ABD1 is an Arabidopsis DCAF substrate receptor for CUL4-DDB1-based E3 ligases that acts as a negative regulator of abscisic acid signaling

Plant Cell

Volumn 26, Issue 2, 2014, Pages 695-711

  Seo, Kyoung In ^a   Lee, Jae Hoon ^a,b   Nezames, Cynthia D ^a   Zhong, Shangwei ^a   Song, Eunyoung ^b   Byun, Myung Ok ^c   Deng, Xing Wang ^a  

^a YALE UNIVERSITY   (United States)

^b Pusan National University   (South Korea)

^c National Institute of Animal Science   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ABD1 PROTEIN, ARABIDOPSIS; ABI5 PROTEIN, ARABIDOPSIS; ABSCISIC ACID; ARABIDOPSIS PROTEIN; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CARRIER PROTEIN; CULLIN; CULLIN4 PROTEIN, ARABIDOPSIS; DDB1A PROTEIN, ARABIDOPSIS; DNA BINDING PROTEIN; SODIUM CHLORIDE; UBIQUITIN PROTEIN LIGASE;

ADAPTATION; AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CHEMISTRY; DROUGHT; DRUG EFFECT; ENZYME SPECIFICITY; GENE EXPRESSION REGULATION; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PLANT SEED; PLANT STOMA; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN STABILITY; SIGNAL TRANSDUCTION;

ABSCISIC ACID; ADAPTATION, PHYSIOLOGICAL; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; CARRIER PROTEINS; CULLIN PROTEINS; DNA-BINDING PROTEINS; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; GERMINATION; MOLECULAR SEQUENCE DATA; PLANT STOMATA; PROTEIN BINDING; PROTEIN STABILITY; PROTEOLYSIS; SEEDS; SIGNAL TRANSDUCTION; SODIUM CHLORIDE; SUBSTRATE SPECIFICITY; UBIQUITIN-PROTEIN LIGASES;

EID: 84897075811     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.119974     Document Type: Article

References (69)

1. Abe, H., Urao, T., Ito, T., Seki, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2003). Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15: 63-78.
2. Agarwal, P.K., Agarwal, P., Reddy, M.K., and Sopory, S.K. (2006). Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep. 25: 1263-1274.
3. Angers, S., Li, T., Yi, X., MacCoss, M.J., Moon, R.T., and Zheng, N. (2006). Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 443: 590-593.
4. Arroyo, A., Bossi, F., Finkelstein, R.R., and Leon, P. (2003). Three genes that affect sugar sensing (abscisic acid insensitive 4, abscisic acid insensitive 5, and constitutive triple response 1) are differentially regulated by glucose in Arabidopsis. Plant Physiol. 133: 231-242.
5. Aubert, Y., Vile, D., Pervent, M., Aldon, D., Ranty, B., Simonneau, T., Vavasseur, A., and Galaud, J.P. (2010). RD20, a stress-inducible caleosin, participates in stomatal control, transpiration and drought tolerance in Arabidopsis thaliana. Plant Cell Physiol. 51: 1975-1987.
6. Bernhardt, A., Mooney, S., and Hellmann, H. (2010). Arabidopsis DDB1a and DDB1b are critical for embryo development. Planta 232: 555-566.
7. Biedermann, S., and Hellmann, H. (2010). The DDB1a interacting proteins ATCSA-1 and DDB2 are critical factors for UV-B tolerance and genomic integrity in Arabidopsis thaliana. Plant J. 62: 404-415.
8. Biedermann, S., and Hellmann, H. (2011). WD40 and CUL4-based E3 ligases: Lubricating all aspects of life. Trends Plant Sci. 16: 38-46.
9. Bracha-Drori, K., Shichrur, K., Katz, A., Oliva, M., Angelovici, R., Yalovsky, S., and Ohad, N. (2004). Detection of protein-protein interactions in plants using bimolecular fluorescence complementation. Plant J. 40: 419-427.
10. Brocard, I.M., Lynch, T.J., and Finkelstein, R.R. (2002). Regulation and role of the Arabidopsis abscisic acid-insensitive 5 gene in abscisic acid, sugar, and stress response. Plant Physiol. 129: 1533-1543.
11. Chen, H., Huang, X., Gusmaroli, G., Terzaghi, W., Lau, O.S., Yanagawa, Y., Zhang, Y., Li, J., Lee, J.H., Zhu, D., and Deng, X.W. (2010). Arabidopsis CULLIN4-damaged DNA binding protein 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1-SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time. Plant Cell 22: 108-123.
12. Chen, H., Shen, Y., Tang, X., Yu, L., Wang, J., Guo, L., Zhang, Y., Zhang, H., Feng, S., Strickland, E., Zheng, N., and Deng, X.W. (2006). Arabidopsis CULLIN4 forms an E3 ubiquitin ligase with RBX1 and the CDD complex in mediating light control of development. Plant Cell 18: 1991-2004.
13. Chen, H., Zou, Y., Shang, Y., Lin, H., Wang, Y., Cai, R., Tang, X., and Zhou, J.M. (2008). Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol. 146: 368-376.
14. Cheong, Y.H., Pandey, G.K., Grant, J.J., Batistic, O., Li, L., Kim, B.G., Lee, S.C., Kudla, J., and Luan, S. (2007). Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J. 52: 223-239.
15. 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.
16. Cutler, S.R., Rodriguez, P.L., Finkelstein, R.R., and Abrams, S.R. (2010). Abscisic acid: Emergence of a core signaling network. Annu. Rev. Plant Biol. 61: 651-679.
17. Dai, M., Xue, Q., McCray, T., Margavage, K., Chen, F., Lee, J.H., Nezames, C.D., Guo, L., Terzaghi, W., Wan, J., Deng, X.W., and Wang, H. (2013). The PP6 phosphatase regulates ABI5 phosphorylation and abscisic acid signaling in Arabidopsis. Plant Cell 24: 517-534.
18. Dreher, K., and Callis, J. (2007). Ubiquitin, hormones and biotic stress in plants. Ann. Bot. (Lond.) 99: 787-822.
19. Dumbliauskas, E., Lechner, E., Jaciubek, M., Berr, A., Pazhouhandeh, M., Alioua, M., Cognat, V., Brukhin, V., Koncz, C., Grossniklaus, U., Molinier, J., and Genschik, P. (2011). The Arabidopsis CUL4-DDB1 complex interacts with MSI1 and is required to maintain MEDEA parental imprinting. EMBO J. 30: 731-743.
20. Finkelstein, R.R., and Lynch, T.J. (2000). The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12: 599-609.
21. Garcia, M.E., Lynch, T., Peeters, J., Snowden, C., and Finkelstein, R. (2008). A small plant-specific protein family of ABI five binding proteins (AFPs) regulates stress response in germinating Arabidopsis seeds and seedlings. Plant Mol. Biol. 67: 643-658.
22. Goda, H., et al. (2008). The AtGenExpress hormone and chemical treatment data set: Experimental design, data evaluation, model data analysis and data access. Plant J. 55: 526-542.
23. Groisman, R., Polanowska, J., Kuraoka, I., Sawada, J., Saijo, M., Drapkin, R., Kisselev, A.F., Tanaka, K., and Nakatani, Y. (2003). The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113: 357-367.
24. Gruber, H., Heijde, M., Heller, W., Albert, A., Seidlitz, H.K., and Ulm, R. (2010). Negative feedback regulation of UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. Proc. Natl. Acad. Sci. USA 107: 20132-20137.
25. Gu, Y., and Innes, R.W. (2011). The KEEP ON GOING protein of Arabidopsis recruits the ENHANCED DISEASE RESISTANCE1 protein to trans-Golgi network/early endosome vesicles. Plant Physiol. 155: 1827-1838.
26. Gu, Y., and Innes, R.W. (2012). The KEEP ON GOING protein of Arabidopsis regulates intracellular protein trafficking and is degraded during fungal infection. Plant Cell 24: 4717-4730.
27. He, Y.J., McCall, C.M., Hu, J., Zeng, Y., and Xiong, Y. (2006). DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev. 20: 2949-2954.
28. Higa, L.A., Wu, M., Ye, T., Kobayashi, R., Sun, H., and Zhang, H. (2006). CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat. Cell Biol. 8: 1277-1283.
29. Hotton, S.K., and Callis, J. (2008). Regulation of cullin RING ligases. Annu. Rev. Plant Biol. 59: 467-489.
30. Hua, Z., and Vierstra, R.D. (2011). The cullin-RING ubiquitin-protein ligases. Annu. Rev. Plant Biol. 62: 299-334.
31. Huang, X., Ouyang, X., Yang, P., Lau, O.S., Chen, L., Wei, N., and Deng, X.W. (2013). Conversion from CUL4-based COP1-SPA E3 apparatus to UVR8-COP1-SPA complexes underlies a distinct biochemical function of COP1 under UV-B. Proc. Natl. Acad. Sci. USA 110: 16669-16674.
32. Jin, J., Arias, E.E., Chen, J., Harper, J.W., and Walter, J.C. (2006). A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 23: 709-721.
33. Keeney, S., Chang, G.J., and Linn, S. (1993). Characterization of a human DNA damage binding protein implicated in xeroderma pigmentosum E. J. Biol. Chem. 268: 21293-21300.
34. Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O., D'Angelo, C., Bornberg-Bauer, E., Kudla, J., and Harter, K. (2007). The AtGenExpress global stress expression data set: Protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 50: 347-363.
35. Kim, S.Y., Ma, J., Perret, P., Li, Z., and Thomas, T.L. (2002). Arabidopsis ABI5 subfamily members have distinct DNA-binding and transcriptional activities. Plant Physiol. 130: 688-697.
36. Lee, J.H., Terzaghi, W., and Deng, X.W. (2011). DWA3, an Arabidopsis DWD protein, acts as a negative regulator in ABA signal transduction. Plant Sci. 180: 352-357.
37. Lee, J.H., Terzaghi, W., Gusmaroli, G., Charron, J.B., Yoon, H.J., Chen, H., He, Y.J., Xiong, Y., and Deng, X.W. (2008). Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell 20: 152-167.
38. Lee, J.H., Yoon, H.J., Terzaghi, W., Martinez, C., Dai, M., Li, J., Byun, M.O., and Deng, X.W. (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.
39. Li, H., Jiang, H., Bu, Q., Zhao, Q., Sun, J., Xie, Q., and 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.
40. Li, T., Chen, X., Garbutt, K.C., Zhou, P., and Zheng, N. (2006). Structure of DDB1 in complex with a paramyxovirus V protein: Viral hijack of a propeller cluster in ubiquitin ligase. Cell 124: 105-117.
41. Liu, H., and Stone, S.L. (2010). Abscisic acid increases Arabidopsis ABI5 transcription factor levels by promoting KEG E3 ligase self-ubiquitination and proteasomal degradation. Plant Cell 22: 2630-2641.
42. Liu, H., and Stone, S.L. (2013). Cytoplasmic degradation of the Arabidopsis transcription factor ABSCISIC ACID INSENSITIVE 5 is mediated by the RING-type E3 ligase KEEP ON GOING. J. Biol. Chem. 288: 20267-20279.
43. Lopez-Molina, L., Mongrand, S., and Chua, N.H. (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.
44. Lopez-Molina, L., Mongrand, S., Kinoshita, N., and Chua, N.H. (2003). AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes Dev. 17: 410-418.
45. Lopez-Molina, L., Mongrand, S., McLachlin, D.T., Chait, B.T., and Chua, N.H. (2002). ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J. 32: 317-328.
46. Ma, Y., Szostkiewicz, I., Korte, A., Moes, D., Yang, Y., Christmann, A., and Grill, E. (2009). Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324: 1064-1068.
47. Mazzucotelli, E., Belloni, S., Marone, D., De Leonardis, A., Guerra, D., Di Fonzo, N., Cattivelli, L., andMastrangelo, A. (2006). The e3 ubiquitin ligase gene family in plants: Regulation by degradation. Curr. Genomics 7: 509-522.
48. Miura, K., Lee, J., Jin, J.B., Yoo, C.Y., Miura, T., and Hasegawa, P.M. (2009). Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proc. Natl. Acad. Sci. USA 106: 5418-5423.
49. Mizuno, T., and Yamashino, T. (2008). Comparative transcriptome of diurnally oscillating genes and hormone-responsive genes in Arabidopsis thaliana: Insight into circadian clock-controlled daily responses to common ambient stresses in plants. Plant Cell Physiol. 49: 481-487.
50. Nakashima, K., Fujita, Y., Katsura, K., Maruyama, K., Narusaka, Y., Seki, M., Shinozaki, K., and Yamaguchi-Shinozaki, K. (2006). Transcriptional regulation of ABI3-and ABA-responsive genes including RD29B and RD29A in seeds, germinating embryos, and seedlings of Arabidopsis. Plant Mol. Biol. 60: 51-68.
51. Nemhauser, J.L., Hong, F., and Chory, J. (2006). Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell 126: 467-475.
52. Nezames, C.D., Sjogren, C.A., Barajas, J.F., and Larsen, P.B. (2012). The Arabidopsis cell cycle checkpoint regulators TANMEI/ ALT2 and ATR mediate the active process of aluminum-dependent root growth inhibition. Plant Cell 24: 608-621.
53. Nishimura, N., Sarkeshik, A., Nito, K., Park, S.Y., Wang, A., Carvalho, P.C., Lee, S., Caddell, D.F., Cutler, S.R., Chory, J., Yates, J.R., and Schroeder, J.I. (2010). PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J. 61: 290-299.
54. Park, S.Y., et al. (2009). Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071.
55. Pazhouhandeh, M., Molinier, J., Berr, A., and Genschik, P. (2011). MSI4/FVE interacts with CUL4-DDB1 and a PRC2-like complex to control epigenetic regulation of flowering time in Arabidopsis. Proc. Natl. Acad. Sci. USA 108: 3430-3435.
56. Pintard, L., Willems, A., and Peter, M. (2004). Cullin-based ubiquitin ligases: Cul3-BTB complexes join the family. EMBO J. 23: 1681-1687.
57. Piskurewicz, U., Jikumaru, Y., Kinoshita, N., Nambara, E., Kamiya, Y., and Lopez-Molina, L. (2008). The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20: 2729-2745.
58. Roelfsema, M.R.G., and Prins, H.B.A. (1995). Effect of abscisic acid on stomatal opening in isolated epidermal strips of abi mutants of Arabidopsis thaliana. Physiol. Plant. 95: 373-378.
59. Santiago, J., Rodrigues, A., Saez, A., Rubio, S., Antoni, R., Dupeux, F., Park, S.Y., Marquez, J.A., Cutler, S.R., and Rodriguez, P.L. (2009). Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J. 60: 575-588.
60. Schroeder, D.F., Gahrtz, M., Maxwell, B.B., Cook, R.K., Kan, J.M., Alonso, J.M., Ecker, J.R., and Chory, J. (2002). De-etiolated 1 and damaged DNA binding protein 1 interact to regulate Arabidopsis photomorphogenesis. Curr. Biol. 12: 1462-1472.
61. Scrima, A., Konickova, R., Czyzewski, B.K., Kawasaki, Y., Jeffrey, P.D., Groisman, R., Nakatani, Y., Iwai, S., Pavletich, N.P., and Thoma, N.H. (2008). Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 135: 1213-1223.
62. Shen, Y., Zhou, Z., Feng, S., Li, J., Tan-Wilson, A., Qu, L.J., Wang, H., and Deng, X.W. (2009). Phytochrome A mediates rapid red lightinduced phosphorylation of Arabidopsis FAR-RED ELONGATED HYPOCOTYL1 in a low fluence response. Plant Cell 21: 494-506.
63. Smalle, J., and Vierstra, R.D. (2004). The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55: 555-590.
64. Stone, S.L., Williams, L.A., Farmer, L.M., Vierstra, R.D., and 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.
65. Uno, Y., Furihata, T., Abe, H., Yoshida, R., Shinozaki, K., and 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.
66. Zhang, H., Ransom, C., Ludwig, P., and van Nocker, S. (2003). Genetic analysis of early flowering mutants in Arabidopsis defines a class of pleiotropic developmental regulator required for expression of the flowering-time switch flowering locus C. Genetics 164: 347-358.
67. Zhang, Y., Feng, S., Chen, F., Chen, H., Wang, J., McCall, C., Xiong, Y., and Deng, X.W. (2008). Arabidopsis DDB1-CUL4 ASSOCIATED FACTOR1 forms a nuclear E3 ubiquitin ligase with DDB1 and CUL4 that is involved in multiple plant developmental processes. Plant Cell 20: 1437-1455.
68. Zhong, W., Feng, H., Santiago, F.E., and Kipreos, E.T. (2003). CUL-4 ubiquitin ligase maintains genome stability by restraining DNAreplication licensing. Nature 423: 885-889.
69. Zhu, J.K. (2002). Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53: 247-273.