Arabidopsis C3HC4-RING finger E3 ubiquitin ligase AtAIRP4 positively regulates stress-responsive abscisic acid signaling

Journal of Integrative Plant Biology

Volumn 58, Issue 1, 2016, Pages 67-80

  Yang, Liang ^a,b   Liu, Qiaohong ^a   Liu, Zhibin ^a   Yang, Hao ^a   Wang, Jianmei ^a   Li, Xufeng ^a   Yang, Yi ^a  

^a SICHUAN UNIVERSITY   (China)

^b CROP RESEARCH INSTITUTE   (China)

Author keywords

Abscisic acid; AtAIRP4; Drought stress; E3 ligase; Salt stress

Indexed keywords

ABSCISIC ACID; DEGRADATION; DROUGHT STRESS; GENE; LIGAND; PROTEIN; SALT;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ABSCISIC ACID; AIRP4 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; BACTERIAL DNA; SODIUM CHLORIDE; T-DNA; UBIQUITIN PROTEIN LIGASE;

AMINO ACID SEQUENCE; ARABIDOPSIS; CHEMISTRY; CYTOPLASM; CYTOSOL; DROUGHT; DRUG EFFECTS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; OSMOTIC PRESSURE; PHENOTYPE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT GENE; PLANT ROOT; PLANT STOMA; SEEDLING; SIGNAL TRANSDUCTION;

ABSCISIC ACID; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CYTOPLASM; CYTOSOL; DNA, BACTERIAL; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GERMINATION; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; OSMOTIC PRESSURE; PHENOTYPE; PLANT ROOTS; PLANT STOMATA; SEEDLINGS; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL; UBIQUITIN-PROTEIN LIGASES;

EID: 84953638511     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/jipb.12364     Document Type: Article

References (62)

1. Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15: 63-78
2. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
3. Bu Q, Li H, Zhao Q, Jiang H, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Wang D, Li C (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
4. Callis J, Vierstra RD (2000) Protein degradation in signaling. Curr Opin Plant Biol 3: 381-386
5. Cheng MC, Hsieh EJ, Chen JH, Chen HY, Lin TP (2012) Arabidopsis RGLG2, functioning as a RING E3 ligase, interacts with AtERF53 and negatively regulates the plant drought stress response. Plant Physiol 158: 363-375
6. 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 acid-mediated drought stress responses. Plant Physiol 157: 2240-2257
7. Clough SJ, Bent AF (1998) Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
8. Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33: 317-345
9. Finkelstein R, Gampala SS, Lynch TJ, Thomas TL, Rock CD (2005) Redundant and distinct functions of the ABA response loci ABA-INSENSITIVE(ABI) 5 and ABRE-BINDING FACTOR (ABF) 3. Plant Mol Biol 59: 253-267
10. Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12: 599-609
11. Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17: 3470-3488
12. Fujita Y, Fujita M, Shinozaki K, Yamaguchi-Shinozaki K (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124: 509-525
13. Glickman MH, Adir N (2004) The proteasome and the delicate balance between destruction and rescue. PLoS Biol 2: E13
14. Guo J, Wang J, Xi L, Huang WD, Liang J, Chen JG (2009) RACK1 is a negative regulator of ABA responses in Arabidopsis. J Exp Bot 60: 3819-3833
15. Guo L, Nezames CD, Sheng L, Deng X, Wei N (2013) Cullin-RING ubiquitin ligase family in plant abiotic stress pathways. J Integr Plant Biol 55: 21-30
16. Hellmann H, Estelle M (2002) Plant development: Regulation by protein degradation. Science 297: 793-797
17. Hetherington AM (2001) Guard cell signaling. Cell 107: 711-714
18. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27: 297-300
19. Holdsworth MJ, Bentsink L, Soppe WJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179: 33-54
20. Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator v3: A reference expression database for the meta-analysis of transcriptomes. Adv Bioinfor 2008: 420747
21. Kang JY, Choi HI, Im MY, Kim SY (2002) Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14: 343-357
22. Kang M, Fokar M, Abdelmageed H, Allen RD (2011) Arabidopsis SAP5 functions as a positive regulator of stress responses and exhibits E3 ubiquitin ligase activity. Plant Mol Biol 75: 451-466
23. Kim JH, Kim WT (2013) The Arabidopsis RING E3 ubiquitin ligase AtAIRP3/LOG2 participates in positive regulation of high-salt and drought stress responses. Plant Physiol 162: 1733-1749
24. Ko JH, Yang SH, Han KH (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47: 343-355
25. Kosarev P, Mayer KF, Hardtke CS (2002) Evaluation and classification of RING-finger domains encoded by the Arabidopsis genome. Genome Biol 3: RESEARCH0016
26. Lee JH, Yoon HJ, Terzaghi W, Martinez C, Dai M, Li J, Byun MO, Deng XW (2010) DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell 22: 1716-1732
27. Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Biol 49: 199-222
28. Leung J, Merlot S, Giraudat J (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9: 759-771
29. Li H, Jiang H, Bu Q, Zhao Q, Sun J, Xie Q, Li C (2011) The Arabidopsis RING finger E3 ligase RHA2b acts additively with RHA2a in regulating abscisic acid signaling and drought response. Plant Physiol 156: 550-563
30. Li J, Han Y, Zhao Q, Li C, Xie Q, Chong K, Xu Y (2013) The E3 ligase AtRDUF1 positively regulates salt stress responses in Arabidopsis thaliana. PLoS ONE 8: e71078
31. Liu ZB, Wang JM, Yang FX, Yang L, Yue YF, Xiang JB, Gao M, Xiong FJ, Lv D, Wu XJ, Liu N, Zhang X, Li XF, Yang Y (2014) A novel membrane-bound E3 ubiquitin ligase enhances the thermal resistance in plants. Plant Biotechnol J 12: 93-104
32. Lopez-Molina L, Mongrand S, Chua NH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci USA 98: 4782-4787
33. Mittal A, Gampala SS, Ritchie GL, Payton P, Burke JJ, Rock CD (2014) Related to ABA-Insensitive3(ABI3)/Viviparous1 and AtABI5 transcription factor coexpression in cotton enhances drought stress adaptation. Plant Biotechnol J 12: 578-589
34. Nemhauser JL, Hong F, Chory J (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126: 467-475
35. Penfield S, King J (2009) Towards a systems biology approach to understanding seed dormancy and germination. Proc Biol Sci 276: 3561-3569
36. Prestridge DS (1991) SIGNAL SCAN: A computer program that scans DNA sequences for eukaryotic transcriptional elements. Comput Appl Biosci 7: 203-206
37. Price J, Li TC, Kang SG, Na JK, Jang JC (2003) Mechanisms of glucose signaling during germination of Arabidopsis. Plant Physiol 132: 1424-1438
38. Rodriguez PL, Benning G, Grill E (1998) ABI2, a second protein phosphatase 2C involved in abscisic acid signal transduction in Arabidopsis. FEBS Lett 421: 185-190
39. Ryu MY, Cho SK, Kim WT (2010) The Arabidopsis C3H2C3-type RING E3 ubiquitin ligase AtAIRP1 is a positive regulator of an abscisic acid-dependent response to drought stress. Plant Physiol 154: 1983-1997
40. Sakuma Y, Maruyama K, Osakabe Y, Qin F, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2006a) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18: 1292-1309
41. Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006b) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103: 18822-18827
42. Salt JN, Yoshioka K, Moeder W, Goring DR (2011) Altered germination and subcellular localization patterns for PUB44/SAUL1 in response to stress and phytohormone treatments. PLoS ONE 6: e21321
43. Serino G, Xie Q (2013) The ever expanding role of ubiquitin and SUMO in plant biology. J Integr Plant Biol 55: 5-6
44. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58: 221-227
45. Smalle J, Vierstra RD (2004) The ubiquitin 26S proteasome proteolytic pathway. Annu Rev Plant Biol 55: 555-590
46. Stone SL, Callis J (2007) Ubiquitin ligases mediate growth and development by promoting protein death. Curr Opin Plant Biol 10: 624-632
47. Stone SL, Hauksdottir H, Troy A, Herschleb J, Kraft E, Callis J (2005) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol 137: 13-30
48. Tamura K, Dudley J, Nei M, Kumar S (2007) MEG A4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599
49. Tanaka H, Osakabe Y, Katsura S, Mizuno S, Maruyama K, Kusakabe K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) Abiotic stress-inducible receptor-like kinases negatively control ABA signaling in Arabidopsis. Plant J 70: 599-613
50. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97: 11632-11637
51. Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45: 523-539
52. Wenzel DM, Lissounov A, Brzovic PS, Klevit RE (2011) UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids. Nature 474: 105-108
53. Winter D, Vinegar B, Nahal H, Ammar R, Wilson GV, Provart NJ (2007) An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2: e718
54. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14 Suppl: S165-183
55. Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57: 781-803
56. Yanhui C, Xiaoyuan Y, Kun H, Meihua L, Jigang L, Zhaofeng G, Zhiqiang L, Yunfei Z, Xiaoxiao W, Xiaoming Q, Yunping S, Li Z, Xiaohui D, Jingchu L, Xing-Wang D, Zhangliang C, Hongya G, Li-Jia Q (2006) The MYB transcription factor superfamily of Arabidopsis: Expression analysis and phylogenetic comparison with the rice MYB family. Plant Mol Biol 60: 107-124
57. Yoo S-D, Cho Y-H, Sheen J (2007) Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565-1572
58. Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010) AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J 61: 672-685
59. Zhang S, Qi Y, Liu M, Yang C (2013) SUMO E3 ligase AtMMS21 regulates drought tolerance in Arabidopsis thaliana. J Integr Plant Biol 55: 83-95
60. Zhang Y, Yang C, Li Y, Zheng N, Chen H, Zhao Q, Gao T, Guo H, Xie Q (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. Plant Cell 19: 1912-1929
61. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53: 247-273
62. Zimmermann P, Hennig L, Gruissem W (2005) Gene-expression analysis and network discovery using Genevestigator. Trends Plant Sci 10: 407-409