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SUMO conjugation in plants

Planta volume 220, pages 1–8 (2004)Cite this article

Abstract

Covalent attachment of small proteins to substrates can regulate protein activity in eukaryotes. SUMO, the small ubiquitin-related modifier, can be covalently linked to a broad spectrum of substrates. An understanding of SUMO’s role in plant biology is still in its infancy. In this review, we briefly summarize the enzymology of SUMO conjugation (sumoylation), and the current knowledge of SUMO modification in Arabidopsis thaliana (L.) Heynh. and other plants, in comparison to animals and fungi. Furthermore, we assemble a list of potential pathway components in the genome of A. thaliana that have either been functionally defined, or are suggested by similarity to pathway components from other organisms.

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Fig. 1
Fig. 2

Abbreviations

SAE :

SUMO-activating enzyme

SCE :

SUMO-conjugating enzyme

SUMO :

Small ubiquitin-related modifier

References

  • Amasino R (2004) Take a cold flower. Nat Genet 26:111–112

    Article  Google Scholar 

  • Bachant J, Alcasabas A, Blat Y, Kleckner N, Elledge SJ (2002) The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II. Mol Cell 9:1169–1182

    Article  CAS  PubMed  Google Scholar 

  • Bachmair A, Novatchkova M, Potuschak T, Eisenhaber F (2001) Ubiquitylation in plants: a post-genomic look at a post-translational modification. Trends Plant Sci 6:463–470

    Article  CAS  PubMed  Google Scholar 

  • Barrett AJ, Rawlings ND, Woessner JF (2004) Handbook of proteolytic enzymes, 2nd edn. Academic Press, New York

  • 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  CAS  PubMed  Google Scholar 

  • Bernier-Villamor V, Sampson DA, Matunis MJ, Lima CD (2002) Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108:345–356

    Article  CAS  PubMed  Google Scholar 

  • Best JL, Ganiatsas S, Agarwal S, Changou A, Salomoni P, Shirihai O, Meluh PB, Pandolfi PP, Zon LI (2002) SUMO-1 protease-1 regulates gene transcription through PML. Mol Cell 10:843–855

    Article  CAS  PubMed  Google Scholar 

  • Bies J, Markus J, Wolff L (2002) Covalent attachment of SUMO-1 protein to the negative regulatory domain of the c-Myb transcription factor modifies its stability and transactivation capacity. J Biol Chem 277:8999–9009

    Article  CAS  PubMed  Google Scholar 

  • Buchberger A (2002) From UBA to UBX: new words in the ubiquitin vocabulary. Trends Cell Biol 12:216–221

    Article  CAS  PubMed  Google Scholar 

  • David G, Neptune MA, DePinho RA (2002) SUMO-1 modification of histone deacetylase 1 (HDAC1) modulates its biological activity. J Biol Chem 277:23658–23663

    Article  CAS  PubMed  Google Scholar 

  • Gill G (2003) Post-translational modification by the small ubiquitin-related modifier SUMO has big effects on transcription factor activity. Curr Opin Genet Dev 13:108–113

    Article  CAS  PubMed  Google Scholar 

  • Girdwood D, Bumpass D, Vaughan OA, Thain A, Anderson LA, Snowden AW, Garcia-Wilson E, Perkins ND, Hay RT (2003) p300 transcriptional repression is mediated by SUMO modification. Mol Cell 11:1043–1054

    Article  CAS  PubMed  Google Scholar 

  • Gough J, Chothia C (2002) SUPERFAMILY: HMMs representing all proteins of known structure. SCOP sequence searches, alignments and genome assignments. Nucleic Acids Res 30:268–272

    Article  CAS  PubMed  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 

  • Hietakangas V, Ahlskog JK, Jakobsson AM, Hellesuo M, Sahlberg NM, Holmberg CI, Mikhailov A, Palvimo JJ, Pirkkala L, Sistonen L (2003) Phosphorylation of serine 303 is a prerequisite for the stress-inducible SUMO modification of heat shock transcription factor 1. Mol Cell Biol 23:2953–2968

    Article  CAS  PubMed  Google Scholar 

  • Hochstrasser M (2000) Evolution and function of ubiquitin-like protein conjugation systems. Nat Cell Biol 2:E153–E157

    Article  CAS  PubMed  Google Scholar 

  • Hoege C, Pfander B, Moldovan G-L, Pyrowolakis G, Jentsch S (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135–141

    Article  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  CAS  PubMed  Google Scholar 

  • Huang J, Dasso M (2002) Association of the human SUMO-1 protease SENP2 with the nuclear pore. J Biol Chem 277:19961–19966

    Article  PubMed  Google Scholar 

  • Huang TT, Wuerzberger-Davis SM, Wu Z-H, Miyamoto S (2003) Sequential modification of NEMO/IKKγ by SUMO-1 and ubiquitin mediates NF-κB activation by genotoxic stress. Cell 115:565–576

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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 

  • Johnson ES, Schwienhorst I, Dohmen RJ, Blobel G (1997) The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer. EMBO J 16:5509–5519

    Article  CAS  PubMed  Google Scholar 

  • Kagey HM, Melhuish TA, Wotton D (2003) The polycomb protein Pc2 is a SUMO E3. Cell 113:127–137

    Article  CAS  PubMed  Google Scholar 

  • Kahyo T, Nishida T, Yasuda H (2001) Involvement of PIAS1 in the sumoylation of tumor suppressor p53. Mol Cell 8:713–718

    Article  CAS  PubMed  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. J Biol Chem 278:6862–6872

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Li S-J, 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  Google Scholar 

  • Li S-J, Hochstrasser M (2003) The Ulp1 SUMO isopeptidase: distinct domains required for viability, nuclear envelope localization, and substrate specificity. J Cell Biol 160:1069–1081

    Article  CAS  PubMed  Google Scholar 

  • Lois LM, Lima CD, Chua N-H (2003) Small ubiquitin-like modifier modulates abscisic acid signaling in Arabidopsis. Plant Cell 15:1–13

    Article  PubMed  Google Scholar 

  • Marchler-Bauer A, Anderson JB, DeWeese-Scott C, Fedorova ND, Geer LY, He S, Hurwitz, DI, Jackson JD, Jacobs AR, Lanczycki CJ, Liebert CA, Liu C, Madej T, Marchler GH, Mazumder R, Nikolskaya AN, Panchenko AR, Rao BS, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Vasudevan S, Wang Y, Yamashita RA, Yin JJ and Bryant SH(2003) CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res 31:383–387

    Article  CAS  PubMed  Google Scholar 

  • Melchior F, Schergaut M, Pichler A (2003) SUMO: ligases, isopeptidases and nuclear pores. Trends Biochem Sci 28:612–618

    Article  CAS  PubMed  Google Scholar 

  • Mendoza HM, Shen L-n, Botting C, Lewis A, Chen J, Ink B, Hay RT (2003) NEDP1, a highly conserved cysteine protease that deneddylates cullins. J Biol Chem 278:25637–25643

    Article  CAS  PubMed  Google Scholar 

  • Müller S, Hoege C, Pyrowolakis G, Jentsch S (2001) SUMO, ubiquitin’s mysterious cousin. Nat Rev Mol Cell Biol 2:202–210

    Article  PubMed  Google Scholar 

  • Müller S, Ledl A, Schmidt D (2004) SUMO: a regulator of gene expression and genome integrity. Oncogene 23:1998–2008

    Article  PubMed  Google Scholar 

  • Murtas G, Reeves PH, Fu Y-F, 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. Plan Cell 15:2308–2319

    Article  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  CAS  PubMed  Google Scholar 

  • Pichler A, Gast A, Seeler JS, Dejean A, Melchior F (2002) The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108:109–120

    Article  CAS  PubMed  Google Scholar 

  • Rao-Naik C, de la Cruz W, Laplaza JM, Tan S, Callis J, Fisher AJ (1998) The Rub family of ubiquitin-like proteins—crystal structure of Arabidopsis Rub1 and expression of multiple Rubs in Arabidopsis. J Biol Chem 273:34976–34982

    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 

  • Rallabhandi P, Hashimoto K, Mo Y-Y, Beck WT, Moitra PK, D’Arpa P (2002) Sumoylation of topoisomerase I is involved in its partitioning between nucleoli and nucleoplasm and its clearing from nucleoli in response to camptothecin. J Biol Chem 277:40020–40026

    Article  CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Rose A, Meier I (2001) A domain unique to plant RanGAP is responsible for its targeting to the plant nuclear rim. Proc Natl Acad Sci USA 98:15377–15382

    Article  CAS  PubMed  Google Scholar 

  • Ross S, Best JL, Zon LI, Gill G (2002) SUMO-1 modification represses Sp3 transcriptional activation and modulates its subnuclear localization. Mol Cell 10:831–842

    Article  CAS  PubMed  Google Scholar 

  • Rychlewski L, Jaroszewski L, Li WZ, Godzik A (2000) Comparison of sequence profiles. Strategies for structural predictions using sequence information. Protein Sci 9:232–241

    CAS  PubMed  Google Scholar 

  • Sachdev S, Bruhn L, Sieber H, Pichler A, Melchior F, Grosschedl R (2001) PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev 15:3088–3103

    Article  CAS  PubMed  Google Scholar 

  • Saitoh H, Hinchey J (2000) Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J Biol Chem 275:6252–6258

    Article  CAS  PubMed  Google Scholar 

  • Sapetschnig A, Rischitor G, Braun H, Doll A, Schergaut M, Melchior F, Suske G (2002) Transcription factor Sp3 is silenced through SUMO modification by PIAS1. EMBO J 21:5206–5215

    Article  CAS  PubMed  Google Scholar 

  • Seeler JS, Dejean A (2003) Nuclear and unclear functions of SUMO. Nat Rev Mol Cell Biol 4:690–699

    Article  CAS  PubMed  Google Scholar 

  • Seufert W, Futcher B, Jentsch S (1995) A ubiquitin-conjugating enzyme involved in degradation of both M- and S-phase cyclins. Nature 373:78–81

    Article  CAS  PubMed  Google Scholar 

  • Shiio Y, Eisenman RN (2003) Histone sumoylation is associated with transcriptional repression. Proc Natl Acad Sci USA 100:13225–13230

    Article  CAS  PubMed  Google Scholar 

  • Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55:555–590

    Article  CAS  Google Scholar 

  • Tatusov RL, Fedorova ND, Jackson JD, Jacobs AR, Kiryutin B, Koonin EV, Krylov DM, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Smirnov S, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ and Natale DA (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:41

    Article  PubMed  Google Scholar 

  • Verger A, Perdomo J, Crossley M (2003) Modification with SUMO. A role in transcriptional regulation. EMBO Rep 4:137–142

    Article  CAS  PubMed  Google Scholar 

  • Walden H, Podgorski MS, Schulman BA (2003) Insights into the ubiquitin transfer cascade from the structure of the activating enzyme for Nedd8. Nature 422:330–334

    Article  CAS  PubMed  Google Scholar 

  • Wheeler DL, Church DM, Edgar R, Federhen S, Helmberg W, Madden TL, Pontius JU, Schuler GD, Schriml LM, Sequeira F, Suzek TO, Tatusova TA and Wagner L (2004) Database resources of the National Center for Biotechnology Information: update. Nucleic Acids Res 32:D35-D40

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Yong-Fu Fu (MPIZ, Cologne) for comments on the manuscript. The work in A.B.’s laboratory was supported by the Austrian Science Foundation FWF (grant P 13927), and by the Max Planck Society. M.N. and F.E. are grateful for generous support from Boehringer Ingelheim. This project was partly funded by the Austrian Gen-AU bioinformatics integration network sponsored by BM-BWK.

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Affiliations

  1. Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, 50829, Cologne, Germany

    Ruchika Budhiraja, George Coupland & Andreas Bachmair

  2. Institute for Molecular Pathology, 1030, Vienna, Austria

    Maria Novatchkova & Frank Eisenhaber

Authors
  1. Maria Novatchkova
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  2. Ruchika Budhiraja
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  3. George Coupland
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  4. Frank Eisenhaber
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  5. Andreas Bachmair
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Correspondence to Andreas Bachmair.

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Novatchkova, M., Budhiraja, R., Coupland, G. et al. SUMO conjugation in plants. Planta 220, 1–8 (2004). https://doi.org/10.1007/s00425-004-1370-y

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  • DOI: https://doi.org/10.1007/s00425-004-1370-y

  • Arabidopsis
  • Protein modification
  • Stress response
  • SUMO
  • Transcriptional regulation
  • Ubiquitin