Reconstitution of Arabidopsis thaliana SUMO pathways in E. coli: Functional evaluation of SUMO machinery proteins and mapping of SUMOylation sites by mass spectrometry

Plant and Cell Physiology

Volumn 50, Issue 6, 2009, Pages 1049-1061

  Okada, Sachiko ^a   Nagabuchi, Mio ^a,b   Takamura, Yusuke ^a   Nakagawa, Tsuyoshi ^b   Shinmyozu, Kaori ^c   Nakayama, Jun Ichi ^c   Tanaka, Katsunori ^a  

^a KWANSEI GAKUIN UNIVERSITY   (Japan)

^b SHIMANE UNIVERSITY   (Japan)

^c RIKEN   (Japan)

Author keywords

Arabidopsis; Post translational modification; Reconstituted SUMOylation system; SUMO

Indexed keywords

ARABIDOPSIS PROTEIN; ISOPROTEIN; MYB30 PROTEIN, ARABIDOPSIS; SUMO PROTEIN; TRANSCRIPTION FACTOR;

ARABIDOPSIS; ARTICLE; ESCHERICHIA COLI; GENETICS; METABOLISM; PROTEIN PROCESSING;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ESCHERICHIA COLI; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; TRANSCRIPTION FACTORS;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA; ESCHERICHIA COLI;

EID: 67649369328     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcp056     Document Type: Article

References (41)

1. Ballesteros , M.L. , Bolle , C. , Lois , L.M. , Moore , J.M. , Vielle-Calzada , J.P. ,
2. Grossniklaus , U. , et al. (2001)LAF1, a MYB transcription activator for phytochrome A signaling . Genes Dev. 15 : 2613 - 2625 .
3. Budhiraja , R. , Hermkes , R. , Muller , S. , Schmidt , J. , Colby , T. , Panigrahi , K. , et al. (2009)Substrates related to chromatin and to RNA-dependent processes are modified by Arabidopsis SUMO isoforms that differ in a conserved residue with influence on de-sumoylation . P lant Physiol.149 : 1529 - 1540 .
4. Bylebyl , G.R. , Belichenko , I . and Johnson , E.S. (2003)The SUMO isopeptidase Ulp2 prevents accumulation of SUMO chains in yeast . J. Biol. Chem. 278 : 44113 - 44120 .
5. Catala , R. , Ouyang , J. , Abreu , I.A. , Hu , Y. , Seo , H. , Zhang , X. , et al. (2007) The Arabidopsis E3 SUMO ligase SIZ1 regulates plant growth and drought responses . P lant Cell 19 : 2952 - 2966 .
6. Chosed , R. , Mukherjee , S. , Lois , L.M. and Orth , K. (2006)Evolution of a signalling system that incorporates both redundancy and diversity: Arabidopsis SUMOylation . B iochem. J. 398 : 521 - 529 . Chosed , R. , Tomchick , D.R. , Brautigam , C.A. , Mukherjee , S. , Negi , V . S. ,
7. Machius , et al. (2007)Structural analysis of Xanthomonas XopD provides insights into substrate specificity of ubiquitin-like protein proteases . J. Biol. Chem. 282 : 6773 - 6782 .
8. Colby , T. , Matthai , A. , Boeckelmann , A. and Stuible , H.P. (2006)SUMOconjugating and SUMO-deconjugating enzymes from Arabidopsis . Plant Physiol. 142 : 318 - 332 . Conti , L. , Price , G. , O'Donnell , E. , Schwessinger , B. , Dominy , P. and
9. Sadanandom , A. (2008)Small ubiquitin-like modifier proteases OVERLY TOLERANT TO SALT1 and -2 regulate salt stress responses in Arabidopsis . P lant Cell 20 : 2894 - 2908 .
10. Daniel , X. , Lacomme , C. , Morel , J.B. and Roby , D. (1999)A novel myb oncogene homologue in Arabidopsis thaliana related to hypersensitive cell death . P lant J. 20 : 57 - 66 .
11. Garcia-Dominguez , M. , March-Diaz , R. and Reyes , J.C. (2008)The PHD domain of plant pias proteins mediates sumoylation of bromodomain GTE proteins . J. Biol. Chem. 283 : 21469 - 21477 .
12. Geiss-Friedlander , R. and Melchior , F. (2007)Concepts in sumoylation: a decade on . N at. Rev. Mol. Cell Biol. 8 : 947 - 956 . Guo , D. , Li , M. , Zhang , Y. , Yang , P. , Eckenrode , S. , Hopkins , D. , et al. (2004) A functional variant of SUMO4, a new I kappa B alpha modifier, is associated with type 1 diabetes . Nat. Genet. 36 : 837 - 841 .
13. Hecker , C.M. , Rabiller , M. , Haglund , K. , Bayer , P. and Dikic , I . (2006) Specification of SUMO1- and SUMO2-interacting motifs . J. Biol . Chem. 281 : 16117 - 16127 .
14. Hotson , A. , Chosed , R. , Shu , H. , Orth , K. and Mudgett , M.B. (2003) Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta . M ol. Microbiol. 50 : 377 - 389 .
15. Jin , J.B. , Jin , Y.H. , Lee , J. , Miura , K. , Yoo , C.Y. , Kim , W.Y. , e t al. (2008) The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through effects on FLC chromatin structure . Plant J. 53 : 530 - 540 .
16. Johnson , E.S. (2004)Protein modification by SUMO . A nnu. Rev . Biochem. 73 : 355 - 382 .
17. Kerscher , O. (2007)SUMO junction - what's your function? New insights through SUMO-interacting motifs . EMBO Rep. 8 : 550 - 555 . Knuesel , M. , Cheung , H.T. , Hamady , M. , Barthel , K.K. and Liu , X. (2005) A method of mapping protein sumoylation sites by mass spectrometry using a modified small ubiquitin-like modifier 1 (SUMO-1) and a computational program . Mol. Cell Proteomics 4 : 1626 - 1636 .
18. Kurepa , J. , Walker , J.M. , Smalle , J. , Gosink , M.M. , Davis , S.J. , Durham , T.L. , et al. (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 .
19. Lee , J. , Nam , J. , Park , H.C. , Na , G. , Miura , K. , Jin , J.B. , et al. (2007)Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase . P lant J. 49 : 79 - 90 .
20. Lois , L.M. and Lima , C.D. (2005)Structures of the SUMO E1 provide mechanistic insights into SUMO activation and E2 recruitment to E1 . E MBO J. 24 : 439 - 451 .
21. Lois , L.M. , Lima , C.D. and Chua , N.H. (2003)Small ubiquitin-like modifier modulates abscisic acid signaling in Arabidopsis . Plant Cell15 : 1347 - 1359 .
22. Martin , S. , Wilkinson , K.A. , Nishimune , A. and Henley , J.M. (2007) Emerging extranuclear roles of protein SUMOylation in neuronal function and dysfunction . N at. Rev. Neurosci. 8 : 948 - 959 .
23. Melchior , F. , Schergaut , M. and Pichler , A. (2003)SUMO: ligases, isopeptidases and nuclear pores . Trends Biochem. Sci. 28 : 612 - 618 .
24. Meluh , P.B. and 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 . Meulmeester , E. , Kunze , M. , Hsiao , H.H. , Urlaub , H. and Melchior , F. (2008) Mechanism and consequences for paralog-specific sumoylation of ubiquitin-specific protease 25 . M ol. Cell 3 0: 6 10- 6 19.
25. Miura , K. , Jin , J.B. and Hasegawa , P.M. (2007)Sumoylation, a posttranslational regulatory process in plants . Curr. Opin. Plant Biol. 10 : 495 - 502 . Miura , K. , Rus , A. , Sharkhuu , A. , Yokoi , S. , Karthikeyan , A.S. , Raghothama ,
26. K.G. , et al. (2005)The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses . P roc. Natl Acad. Sci. USA 102 : 7760 - 7765 . Murtas , G. , Reeves , P.H. , Fu , Y.F. , Bancroft , I . , Dean , C. and Coupland , G. (2003) A nuclear protease required for flowering-time regulation in Arabidopsis reduces the abundance of SMALL UBIQUITINRELATED MODIFIER conjugates . P lant Cell 15 : 2308 - 2319 .
27. Raffaele , S. , Rivas , S. and Roby , D. (2006)An essential role for salicylic acid in AtMYB30-mediated control of the hypersensitive cell death program in Arabidopsis . F EBS Lett. 580 : 3498 - 3504 . Raffaele , S. , Vailleau , F. , Leger , A. , Joubes , J. , Miersch , O. , Huard , C. , et al. (2008) A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis . P lant Cell 20 : 752 - 767 .
28. Roden , J. , Eardley , L. , Hotson , A. , Cao , Y. and Mudgett , M.B. (2004) Characterization of the Xanthomonas AvrXv4 effector, a SUMO protease translocated into plant cells . Mol. Plant-Microbe. Interact.17 : 633 - 643 . Rosas-Acosta , G. , Russell , W.K. , Deyrieux , A. , Russell , D.H. and Wilson , V.G. (2005) A universal strategy for proteomic studies of SUMO and other ubiquitin-like modifiers . M ol. Cell Proteomics 4 : 56 - 72 .
29. Saitoh , H. and Hinchey , J. (2000)Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3 . J. Biol. Chem. 275 : 6252 - 6258 .
30. Saracco , S.A. , Miller , M.J. , Kurepa , J. and Vierstra , R.D. (2007)Genetic analysis of SUMOylation in Arabidopsis: conjugation of SUMO1 and SUMO2 to nuclear proteins is essential . Plant Physiol. 145 : 119 - 134 .
31. Schmidt , D. and Muller , S. (2003)PIAS/SUMO: new partners in transcriptional regulation . C ell Mol. Life Sci. 60 : 2561 - 2574 .
32. Seeler , J.S. and Dejean , A. (2003)Nuclear and unclear functions of SUMO . N at. Rev. Mol. Cell Biol. 4 : 690 - 699 . Tatham , M.H. , Jaffray , E. , Vaughan , O.A. , Desterro , J.M. , Botting , C.H. ,
33. Naismith , J.H. , et al. (2001)Polymeric chains of SUMO-2 and SUMO-3 are conjugated to protein substrates by SAE1/SAE2 and Ubc9 . J. Biol. Chem. 276 : 35368 - 35374 . Uchimura , Y. , Nakamura , M. , Sugasawa , K. , Nakao , M. and Saitoh , H. (2004a) Overproduction of eukaryotic SUMO-1- and SUMO-2- conjugated proteins in Escherichia coli. Anal. Biochem. 331 : 204 - 206 . Uchimura , Y. , Nakao , M. and Saitoh , H. (2004b) Generation of SUMO-1 modified proteins in E. coli : towards understanding the biochemistry/structural biology of the SUMO-1 pathway . FEBS Lett.564 : 85 - 90 .
34. Vailleau , F. , Daniel , X. , Tronchet , M. , Montillet , J.L. , Triantaphylides , C. and 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 .
35. Vertegaal , A.C. , Andersen , J.S. , Ogg , S.C. , Hay , R.T. , Mann , M. and Lamond , A.I . (2006)Distinct and overlapping sets of SUMO-1 and SUMO-2 target proteins revealed by quantitative proteomics . Mol . Cell Proteomics 5 : 2298 - 2310 .
36. Wang , Y. , Ladunga , I . , Miller , A.R. , Horken , K.M. , Plucinak , T. , Weeks , D.P. , et al. (2008)The small ubiquitin-like modifier (SUMO) and SUMOconjugating system of Chlamydomonas reinhardtii . Genetics 179 : 177 - 192 .
37. Wohlschlegel , J.A. , Johnson , E.S. , Reed , S.I. and Yates , J.R. , 3rd (2006) Improved identification of SUMO attachment sites using C-terminal SUMO mutants and tailored protease digestion strategies . J. Proteome Res. 5 : 761 - 770 .
38. Xu , J. , He , Y. , Qiang , B. , Yuan , J. , Peng , X. and Pan , X.M. (2008)A novel method for high accuracy sumoylation site prediction from protein sequences . B MC Bioinformatics 9 : 8 .
39. Xue , Y. , Zhou , F. , Fu , C. , Xu , Y. and Yao , X. (2006)SUMOsp: a web server for sumoylation site prediction . Nucleic Acids Res. 34 : W254 - W257 .
40. Yoo , C.Y. , Miura , K. , Jin , J.B. , Lee , J. , Park , H.C. , Salt , D.E. , et al. (2006)SIZ1 small ubiquitin-like modifier E3 ligase facilitates basal thermotolerance in Arabidopsis independent of salicylic acid . Plant Physiol. 142 : 1548 - 1558
41. Zimmermann , P. , Hirsch-Hoffmann , M. , Hennig , L. and Gruissem , W. (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox . P lant Physiol. 136 : 2621 - 2632.