Skip to main content
SpringerLink
Log in

SUMO proteins grapple with biotic and abiotic stresses in Arabidopsis

  • Review Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

The small ubiquitin-like modifier, i.e., SUMO, utilizes conjugation and deconjugation mechanisms that are similar to those for ubiquitination. In plants, this modifier modulates important biological processes, including growth, development, and flowering. Sumoylation has a crucial role in responses to abiotic stresses, e.g., phosphate deficiency, heat or low temperature, and drought, as well as in defenses against biotic stresses such as pathogen infection. Our review focuses on the current state of knowledge about SUMO and the functions of sumoylation related to stress responses in Arabidopsis thaliana.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alfano JR, Collmer A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42:385–414

    Article  PubMed  CAS  Google Scholar 

  • Bari R, Datt Pant B, Stitt M, Scheible W-R (2006) PHO2, MicroRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999

    Article  PubMed  CAS  Google Scholar 

  • Bartetzko V, Sonnewald S, Vogel F, Hartner K, Stadler R, Hammes U, Börnke F (2009) The Xanthomonas campestris pv. vesicatoria Type III effector protein XopJ inhibits protein secretion: evidence for interference with cell wall-associated defense responses. Mol Plant-Microbe Interact 22:655–664

    Article  PubMed  CAS  Google Scholar 

  • Bayer P, Arndt A, Metzger S, Mahajan R, Melchior F, Jaenicke R, Becker J (1998) Structure determination of the small ubiquitin-related modifier SUMO-1. J Mol Biol 280:275–286

    Article  PubMed  CAS  Google Scholar 

  • Block A, Li G, Fu ZQ, Alfano JR (2008) Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol 11:396–403

    Article  PubMed  CAS  Google Scholar 

  • Bonshtien A, Lev A, Gibly A, Debbie P, Avni A, Sessa G (2005) Molecular properties of the Xanthomonas AvrRxv effector and global transcriptional changes determined by its expression in resistant tomato plants. Mol Plant-Microbe Interact 18:300–310

    Article  PubMed  CAS  Google Scholar 

  • Brown MT, Goetsch L, Hartwell LH (1993) MIF2 is required for mitotic spindle integrity during anaphase spindle elongation in Saccharomyces cerevisiae. J Cell Biol 123:387–403

    Article  PubMed  CAS  Google Scholar 

  • Canonne J, Marino D, Noël LD, Arechaga I, Pichereaux C, Rossignol M, Roby D, Rivas S (2010) Detection and functional characterization of a 215 amino acid N-terminal extension in the Xanthomonas Type III effector XopD. PLoS One 5:e15773

    Article  PubMed  CAS  Google Scholar 

  • Canonne J, Marino D, Jauneau A, Pouzet C, Brière C, Roby D, Rivas S (2011) The Xanthomonas Type III effector XopD targets the Arabidopsis transcription factor MYB30 to suppress plant defense. Plant Cell 23:3498–3511

    Article  PubMed  CAS  Google Scholar 

  • Castillo AG, Kong LJ, Hanley-Bowdoin L, Bejarano ER (2004) Interaction between a Geminivirus replication protein and the plant sumoylation system. J Virol 78:1758–1769

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chaikam V, Karlson DT (2010) Response and transcriptional regulation of rice sumoylation system during development and stress conditions. BMB Rep 43:103–109

    Article  PubMed  CAS  Google Scholar 

  • Chen C-C, Chen Y-Y, Tang I-C, Liang H-M, Lai C-C, Chiou J-M, Yeh K-C (2011) Arabidopsis SUMO E3 ligase SIZ1 is involved in excess copper tolerance. Plant Physiol 156:2225–2234

    Article  PubMed  CAS  Google Scholar 

  • Cheong MS, Park HC, Hong MJ, Lee J, Choi W, Jin JB, Bohnert HJ, Lee SY, Bressan RA, Yun D-J (2009) Specific domain structures control abscisic acid-, salicylic acid-, and stress-mediated SIZ1 phenotypes. Plant Physiol 151:1930–1942

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Zhu J, Zhu J-K (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451

    Article  PubMed  CAS  Google Scholar 

  • Chosed R, Tomchick DR, Brautigam CA, Mukherjee S, Negi VS, Machius M, Orth K (2007) Structural analysis of Xanthomonas XopD provides insights into substrate specificity of ubiquitinlike protein proteases. J Biol Chem 282:6773–6782

    Article  PubMed  CAS  Google Scholar 

  • Cohen-Peer R, Schuster S, Meiri D, Breiman A, Avni A (2010) Sumoylation of Arabidopsis heat shock factor A2 (HsfA2) modifies its activity during acquired thermotholerance. Plant Mol Biol 74:33–45

    Article  PubMed  CAS  Google Scholar 

  • Colby T, Matthäi A, Boeckelmann, Stuible H-P (2006) SUMOconjugating and SUMO-deconjugating enzymes from Arabidopsis. Plant Physiol 142:318–332

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Duan K, Yi K, Dang L, Huang H, Wu W, Wu P (2008) Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. Plant J 54:965–975

    Article  PubMed  CAS  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 USA 107:17415–17420

    Article  PubMed  CAS  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371

    Article  PubMed  CAS  Google Scholar 

  • Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Dominguez M, March-Diaz R, Reyes JC (2008) The PHD domain of plant PIAS proteins mediates sumoylation of bromodomain GTE proteins. J Biol Chem 283:21469–21477

    Article  PubMed  CAS  Google Scholar 

  • Hay RT (2005) Sumo: a history of modification. Mol Cell 18:1–12

    Article  PubMed  CAS  Google Scholar 

  • Hermkes R, Fu Y-F, Nürrenberg 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  PubMed  CAS  Google Scholar 

  • Hotson A, Mudgett MB (2004) Cysteine proteases in phytopathogenic bacteria: identification of plant targets and activation of innate immunity. Curr Opin Plant Biol 7:384–390

    Article  PubMed  CAS  Google Scholar 

  • Hotson A, Chosed R, Shu H, Orth K, Mudgett MB (2003) Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Mol Microbiol 50:377–389

    Article  PubMed  CAS  Google Scholar 

  • Huang L, Yang S, Zhang S, Liu M, Lai J, Qi Y, Shi S, Wang J, Wang Y, Xie Q, Yang C (2009) The Arabidopsis SUMO E3 ligase AtMMS21, a homologue of NSE2/MMS21, regulates cell proliferation in the root. Plant J 60:666–678

    Article  PubMed  CAS  Google Scholar 

  • Ishida T, Fujiwara S, Miura K, Stacey N, Yoshimura M, Schneider K, Adachi S, Minamisawa K, Umeda M, Sugimoto K (2009) SUMO E3 ligase HIGH PLOIDY2 regulates endocycle onset and meristem maintenance in Arabidopsis. Plant Cell 21:2284–2297

    Article  PubMed  CAS  Google Scholar 

  • Ishida T, Yoshimura M, Miura K, Sugimoto K (2012) MMS21/HPY2 and SIZ1, two Arabidopsis SUMO E3 ligases, have distinct functions in development. PLOS One 7:e46897

    Article  PubMed  CAS  Google Scholar 

  • Johnson ES (2004) Protein modification by SUMO. Annu Rev Biochem 73:355–382

    Article  PubMed  CAS  Google Scholar 

  • Kim J-G, Taylor KW, Hotson A, Keegan M, Schmelz EA, Mudgett MB (2008a) XopD SUMO protease affects host transcription, promotes pathogen growth, and delays symptom development in Xanthomonas-infected tomato leaves. Plant Cell 20:1915–1929

    Article  PubMed  CAS  Google Scholar 

  • Kim K-C, Lai Z, Fan B, Chen Z (2008b) Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 20:2357–2371

    Article  PubMed  CAS  Google Scholar 

  • Kim MG (2010) Alerted defense system attenuates hypersensitive response-associated cell death in Arabidopsis siz1 mutant. J Plant Biol 53:70–78

    Article  CAS  Google Scholar 

  • Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Sung D-Y, Vierstra RD (2003) The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis: accumulation of SUMO 1 and 2 conjugates is increased by stress. J Biol Chem 278:6862–6872

    Article  PubMed  CAS  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 S-S, Bressan RA, Hasegawa PM, Yun D-J (2006) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79–90

    Article  PubMed  Google Scholar 

  • Lois LM (2010) Diversity of the sumoylation machinery in plants. Biochem Soc Trans 38:60–64

    Article  PubMed  CAS  Google Scholar 

  • Meluh PB, Koshland D (1995) Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C. Mol Biol Cell 6:793–807

    PubMed  CAS  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 USA 107:16512–16517

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Hasegawa PM (2010) Sumoylation and other ubiquitin-like post-translational modifications in plants. Trends Cell Biol 20:223–232

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, Baek D, Koo YD, Jin JB, Bressan RA, Yun D-J, Hasegawa PM (2005) The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci USA 102:7760–7765

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Jin JB, Hasegawa PM (2007a) Sumoylation, a posttranslational regulatory process in plants. Curr Opin Plant Biol 10:495–502

    Article  PubMed  CAS  Google Scholar 

  • Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Ashworth EN, Bressan RA, Hasegawa PM (2007b) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19:1403–1414

    Article  PubMed  CAS  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 USA 106:5418–5423

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Mossessova E, Lima CD (2000) Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol Cell 5:865–876

    Article  PubMed  CAS  Google Scholar 

  • Mudgett MB (2005) New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu Rev Plant Biol 56:509–531

    Article  PubMed  CAS  Google Scholar 

  • Mukherjee S, Keitany G, Li Y, Wang Y, Ball HL, Goldsmith EJ, Orth K (2006) Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312:1211–1214

    Article  PubMed  CAS  Google Scholar 

  • Mukherjee S, Hao Y-H, Orth K (2007) A newly discovered posttranslational modification — The acetylation of serine and threonine residues. Trends Biochem Sci 32:210–216

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Okada S, Nagabuchi M, Takamura Y, Nakagawa T, Shinmyozu K, Nakayama J, Tanaka K (2009) Reconstitution of Arabidopsis thaliana SUMO pathways in E. coli: functional evaluation of SUMO machinery proteins and mapping of sumoylation sites by mass spectrometry. Plant Cell Physiol 50:1049–1061

    Article  PubMed  CAS  Google Scholar 

  • Orth K (2002) Function of the Yersinia effector YopJ. Curr Opin Microbiol 5:38–43

    Article  PubMed  CAS  Google Scholar 

  • Orth K, Xu Z, Mudgett MB, Bao ZQ, Palmer LE, Bliska JB, Mangel WF, Staskawicz B, Dixon JE (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290:1594–1597

    Article  PubMed  CAS  Google Scholar 

  • Park HC, Kim H, Koo SC, Park HJ, Cheong MS, Hong H, Baek D, Chung WS, Kim DH, Bressan RA, Lee SY, Bohnert HJ, Yun DJ (2010) Functional characterization of the SIZ/PIAS-type SUMO E3 ligases, OsSIZ1 and OsSIZ2, in rice. Plant Cell Environ 33:1923–1934

    Article  PubMed  CAS  Google Scholar 

  • Park HJ, Park HC, Lee SY, Bohnert HJ, Yun D-J (2011) Ubiquitin and ubiquitin-like modifiers in plants. J Plant Biol 54:275–285

    Article  CAS  Google Scholar 

  • Park H-J, Yun D-J (2013) New insights into the role of the small ubiquitin-like modifier (SUMO) in Plants. Intl Rev Cell Mol Biol 300:161–209

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Roden J, Eardley L, Hotson A, Cao Y, Mudgett MB (2004) Characterization of the Xanthomonas AvrXv4 effector, a SUMO protease translocated into plant cells. Mol Plant-Microbe Interact 17:633–643

    Article  PubMed  CAS  Google Scholar 

  • Rubio V, Linhares F, Solano R, Martín AC, Iglesias J, Leyva A, Paz-Ares J (2001) A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev 15:2122–2133

    Article  PubMed  CAS  Google Scholar 

  • Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee B, Matsumoto TK, Koiwa H, Zhu J-K, Bressan RA, Hasegawa PM (2001) AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proc Natl Acad Sci USA 98:14150–14155

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Shin Y-C, Liu B-Y, Tsai J-Y, Wu J-T, Chang L-K, Chang S-C (2010) Biochemical characterization of the small ubiquitin-like modifiers of Chlamydomonas reinhardtii. Planta 232:649–662

    Article  PubMed  CAS  Google Scholar 

  • Thangasamy S, Guo C-L, Chuang M-H, Lai M-H, Chen J, Jauh G-Y (2011) Rice SIZ1, a SUMO E3 ligase, controls spikelet fertility through regulation of anther dehiscence. New Phytol 189:869–882

    Article  PubMed  CAS  Google Scholar 

  • Ulrich HD (2005) SUMO modification: wrestling with protein conformation. Curr Biol 15:R257–R259

    Article  PubMed  CAS  Google Scholar 

  • Vailleau F, Daniel X, Tronchet M, Montillet J-L, Triantaphylidès C, Roby D (2002) A R2R3-MYB gene, AtMYB30, acts as a positive regulator of the hypersensitive cell death program in plants in response to pathogen attack. Proc Natl Acad Sci USA 99:10179–10184

    Article  PubMed  CAS  Google Scholar 

  • van den Burg HA, Takken FLW (2009) Does chromatin remodeling mark systemic acquired resistance? Trends Plant Sci 14:286–294

    Article  PubMed  Google Scholar 

  • van den Burg HA, Takken FLW (2010) SUMO-, MAPK- and resistance protein-signaling converge at transcription complexes that regulate plant innate immunity. Plant Signal Behav 5:1597–1601

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Vijay-Kumar S, Bugg CE, Cook WJ (1987) Structure of ubiquitin refined at 1.8 Å resolution. J Mol Biol 194:531–544

    Article  PubMed  CAS  Google Scholar 

  • Wang H, Makeen K, Yan Y, Cao Y, Sun S, Xu G (2010a) OsSIZ1 regulates the vegetative growth and reproductive development in rice. Plant Mol Biol Rep 29:1–7

    Google Scholar 

  • Wang X, Du G, Wang X, Meng Y, Li Y, Wu P, Yi K (2010b) The function of LPR1 is controlled by an element in the promoter and is independent of SUMO E3 ligase SIZ1 in response to low Pi stress in Arabidopsis thaliana. Plant Cell Physiol 51:380–394

    Article  PubMed  Google Scholar 

  • Wang Y, Ladunga I, Miller AR, Horken KM, Plucinak T, Weeks DP, Bailey CP (2008) The small ubiquitin-like modifier (SUMO) and SUMO-conjugating system of Chlamydomonas reinhardtii. Genetics 179:166–192

    Google Scholar 

  • Westermann S, Cheeseman IM, Anderson S, Yates JR, Drubin DG, Barnes G (2003) Architecture of the budding yeast kinetochore reveals a conserved molecular core. J Cell Biol 163:215–222

    Article  PubMed  CAS  Google Scholar 

  • Yoo CY, Miura K, Jin JB, Lee J, Park HC, Salt DE, Yun D-J, Bressan RA, Hasegawa PM (2006) SIZ1 small ubiquitin-like modifier E3 ligase facilitates basal thermotolerance in Arabidopsis independent of salicylic acid. Plant Physiol 142:1548–1558

    Article  PubMed  CAS  Google Scholar 

  • Yuan H, Liu D (2008) Signaling components involved in plant responses to phosphate starvation. J Intl Plant Biol 50:849–859

    Article  CAS  Google Scholar 

  • Zheng Y, Schumaker KS, Guo Y (2012) Sumoylation of transcription factor MYB30 by the small ubiquitin-like modifier E3 ligase SIZ1 mediates abscisic acid response in Arabidopsis thaliana. Proc Natl Acad Sci USA 109:12822–12827

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Division of Applied Life Science (BK21 Program) and Plant Molecular Biology and Biotechnology Research Center, Gyeongsang National University, Jinju, 660-701, Korea

    Hee Jin Park & Dae-Jin Yun

Authors
  1. Hee Jin Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dae-Jin Yun
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dae-Jin Yun.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Park, H.J., Yun, DJ. SUMO proteins grapple with biotic and abiotic stresses in Arabidopsis . J. Plant Biol. 56, 77–84 (2013). https://doi.org/10.1007/s12374-013-0904-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-013-0904-x

Keywords

Search

Navigation