ABA receptors: The START of a new paradigm in phytohormone signalling

Journal of Experimental Botany

Volumn 61, Issue 12, 2010, Pages 3199-3210

  Klingler, John P ^a,b   Batelli, Giorgia ^a,b   Zhu, Jian Kang ^a,b  

^a KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Abiotic stress; Abscisic acid; Bet v 1 fold; Drought; PP2C; PYR PYL RCAR; Salinity; Signal receptor; SnRK; START domain

Indexed keywords

ABSCISIC ACID; ARABIDOPSIS PROTEIN; CELL SURFACE RECEPTOR; PHYTOHORMONE;

AMINO ACID SEQUENCE; ARABIDOPSIS; CROP; GENETICS; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; REVIEW; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

ABSCISIC ACID; AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CROPS, AGRICULTURAL; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PLANT GROWTH REGULATORS; RECEPTORS, CELL SURFACE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

ARABIDOPSIS;

EID: 77954763983     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erq151     Document Type: Review

References (92)

1. Bruzzone S, Moreschi I, Usai C, Guida L, Damonte G, Salis A, Scarfi S, Millo E, De Flora A, Zocchi E. 2007. Abscisic acid is an endogenous cytokine in human granulocytes with cyclic ADP-ribose as second messenger. Proceedings of the National Academy of Sciences, USA 104, 5759-5764.
2. Cao YJ, Wei Q, Liao Y, Song HL, Li X, Xiang CB, Kuai BK. 2009. Ectopic overexpression of AtHDG11 in tall fescue resulted in enhanced tolerance to drought and salt stress. Plant Cell Reports 28, 579-588.
3. Chen JG. 2008. Heterotrimeric G-protein signalling in Arabidopsis: puzzling G-protein-coupled receptor. Plant Signalling and Behavior 3, 1042-1045.
4. Chini A, Fonseca S, Fernandez G, et al. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666-671.
5. Chinnusamy V, Zhu JK. 2009. Epigenetic regulation of stress responses in plants. Current Opinion in Plant Biology 12, 133-139.
6. Christmann A, Moes D, Himmelbach A, Yang Y, Tang Y, Grill E. 2006. Integration of abscisic acid signalling into plant responses. Plant Biology 8, 314-325.
7. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR. 2010. Abscisic acid: emergence of a core signalling network. Annual Review of Plant Biology (In press).
8. Dharmasiri N, Dharmasiri S, Estelle M. 2005. The F-box protein TIR1 is an auxin receptor. Nature 435, 441-445.
9. Fernandes H, Pasternak O, Bujacz G, Bujacz A, Sikorski MM, Jaskolski M. 2008. Lupinus luteus pathogenesis-related protein as a reservoir for cytokinin. Journal of Molecular Biology 378, 1040-1051.
10. Finkelstein RR, Gampala SSL, Rock CD. 2002. Abscisic acid signalling in seeds and seedlings. The Plant Cell 14, S15-S45.
11. Fu DL, Uauy C, Distelfeld A, Blechl A, Epstein L, Chen XM, Sela HA, Fahima T, Dubcovsky J. 2009. A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323, 1357-1360.
12. Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park S-Y, Cutler SR, Sheen J, Rodriguez PL, Zhu JK. 2009. In vitro reconstitution of an abscisic acid signalling pathway. Nature 462, 660-664.
13. Fujii H, Zhu JK. 2009. Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proceedings of the National Academy of Sciences, USA 106, 8380-8385.
14. Fujii H, Verslues PE, Zhu JK. 2007. Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis. The Plant Cell 19, 485-494.
15. Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K. 2006. Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signalling networks. Current Opinion in Plant Biology 9, 436-442.
16. Fujita Y, Nakashima K, Yoshida T, et al. 2009. Three SnRK2 protein kinases are the main positive regulators of abscisic acid signalling in response to water stress in Arabidopsis. Plant and Cell Physiology 50, 2123-2132.
17. Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K. 2006. Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proceedings of the National Academy of Sciences, USA 103, 1988-1993.
18. Gao YJ, Zeng QN, Guo JJ, Cheng J, Ellis BE, Chen JG. 2007. Genetic characterization reveals no role for the reported ABA receptor, GCR2, in ABA control of seed germination and early seedling development in Arabidopsis. The Plant Journal 52, 1001-1013.
19. Geiger D, Scherzer S, Mumm P, et al. 2009. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signalling kinase-phosphatase pair. Proceedings of the National Academy of Sciences, USA 106, 21425-21430.
20. 2+ affinities. Proceedings of the National Academy of Sciences, USA doi/10.1073/pnas. 0912030107.
21. Griffiths J, Murase K, Rieu I, et al. 2006. Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. The Plant Cell 18, 3399-3414.
22. Guo J, Zeng Q, Emami M, Ellis BE, Chen J-G. 2008. The GCR2 gene family is not required for ABA control of seed germination and early seedling development in Arabidopsis. PLoS ONE 3, e2982.
23. 2+ channels at the plasma membrane of stomatal guard cells are activated by hyperpolarization and abscisic acid. Proceedings of the National Academy of Sciences, USA 97, 4967-4972.
24. Hirayama T, Shinozaki K. 2007. Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends in Plant Science 12, 343-351.
25. Huang DQ, Jaradat MR, Wu WR, Ambrose SJ, Ross AR, Abrams SR, Cutler AJ. 2007. Structural analogs of ABA reveal novel features of ABA perception and signalling in Arabidopsis. The Plant Journal 50, 414-428.
26. Illingworth CJR, Parkes KE, Snell CR, Mullineaux PM, Reynolds CA. 2008. Criteria for confirming sequence periodicity identified by Fourier transform analysis: application to GCR2, a candidate plant GPCR? Biophysical Chemistry 133, 28-35.
27. Iyer LM, Koonin EV, Aravind L. 2001. Adaptations of the helix-grip fold for ligand binding and catalysis in the START domain superfamily. Proteins-Structure Function and Genetics 43, 134-144.
28. Johnson RR, Wagner RL, Verhey SD, Walker-Simmons MK. 2002. The abscisic acid-responsive kinase PKABA1 interacts with a seed-specific abscisic acid response element-binding factor, TaABF, and phosphorylates TaABF peptide sequences. Plant Physiology 130, 837-846.
29. Johnston CA, Temple BR, Chen J-G, Gao Y, Moriyama EN, Jones AM, Siderovski DP, Willard FS. 2007. Comment on 'A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid'. Science 318, 914c.
30. Jones AM, Assmann SM. 2004. Plants: the latest model system for G-protein research. EMBO Reports 5, 572-578.
31. Jones AM, Sussman MR. 2009. A binding resolution. Plant Physiology 150, 3-5.
32. Koornneef M, Reuling G, Karssen CM. 1984. The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiologia Plantarum 61, 377-383.
33. Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI. 2003. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signalling in Arabidopsis. EMBO Journal 22, 2623-2633.
34. Lee SC, Lan W, Buchanan BB, Luan S. 2009. A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signalling in plant guard cells. Proceedings of the National Academy of Sciences, USA 106, 21419-21424.
35. Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J. 1994. Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science 264, 1448-1452.
36. 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. The Plant Cell 9, 759-771.
37. 2+ signals. Proceedings of the National Academy of Sciences, USA 102, 4203-4208.
38. Lin BL, Wang HJ, Wang JS, Zaharia LI, Abrams SR. 2005. Abscisic acid regulation of heterophylly in Marsilea quadrifolia L.: effects of R-(-) and S-(+) isomers. Journal of Experimental Botany 56, 2935-2948.
39. Liu JJ, Ekramoddoullah AKM. 2006. The family 10 of plant pathogenesis-related proteins: their structure, regulation, and function in response to biotic and abiotic stresses. Physiological and Molecular Plant Pathology 68, 3-13.
40. Liu XG, Yue YL, Li B, Nie YL, Li W, Wu WH, Ma LG. 2007. A G protein-coupled receptor is a plasma membrane receptor for the plant hormone abscisic acid. Science 315, 1712-1716.
41. Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E. 2009. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324, 1064-1068.
42. Markovic-Housley Z, Degano M, Lamba D, von Roepenack-Lahaye E, Clemens S, Susani M, Ferreira F, Scheiner O, Breiteneder H. 2003. Crystal structure of a hypoallergenic isoform of the major birch pollen allergen Bet v 1 and its likely biological function as a plant steroid carrier. Journal of Molecular Biology 325, 123-133.
43. McCourt P, Creelman R. 2008. The ABA receptors: we report you decide. Current Opinion in Plant Biology 11, 474-478.
44. Melcher K, Ng L-M, Zhou XE, et al. 2009. A gate-latch-lock mechanism for hormone signalling by abscisic acid receptors. Nature 462, 602-608.
45. Meyer K, Leube MP, Grill E. 1994. A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science 264, 1452-1455.
46. Miyazono K-I, Miyakawa T, Sawano Y, et al. 2009. Structural basis of abscisic acid signalling. Nature 462, 609-614.
47. Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J. 2001. Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proceedings of the National Academy of Sciences, USA 98, 2053-2058.
48. Muller AH, Hansson M. 2009. The barley magnesium chelatase 150-kD subunit is not an abscisic acid receptor. Plant Physiology 150, 157-166.
49. Murase K, Hirano Y, Sun T-p, Hakoshima T. 2008. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456, 459-463.
50. Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J. 2002. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. The Plant Cell 14, 3089-3099.
51. Nambara E, Marion-Poll A. 2005. Abscisic acid biosynthesis and catabolism. Annual Review of Plant Biology 56, 165-185.
52. Nambara E, Suzuki M, Abrams S, McCarty DR, Kamiya Y, McCourt P. 2002. A screen for genes that function in abscisic acid signalling in Arabidapsis thaliana. Genetics 161, 1247-1255.
53. 2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452, 483-486.
54. Nishimura N, Sarkeshi A, Nito K, et al. 2010. PYR/PYL/RACR family members are major in vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. The Plant Journal 61, 290-299
55. Nishimura N, Hitomi K, Arvai AS, Rambo R, Hitomi C, Cutler SR, Schroeder JI, Getzoff ED. 2009. Structural mechanism of abscisic acid binding and signalling by dimeric PYR1. Science 326, 1373-1379.
56. Nishimura N, Yoshida T, Kitahata N, Asami T, Shinozaki K, Hirayama T. 2007. ABA-Hypersensitive Germination1 encodes a protein phosphatase 2C, an essential component of abscisic acid signalling in Arabidopsis seed. The Plant Journal 50, 935-949.
57. Oritani T, Kiyota H. 2003. Biosynthesis and metabolism of abscisic acid and related compounds. Natural Product Reports 20, 414-425.
58. Pandey S, Nelson DC, Assmann SM. 2009. Two novel GPCR-type G Proteins are abscisic acid receptors in Arabidopsis. Cell 136, 136-148.
59. Park S-Y, Fung P, Nishimura N, et al. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324, 1068-1071.
60. Pasternak O, Bujacz GD, Fujimoto Y, Hashimoto Y, Jelen F, Otlewski J, Sikorski MM, Jaskolski M. 2006. Crystal structure of Vigna radiata cytokinin-specific binding protein in complex with zeatin. The Plant Cell 18, 2622-2634.
61. Peng JR, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP. 1997. The Arabidopsis GAI gene defines a signalling pathway that negatively regulates gibberellin responses. Genes and Development 11, 3194-3205.
62. Ponting CP, Aravind L. 1999. START: a lipid binding domain in StAR, HD-ZIP and signalling proteins. Trends in Biochemical Sciences 24, 130-132.
63. Radauer C, Lackner P, Breiteneder H. 2008. The Bet v. 1 fold: an ancient, versatile scaffold for binding of large, hydrophobic ligands. BMC Evolutionary Biology 8, 19.
64. Risk JM, Day CL, Macknight RC. 2009. Reevaluation of abscisic acid-binding assays shows that G-Protein-Coupled Receptor 2 does not bind abscisic acid. Plant Physiology 150, 6-11.
65. Saavedra X, Modrego A, Rodriguez D, Gonzalez-Garcia MP, Sanz L, Nicolas G, Lorenzo O. 2010. The nuclear interactor PYL8/RCAR3 of the Fagus sylvatica FSPP2C1 is a positive regulator of ABA signalling in seeds and stress. Plant Physiology 152, 133-150.
66. Saez A, Apostolova N, Gonzalez-Guzman M, Gonzalez-Garcia MP, Nicolas C, Lorenzo O, Rodriguez PL. 2004. Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. The Plant Journal 37, 354-369.
67. Santiago J, Dupeux F, Round A, Antoni R, Park S-Y, Jamin M, Cutler SR, Rodriguez PL, Marquez JA. 2009a. The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462, 665-668.
68. Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park S-Y, Marquez JA, Cutler SR, Rodriguez PL. 2009b. Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. The Plant Journal 60, 575-588.
69. Santner A, Estelle M. 2009. Recent advances and emerging trends in plant hormone signalling. Nature 459, 1071-1078.
70. Schweighofer A, Hirt H, Meskiene L. 2004. Plant PP2C phosphatases: emerging functions in stress signalling. Trends in Plant Science 9, 236-243.
71. Shen YY, Wang XF, Wu FQ, et al. 2006. The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443, 823-826.
72. Shimada A, Ueguchi-Tanaka M, Nakatsu T, Nakajima M, Naoe Y, Ohmiya H, Kato H, Matsuoka M. 2008. Structural basis for gibberellin recognition by its receptor GID1. Nature 456, 520-523.
73. Sirichandra C, Gu D, Hu HC, et al. 2009. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Letters 583, 2982-2986.
74. Sondheim E, Galson EC, Chang YP, Walton DC. 1971. Asymmetry, its importance to action and metabolism of abscisic acid. Science 174, 829-831.
75. 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 signalling. The Plant Cell 18, 3415-3428.
76. Sturla L, Fresia C, Guida L, et al. 2009. LANCL2 is necessary for abscisic acid binding and signalling in human granulocytes and in rat insulinoma cells. Journal of Biological Chemistry 284, 28045-28057.
77. Szostkiewicz I, Richter K, Kepka M, Demmel S, Ma Y, Korte A, Assaad FF, Christmann A, Grill E. 2010. Closely related receptor complexes differ in their ABA selectivity and sensitivity. The Plant Journal 61, 25-35.
78. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J. 2007. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448, 661-665.
79. Ueguchi-Tanaka M, Nakajima M, Katoh E, et al. 2007. Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. The Plant Cell 19, 2140-2155.
80. Urano K, Maruyama K, Ogata Y, et al. 2009. Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. The Plant Journal 57, 1065-1078.
81. Vahisalu T, Kollist H, Wang YF, et al. 2008. SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452, 487-491.
82. Verslues PE, Zhu JK. 2007. New developments in abscisic acid perception and metabolism. Current Opinion in Plant Biology 10, 447-452.
83. Walker-Simmons MK, Anderberg RJ, Rose PA, Abrams SR. 1992. Optically pure abscisic-acid analogs: tools for relating germination inhibition and gene-expression in wheat embryos. Plant Physiology 99, 501-507.
84. 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.
85. Wu FQ, Xin Q, Cao Z, et al. 2009. The magnesium-chelatase H subunit binds abscisic acid and functions in abscisic acid signalling: new evidence in Arabidopsis. Plant Physiology 150, 1940-1954.
86. Yan J, Zhang C, Gu M, et al. 2009. The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. The Plant Cell 21, 2220-2236.
87. Yin P, Fan H, Hao Q, Yuan X, Wu D, Pang Y, Yan C, Li W, Wang J, Yan N. 2009. Structural insights into the mechanism of abscisic acid signalling by PYL proteins. Nature Structural and Molecular Biology 16, 1230-1236.
88. Yoshida T, Nishimura N, Kitahata N, Kuromori T, Ito T, Asami T, Shinozaki K, Hirayama T. 2006. ABA-Hypersensitive germination3 encodes a protein phosphatase 2C (AtPP2CA) that strongly regulates abscisic acid signalling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiology 140, 115-126.
89. Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker JR, Shinozaki K. 2002. ABA-activated SnRK2 protein kinase is required for dehydration stress signalling in Arabidopsis. Plant and Cell Physiology 43, 1473-1483.
90. Yu H, Chen X, Hong YY, Wang Y, Xu P, Ke SD, Liu HY, Zhu JK, Oliver DJ, Xiang CB. 2008. Activated expression of an Arabidopsis HD-START protein confers drought tolerance with improved root system and reduced stomatal density. The Plant Cell 20, 1134-1151.
91. Zhang XR, Garreton V, Chua NH. 2005. The AIP2 E3 ligase acts as a novel negative regulator of ABA signalling by promoting ABI3 degradation. Genes and Development 19, 1532-1543.
92. Zhu JK. 2002. Salt and drought stress signal transduction in plants. Annual Review of Plant Biology 53, 247-273.