Overexpression of VrUBC1, a Mung Bean E2 Ubiquitin-Conjugating Enzyme, Enhances Osmotic Stress Tolerance in Arabidopsis

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Chung, Eunsook ^a   Cho, Chang Woo ^a   So, Hyun Ah ^a   Kang, Jee Sook ^a   Chung, Young Soo ^a   Lee, Jai Heon ^a  

^a Dong A University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ABSCISIC ACID; MESSENGER RNA; PROTEIN ATVBP1; RECOMBINANT PROTEIN; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; PLANT PROTEIN; UBIQUITIN;

ARABIDOPSIS THALIANA; ARTICLE; DEHYDRATION; DROUGHT STRESS; GENE FUNCTION; GENE INTERACTION; GENE OVEREXPRESSION; GENETIC CODE; GENETIC COMPLEMENTATION; GERMINATION; MUNG BEAN; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOTIC STRESS; PLANT GENE; PLANT RESPONSE; PLANT STOMA; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RNA GEL BLOT ANALYSIS; SALT STRESS; TRANSCRIPTION REGULATION; TWO HYBRID SYSTEM; UNINDEXED SEQUENCE; VRUBC1 GENE; WILD TYPE; ADAPTATION; ARABIDOPSIS; METABOLISM; OSMOTIC PRESSURE; PHYSIOLOGY; VIGNA;

ARABIDOPSIS; ARABIDOPSIS THALIANA; VIGNA RADIATA; VIGNA RADIATA VAR. RADIATA;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; OSMOTIC PRESSURE; PLANT PROTEINS; UBIQUITIN; VIGNA;

EID: 84879165754     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066056     Document Type: Article

References (66)

1. Boyer JS, (1982) Plant productivity and environment. Science 218: 443-448.
2. Bray EA, (1997) Plant responses to water deficit. Trends Plant Sci 2: 48-54.
3. Zhu JK, (2002) Salt and drought stress signal transduction in plants. Ann Rev Plant Biol 53: 247-273.
4. Kornitzer D, Ciechanover A, (2000) Modes of regulation of ubiquitin-mediated protein degradation. J Cell Physiol 182: 1-11.
5. Takai R, Matsuda N, Nakano A, Hasegawa K, Akimoto C, et al. (2002) EL5, a rice N-acetylchitooligosaccharide elicitor-responsive RING-H2 finger protein, is a ubiquitin ligase which functions in vitro in co-operation with an elicitor-responsive ubiquitin-conjugating enzyme, OsUBC5b. Plant J 30: 447-455.
6. Moon J, Parry G, Estelle M, (2004) The ubiquitin-proteasome pathway and plant development. Plant Cell 16: 3181-3195.
7. Dreher K, Callis J, (2007) Ubiquitin, hormones and biotic stress in plants. Ann Bot 99: 787-822.
8. Xu L, Ménard R, Berr A, Fuchs J, Cognat V, et al. (2009) The E2 ubiquitin-conjugating enzymes, AtUBC1 and AtUBC2, play redundant roles and are involved in activation of FLC expression and repression of flowering in Arabidopsis thaliana. Plant J 57: 279-288.
9. Jentsch S, (1992) The ubiquitin-conjugation system. Ann Rev Genet 26: 179-207.
10. Hershko A, Ganoth D, Sudakin V, Dahan A, Cohen LH, et al. (1998) The ubiquitin system. Ann Rev Biochem 67: 425-479.
11. Smalle J, Vierstra RD, (2004) The ubiquitin 26S proteasome proteolytic pathway. Ann Rev Plant Biol 55: 555-590.
12. Kraft E, Stone SL, Ma L, Su N, Gao Y, et al. (2005) Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiol 139: 1597-1611.
13. Glickman MH, Ciechanover A, (2002) The ubiquitin-proteasome proteolytic pathway, destruction for the sake of construction. Physiol Rev 82: 373-428.
14. Sung P, Prakash S, Prakash L, (1990) Mutation of cysteine-88 in the Saccharomyces cerevisiae RAD6 protein abolishes its ubiquitin-conjugating activity and its various biological functions. Proc Natl Acad Sci USA 87: 2695-2699.
15. Kalchman MA, Graham RK, Xia G, Kode HHB, Hodgson JG, et al. (1996) Huntingtin is ubiquitinated and interacts with a specific ubiquitin-conjugating enzyme. J Biol Chem 271: 19385-19394.
16. van Nocker S, Walker JM, Vierstra RD, (1996) The Arabidopsis thaliana UBC7/13/14 genes encode a family of multiubiquitin chain-forming E2 enzymes. J Biol Chem 271: 12150-12158.
17. Criqui MC, Engler JA, Camasses A, Capron A, Parmentier Y, et al. (2002) Molecular characterization of plant ubiquitin-conjugating enzymes belonging to the UbcP4/E2-C/UBCx/UbcH10 gene family. Plant Physiol 130: 1230-1240.
18. Wen R, Newton L, Li G, Wang H, Xiao W, (2006) Arabidopsis thaliana UBC13, implication of error-free DNA damage tolerance and Lys63-linked polyubiqutylation in plants. Plant Mol Biol 61: 241-253.
19. Sullivan ML, Vierstra RD, (1993) Formation of a stable adduct between ubiquitin and the Arabidopsis ubiquitin-conjugating enzyme AtUBC1. J Biol Chem 268: 8777-8780.
20. Feussner K, Feussner I, Leopold I, Wasternack C, (1997) Isolation of a cDNA coding for an ubiquitin-conjugating enzyme UBC1 of tomato - the first stress-induced UBC of higher plants. FEBS Lett 409: 211-215.
21. Zhou G-A, Chang R-Z, Qiu L-J, (2009) Overexpression of soybean ubiquitin-conjugating enzyme gene GmUBC2 confers enhanced drought and salt tolerance through modulating abiotic stress-responsive gene expression in Arabidopsis. Plant Mol Biol 72: 357-367.
22. Wan X, Mo A, Liu S, Yang L, Li L, (2011) Constitutive expression of a peanut ubiquitin-conjugating enzyme gene in Arabidopsis confers improved water-stress tolerance through regulation of stress-responsive gene expression. J Biosci Bioeng 111: 478-484.
23. Cui F, Liu L, Zhao Q, Zhang Z, Li Q, et al. (2012) Arabidopsis Ubiquitin Conjugase UBC32 Is an ERAD Component That Functions in Brassinosteroid-Mediated Salt Stress Tolerance. Plant Cell 24: 233-244.
24. Jeon EH, Pak JH, Kim MJ, Kim HJ, Shin SH, et al. (2012) Ectopic expression of ubiquitin-conjugating enzyme gene fro wild rice, OgUBC1, confers resistance against UV-B radiation and Botrytis infection in Arabidopsis thaliana. Biochem Biophys Res Commun 427: 309-314.
25. Lyzenga WJ, Stone SL, (2012) Abiotic stress tolerance mediated by protein ubiquitination. J Exp Bot 63: 599-616.
26. Cho SK, Chung HS, Ryu MY, Park MJ, Lee MM, et al. (2006) Heterologous expression and molecular and cellular characterization of CaPUB1 encoding a hot pepper U-box E3 ubiquitin ligase homolog. Plant Physiol 142: 1664-1682.
27. Cho SK, Ryu MY, Song C, Kwak JM, Kim WT, (2008) Arabidopsis PUB22 and PUB23 are homologous U-box E3 ubiquitin ligases that play combinatory roles in response to drought stress. Plant Cell 20: 1899-1914.
28. Lee H, Xiong L, Gong Z, Ishitani M, Stevenson B, et al. (2001) The Arabidopsis HOS1 gene negatively regulates cold signal transduction and encodes a RING finger protein that displays cold-regulated nucleocytoplasmic partitioning. Genes Dev 15: 912-924.
29. He YW, Xu M, Lin K, Ng YJ, Wen CM, et al. (2006) Genome scale analysis of diffusible signal factor regulon in Xanthomonas campestris pv. Campestris, Identification of novel cell-cell communication-dependent genes and functions. Mol Microbiol 59: 610-622.
30. Zhang X, Garreton V, Chua NH, (2005) The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Dev 19: 1532-1543.
31. Qin F, Sakuma Y, Tran L-SP, Maruyama K, Kidokoro S, et al. (2008) Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20: 1693-1707.
32. Stone SL, Williams LA, Farmer LM, Vierstra RD, Callis J, (2006) KEEP ON GOING, a RING E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 18: 3415-3428.
33. Luo J, Shen G, Yan J, He C, Zhang H, (2006) AtCHIP functions as an E3 ubiquitin ligase of protein phosphatase 2A subunits and alters plant responses to abscisic acid treatment. Plant J 46: 649-657.
34. Ko J-H, Yang SH, Han K-H, (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47: 343-355.
35. Bu Q, Li H, Zhao Q, Jiang H, Zhai Q, et al. (2009) The Arabidopsis RING finger E3 ligase RHA2a is a novel positive regulator of abscisic acid signaling during seed germination and early seedling development. Plant Physiol 150: 463-481.
36. Zhang Y, Yang C, Li Y, Zheng N, Chen H, et al. (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 19: 1912-1929.
37. Ryu MY, Cho SK, Kim WT, (2010) The Arabidopsis C3H2C3-type IRNG E3 ubiquitin ligase AtAIRP1 is a positive regulator of an abscisic acid-dependent response to drought stress. Plant Physiol 154: 1983-1997.
38. Cho SK, Ryu MY, Seo DH, Kang BG, Kim WT, (2011) The Arabidopsis RING E3 ubiquitin ligase AtAIRP2 plays combinatory roles with AtAIRP1 in abscisic-mediated drought stress responses. Plant Physiol 157: 2240-2257.
39. Chung E, Kim KM, Heo JE, Cho C-W, Lee SW, et al. (2009) Molecular characterization of mungbean alanine glyoxylate aminotransferase gene induced by low temperature stress. Genes Genomics 31: 11-18.
40. Treier M, Seufert W, Jentsch S, (1992) Drosophila UbcD1 encodes a highly conserved ubiquitin-conjugating enzyme involved in selective protein degradation. EMBO J 11: 367-372.
41. Zhen M, Heinlein R, Jones D, Jentsch S, Candido EP, (1993) The ubc-2 gene of Caenorhabditis elegans encodes a ubiquitin-conjugating enzyme involved in selective protein degradation. Mol Cell Biol 13: 1371-1377.
42. Liu ZM, Kolattukudy PE, (1998) Identification of a gene product induced by hard-surface contact of Colletotrichum gloeosporioides conidia as a ubiquitin-conjugating enzyme by yeast complementation. J Bacteriol 180: 3592-3597.
43. Zhang X-D, Jenkins JN, Callahan FE, Creech RG, Si Y, et al. (2003) Molecular cloning, differential expression, and functional characterization of a family of class I ubiquitin-conjugating enzyme (E2) genes in cotton (Gossypium). Biochim Biophys Acta 1625: 269-279.
44. Seufert W, Jentsch S, (1990) Ubiquitin-conjugating enzymes UBC4 and UBC5 mediate selective degradation of short-lived and abnormal proteins. EMBO J 9: 543-550.
45. Wu P-Y, Hanlon M, Eddins M, Tsui C, Rogers RS, et al. (2003) A conserved catalytic residue in the ubiquitin-conjugating enzyme family. EMBO J 22: 5241-5250.
46. Leung J, Giraudat J, (1998) Abscisic acid signal transduction. Ann Rev Plant Physiol Plant Mol Biol 49: 199-222.
47. Giraudat J, Parcy F, Bertauche N, Gosti F, Leung J, (1994) Current advances in abscisic acid action and signaling. Plant Mol Biol 26: 1557-1577.
48. Choi H, Hong J, Kang J, Kim SY, (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 21: 1723-1730.
49. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, et al. (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity. Proc Natl Acad Sci USA 97: 11632-11637.
50. Kim S, Kang J-Y, Cho D-I, Park JH, Kim SY, (2004) ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J 40: 75-87.
51. Kim SY, Ma J, Perret P, Li Z, Thomas TL, (2002) Arabidopsis ABI5 subfamily members have distinct DNA-binding and transcriptional activities. Plant Physiol 130: 688-697.
52. Lopez-Molina L, Mongrand S, Chua NH, (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABII5 transcription factor in Arabidopsis. Proc Natl Acad Sci USA 98: 4782-4787.
53. Stone SL, Hauksdóttir H, Troy A, Herschleb J, Kraft, et al, (2005) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol 137: 13-30.
54. Chung E, Seong E, Kim Y-C, Chung EJ, Oh S-K, et al. (2004) A method for high frequency virus-induced gene silencing in chilli pepper (Capsicum annuum L. cv. Bukang). Mol Cells 17: 377-380.
55. Hellmann H, Estelle M, (2002) Plant development, Regulation by protein degradation. Science 297: 793-797.
56. Zwirn P, Stary S, Luschnig C, Bachmair A, (1997) Arabidopsis thaliana RAD6 homolog AtUBC2 complements UV sensitivity, but not N-end rule degradation deficiency, of Saccharomyces cerevisiae rad6 mutants. Curr Genet 32: 309-314.
57. Reynolds P, Weber S, Prakash L, (1985) RAD6 gene of Saccharomyces cerevisiae encodes a protein containing a tract of 13 consecutive aspartates. Proc Natl Acad Sci USA 82: 168-172.
58. Schroeder JI, Kwak JM, Allen GJ, (2001) Guard cell abscisic acid signaling and engineering drought hardiness in plants. Nature 410: 327-330.
59. Markson G, Kiel C, Hyde R, Brown S, Charalabous P, et al. (2009) Analysis of the human E2 ubiquitin conjugating enzyme protein interaction network. Genome Res 19: 1905-1911.
60. van Wijk SJL, de Vries SJ, Kemmeren P, Huang A, Boelens R, et al. (2009) A comprehensive framework of E2-RING E3 interactions of the human hbiquitin-proteasome system. Mol Syst Biol 5: 295.
61. Chung E, Cho CW, Yun BH, Choi HK, So HA, et al. (2009) Molecular cloning and characterization of the soybean DEAD-box RNA helicase gene induced by low temperature stress. Gene 443: 91-99.
62. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Hoggins DG, (1997) The CLUSYAL-X windows interface, flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
63. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
64. Sullivan ML, Vierstra RD, (1991) Cloning of a 16-kDa ubiquitin carrier protein from wheat and Arabidopsis thaliana. J Biol Chem 266: 23878-23885.
65. Clough SJ, Bent AF, (1998) Floral dip, a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
66. Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, et al. (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40: 428-438.