G, Srivastava AK, Sadanandom A (2016) SUMO proteases: uncovering the roles of deSUMOylation in plants. J Exp Bot 67:2541–2548

    Article  CAS  PubMed  Google Scholar 

  • Yin Y, Wang ZY, 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 

  • Yunus AA, Lima CD (2006) Lysine activation and functional analysis of E2-mediated conjugation in the SUMO pathway. Nat Struct Mol Biol 13:491–499

    Article  CAS  PubMed  Google Scholar 

  • Zentella R, Hu J, Hsieh WP, Matsumoto PA, Dawdy A, Barnhill B, Oldenhof H, Hartweck LM, Maitra S, Thomas SG, Cockrell S, Boyce M, Shabanowitz J, Hunt DF, Olszewski NE, Sun TP (2016) O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis. Genes Dev 30:164–176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Cheng YT, Qu N, Zhao Q, Bi D, Li X (2006) Negative regulation of defense responses in Arabidopsis by two NPR1 paralogs. Plant J 48:647–656

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Han Q, Xiong J, Zheng T, Han J, Zhou H, Lin H, Yin Y, Zhang D (2019) Sumoylation of BRI1-EMS-SUPPRESSOR 1 (BES1) by the SUMO E3 Ligase SIZ1 negatively regulates brassinosteroids signaling in Arabidopsis thaliana. Plant Cell Physiol 60:2282–2292

    Article  CAS  PubMed  Google Scholar 

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Funding

This review is partly supported by the DBT-Ramalingaswami Re-entry Fellowship grants received by VV and AS.

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Authors and Affiliations

  1. Department of Biosciences, Durham University, Durham, DH1 3LE, UK

    Moumita Srivastava

  2. Department of Biotechnology, School of Life Sciences, Central University of Rajasthan, Ajmer, Rajasthan, 305817, India

    Vivek Verma

  3. National Agri-Food Biotechnology Institute (NABI), Sector-81 (Knowledge City), S.A.S. Nagar, Mohali, Punjab, 140306, India

    Anjil Kumar Srivastava

Authors
  1. Moumita Srivastava
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  2. Vivek Verma
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  3. Anjil Kumar Srivastava
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MS, VV and AKS conceptualized and wrote the manuscript. All the authors edited and approved the manuscript.

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Correspondence to Vivek Verma or Anjil Kumar Srivastava.

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Communicated by Aryadeep Roychoudhury.

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Srivastava, M., Verma, V. & Srivastava, A.K. The converging path of protein SUMOylation in phytohormone signalling: highlights and new frontiers. Plant Cell Rep 40, 2047–2061 (2021). https://doi.org/10.1007/s00299-021-02732-2

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