Arabidopsis HIGH PLOIDY2 Sumoylates and stabilizes flowering locus C through Its E3 ligase activity

Frontiers in Plant Science

Volumn 7, Issue APR2016, 2016, Pages

  Kwak, Jun S ^a   Son, Ga H ^a   Kim, Sung Ii ^a   Song, Jong T ^b   Seo, Hak S ^a,c  

^a Seoul National University   (South Korea)

^b Kyungpook National University   (South Korea)

^c Seoul National University   (South Korea)

Author keywords

E3 SUMO ligase; FLC; HPY2; Post translational modification; SUMO; Sumoylation

Indexed keywords

EID: 84964253049     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.00530     Document Type: Article

References (54)

1. Bernier-Villamor, V., Sampson, D. A., Matunis, M. J., and Lima, C. D. (2002). Structural basis for E2-mediated SUMO conjugation revealed by a complex between ubiquitin-conjugating enzyme Ubc9 and RanGAP1. Cell 108, 345-356. doi: 10. 1016/S0092-8674(02)00630-X
2. Castro, P. H., Tavares, R. M., Bejarano, E. R., and Azevedo, H. (2012). SUMO, a heavyweight player in plant abiotic stress responses. Cell. Mol. Life Sci. 69, 3269-3283. doi: 10. 1007/s00018-012-1094-2
3. 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. Plant Cell 19, 2952-2966. doi: 10. 1105/tpc. 106. 049981
4. Cheong, M. S., Park, H. C., Hong, M. J., Lee, J., Choi, W., Jin, J. B., et al. (2009). Specific domain structures control abscisic acid-, salicylic acid-, and stress-mediated SIZ1 phenotypes. Plant Physiol. 151, 1930-1942. doi: 10. 1104/pp. 109. 143719
5. Clough, S. J., and Bent, A. F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743. doi: 10. 1046/j. 1365-313x. 1998. 00343. x
6. Colby, T., Matthai, A., Boeckelmann, A., and Stuible, H. P. (2006). SUMO-conjugating and SUMO-deconjugating enzymes from Arabidopsis. Plant Physiol. 142, 318-332. doi: 10. 1104/pp. 106. 085415
7. Conti, L., Nelis, S., Zhang, C., Woodcock, A., Swarup, R., Galbiati, M., et al. (2014). Small Ubiquitin-like Modifier protein SUMO enables plants to control growth independently of the phytohormone gibberellin. Dev. Cell 28, 102-110. doi: 10. 1016/j. devcel. 2013. 12. 004
8. Conti, L., Price, G., O'Donnell, E., Schwessinger, B., Dominy, P., and 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. doi: 10. 1105/tpc. 108. 058669
9. Elrouby, N., and 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. doi: 10. 1073/pnas. 1005452107
10. 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. doi: 10. 1074/jbc. M708176200
11. Greb, T., Mylne, J. S., Crevillen, P., Geraldo, N., An, H., Gendall, A. R., et al. (2007). The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Curr. Biol. 17, 73-78. doi: 10. 1016/j. cub. 2006. 11. 052
12. He, Y., and Amasino, R. M. (2005). Role of chromatin modification in flowering-time control. Trends Plant Sci. 10, 30-35. doi: 10. 1016/j. tplants. 2004. 11. 003
13. Heo, J. B., and Sung, S. (2011). Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76-79. doi: 10. 1126/science. 1197349
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. Mol. Microbiol. 50, 377-389. doi: 10. 1046/j. 1365-2958. 2003. 03730. x
15. Huang, L., Yang, S., Zhang, S., Liu, M., Lai, J., Qi, Y., et al. (2009). The Arabidopsis SUMO E3 ligase AtMMS21, a homologue of NSE2/MMS21, regulates cell proliferation in the root. Plant J. 60, 666-678.
16. Ishida, T., Fujiwara, S., Miura, K., Stacey, N., Yoshimura, M., Schneider, K., et al. (2009). SUMO E3 ligase HIGH PLOIDY2 regulates endocycle onset and meristem maintenance in Arabidopsis. Plant Cell 21, 2284-2297. doi: 10. 1105/tpc. 109. 068072
17. Ishida, T., Yoshimura, M., Miura, K., and Sugimoto, K. (2012). MMS21/HPY2 and SIZ1, two Arabidopsis SUMO E3 ligases, have distinct functions in development. PLoS ONE 7: e46897. doi: 10. 1371/journal. pone. 0046897
18. Jin, J. B., Jin, Y. H., Lee, J., Miura, K., Yoo, C. Y., Kim, W. Y., et al. (2008). The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure. Plant J. 53, 530-540.
19. Johnson, E. S., and Gupta, A. A. (2001). An E3-like factor that promotes SUMO conjugation to the yeast septins. Cell 106, 735-744. doi: 10. 1016/S0092-8674(01)00491-3
20. Kagey, M. H., Melhuish, T. A., and Wotton, D. (2003). The polycomb protein Pc2 is a SUMO E3. Cell 113, 127-137. doi: 10. 1016/S0092-8674(03)00159-4
21. Kahyo, T., Nishida, T., and Yasuda, H. (2001). Involvement of PIAS1 in the sumoylation of tumor suppressor p53. Mol. Cell 8, 713-718. doi: 10. 1016/S1097-2765(01)00349-5
22. Kim, D. Y., Han, Y. J., Kim, S., Song, J. T., and Seo, H. S. (2015). Arabidopsis CMT3 activity is positively regulated by AtSIZ1-mediated sumoylation. Plant Sci. 239, 209-215. doi: 10. 1016/j. plantsci. 2015. 08. 003
23. Kim, S. I., Park, B. S., Kim, D. Y., Yeu, S. Y., Song, S. I., Song, J. T., et al. (2015). E3 SUMO ligase AtSIZ1 positively regulates SLY1-mediated GA signaling and plant development. Biochem. J. 469, 299-314. doi: 10. 1042/BJ20141302
24. Krichevsky, A., Gutgarts, H., Kozlovsky, S. V., Tzfira, T., Sutton, A., Sternglanz, R., et al. (2006). C2H2 zinc finger-SET histone methyltransferase is a plant-specific chromatin modifier. Dev. Biol. 303, 259-269. doi: 10. 1016/j. ydbio. 2006. 11. 012
25. 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. doi: 10. 1074/jbc. M209694200
26. 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. Plant J. 49, 79-90. doi: 10. 1111/j. 1365-313X. 2006. 02947. x
27. Lois, L. M., Lima, C. D., and Chua, N. H. (2003). Small ubiquitin-like modifier modulates abscisic acid signaling in Arabidopsis. Plant Cell 15, 1347-1359. doi: 10. 1105/tpc. 009902
28. 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. Mol. Cell 30, 610-669. doi: 10. 1016/j. molcel. 2008. 03. 021
29. Michaels, S. D., and Amasino, R. M. (1999). FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11, 949-956. doi: 10. 1105/tpc. 11. 5. 949
30. Miller, M. J., Barrett-Wilt, G. A., Hua, Z., and Vierstra, R. D. (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. doi: 10. 1073/pnas. 1004181107
31. Miura, K., and Hasegawa, P. M. (2010). Sumoylation and other ubiquitin-like posttranslational modifications in plants. Trends Cell Biol. 20, 223-232. doi: 10. 1016/j. tcb. 2010. 01. 007
32. Miura, K., Jin, J. B., and Hasegawa, P. M. (2007a). Sumoylation, a post-translational regulatory process in plants. Curr. Opin. Plant Biol. 10, 495-502. doi: 10. 1016/j. pbi. 2007. 07. 002
33. Miura, K., Jin, J. B., Lee, J., Yoo, C. Y., Stirm, V., Miura, T., et al. (2007b). SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 9, 1403-1414. doi: 10. 1105/tpc. 106. 048397
34. Miura, K., Lee, J., Miura, T., and Hasegawa, P. M. (2010). SIZ1 controls cell growth and plant development in Arabidopsis through salicylic acid. Plant Cell Physiol. 51, 103-113. doi: 10. 1093/pcp/pcp171
35. Miura, K., and Ohta, M. (2010). SIZ1, a small ubiquitin-related modifier ligase, controls cold signaling through regulation of salicylic acid accumulation. J. Plant Physiol. 167, 555-560. doi: 10. 1016/j. jplph. 2009. 11. 003
36. Miura, K., Rus, A., Sharkhuu, A., Yokoi, S., Karthikeyan, A. S., Raghothama, K. G., et al. (2005). The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc. Natl. Acad. Sci. U. S. A. 102, 7760-7765. doi: 10. 1073/pnas. 0500778102
37. 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 UBIQUITIN-RELATED MODIFIER conjugates. Plant Cell 15, 2308-2319. doi: 10. 1105/tpc. 015487
38. Okushima, Y., Shimizu, K., Ishida, T., Sugimoto, K., and Umeda, M. (2014). Differential regulation of B2-type CDK accumulation in Arabidopsis roots. Plant Cell Rep. 33, 1033-1040. doi: 10. 1007/s00299-014-1581-z
39. Park, B. S., Sang, W. G., Yeu, S. Y., Choi, Y. D., Paek, N. C., Kim, M. C., et al. (2007). Post-translational regulation of FLC is mediated by an E3 ubiquitin ligase activity of SINAT5 in Arabidopsis. Plant Sci. 173, 269-275. doi: 10. 1016/j. plantsci. 2007. 06. 001
40. Park, B. S., Song, J. T., and Seo, H. S. (2011). Arabidopsis nitrate reductase activity is stimulated by the E3 SUMO ligase AtSIZ1. Nat. Commun. 2, 400. doi: 10. 1038/natcomms1408
41. Park, H. J., and Yun, D. J. (2013). New insights into the role of the small ubiquitin-like modifier (SUMO) in plants. Int. Rev. Cell Mol. Biol. 300, 161-209. doi: 10. 1016/B978-0-12-405210-9. 00005-9
42. Pichler, A., Gast, A., Seeler, J. S., Dejean, A., and Melchior, F. (2002). The nucleoporin RanBP2 has SUMO1 E3 ligase activity. Cell 108, 109-120. doi: 10. 1016/S0092-8674(01)00633-X
43. Rose, A., and Meier, I. (2001). A domain unique to plant RanGAP is responsible for its targeting to the plant nuclear rim. Proc. Natl. Acad. Sci. U. S. A. 98, 15377-15382. doi: 10. 1073/pnas. 261459698
44. Samach, A., Onouchi, H., Gold, S. E., Ditta, Z. S., Schwarz-Sommer, Z., Yanofsky, M. F., et al. (2000). Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288, 1613-1616. doi: 10. 1126/science. 288. 5471. 1613
45. Sharrocks, A. D. (2006). PIAS proteins and transcriptional regulation-more than just SUMO E3 ligases? Genes Dev. 20, 754-758. doi: 10. 1101/gad. 1421006
46. Sheldon, C. C., Burn, J. E., Perez, P. P., Metzger, J., Edwards, J. A., Peacock, W. J., et al. (1999). The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11, 445-458. doi: 10. 1105/tpc. 11. 3. 445
47. Simpson, G. G., and Dean, C. (2002). Arabidopsis, the Rosetta stone of flowering time? Science 296, 285-289. doi: 10. 1126/science. 296. 5566. 285
48. Son, G. H., Park, B. S., Song, J. T., and Seo, H. S. (2014). FLC-mediated flowering repression is positively regulated by sumoylation. J. Exp. Bot. 65, 339-351. doi: 10. 1093/jxb/ert383
49. Swiezewski, S., Liu, F., Magusin, A., and Dean, C. (2009). Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462, 799-802. doi: 10. 1038/nature08618
50. Verger, A., Perdomo, J., and Crossley, M. (2003). Modification with SUMO. EMBO Rep. 4, 137-142. doi: 10. 1038/sj. embor. embor738
51. Wilkinson, K. A., and Henley, J. M. (2010). Mechanisms, regulation and consequences of protein SUMOylation. Biochem. J. 428, 133-145. doi: 10. 1042/BJ20100158
52. 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. 42, 1548-1558. doi: 10. 1104/pp. 106. 088831
53. Zheng, Y., Schumaker, K. S., and 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. U. S. A. 109, 12822-12827. doi: 10. 1073/pnas. 1202630109
54. Zhu, J., Zhu, S., Guzzo, C. M., Ellis, N. A., Sung, K. S., Choi, C. Y., et al. (2008). Small ubiquitin-related modifier (SUMO) binding determines substrate recognition and paralog-selective SUMO modification. J. Biol. Chem. 283, 29405-29415. doi: 10. 1074/jbc. M803632200