Tomato PYR/PYL/RCAR abscisic acid receptors show high expression in root, differential sensitivity to the abscisic acid agonist quinabactin, and the capability to enhance plant drought resistance

Journal of Experimental Botany

Volumn 65, Issue 15, 2014, Pages 4451-4464

  Gonzalez Guzman, Miguel ^a   Rodriguez, Lesia ^a   Lorenzo Orts, Laura ^a   Pons, Clara ^a   Sarrion Perdigones, Alejandro ^a   Fernandez, Maria A ^a   Peirats Llobet, Marta ^a   Forment, Javier ^a   Moreno Alvero, Maria ^b   Cutler, Sean R ^c   Albert, Armando ^b   Granell, Antonio ^a   Rodriguez, Pedro L ^a  

^a Ciudad Politécnica de la Innovación   (Spain)

^b INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Abscisic acid (ABA); drought resistance; tomato ABA receptor; tomato clade A PP2C

Indexed keywords

ABSCISIC ACID; ARABIDOPSIS PROTEIN; CARRIER PROTEIN; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN PHOSPHATASE 2C; PYR1 PROTEIN, ARABIDOPSIS; QUINABACTIN; QUINOLONE DERIVATIVE; RCAR1 PROTEIN, ARABIDOPSIS; SULFONAMIDE; VEGETABLE PROTEIN;

ADAPTATION; AGONISTS; ANTAGONISTS AND INHIBITORS; ARABIDOPSIS; DROUGHT; GENE EXPRESSION REGULATION; METABOLISM; PLANT GENOME; PLANT ROOT; TOMATO;

ABSCISIC ACID; ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CARRIER PROTEINS; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; GENOME, PLANT; LYCOPERSICON ESCULENTUM; MEMBRANE TRANSPORT PROTEINS; PHOSPHOPROTEIN PHOSPHATASES; PLANT PROTEINS; PLANT ROOTS; QUINOLONES; SULFONAMIDES;

EID: 84905167597     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru219     Document Type: Article

References (59)

1. Antoni R, Gonzalez-Guzman M, Rodriguez L, Rodrigues A, Pizzio GA, Rodriguez PL. 2012. Selective inhibition of clade A phosphatases type 2C by PYR/PYL/RCAR abscisic acid receptors. Plant Physiology 158, 970-980.
2. Antoni R, Gonzalez-Guzman M, Rodriguez L, et al. 2013. PYRABACTIN RESISTANCE1-LIKE8 plays an important role for the regulation of abscisic acid signalling in root. Plant Physiology 161, 931-941.
3. Bai G, Yang DH, Zhao Y, Ha S, Yang F, Ma J, Gao XS, Wang ZM, Zhu JK. 2013. Interactions between soybean ABA receptors and type 2C protein phosphatases. Plant Molecular Biology 83, 651-664.
4. Baykov AA, Evtushenko OA, Avaeva SM. 1988. A malachite green procedure for orthophosphate determination and its use in alkaline phosphatase-based enzyme immunoassay. Analytical Biochemistry 171, 266-270.
5. Ben-Ari G. 2012. The ABA signal transduction mechanism in commercial crops: learning from Arabidopsis. Plant Cell Reports 31, 1357-1369.
6. Bensmihen S, To A, Lambert G, Kroj T, Giraudat J, Parcy F. 2004. Analysis of an activated ABI5 allele using a new selection method for transgenic Arabidopsis seeds. FEBS Letters 561, 127-131.
7. Bhaskara GB, Nguyen TT, Verslues PE. 2012. Unique drought resistance functions of the highly ABA-induced clade A protein phosphatase 2Cs. Plant Physiology 160, 379-395.
8. Boneh U, Biton I, Zheng C, Schwartz A, Ben-Ari G. 2012. Characterization of potential ABA receptors in Vitis vinifera. Plant Cell Reports 31, 311-321.
9. Boursiac Y, Leran S, Corratge-Faillie C, Gojon A, Krouk G, Lacombe B. 2013. ABA transport and transporters. Trends in Plant Science 18, 325-333.
10. Cao M, Liu X, Zhang Y, et al. 2013. An ABA-mimicking ligand that reduces water loss and promotes drought resistance in plants. Cell Research 23, 1043-1054.
11. Chai YM, Jia HF, Li CL, Dong QH, Shen YY. 2011. FaPYR1 is involved in strawberry fruit ripening. Journal of Experimental Botany 62, 5079-5089.
12. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR. 2010. Abscisic acid: emergence of a core signalling network. Annual Review of Plant Biology 61, 651-679.
13. Deblaere R, Bytebier B, De Greve H, Deboeck F, Schell J, Van Montagu M, Leemans J. 1985. Effcient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants. Nucleic Acids Research 13, 4777-4788.
14. Des Marais DL, McKay JK, Richards JH, Sen S, Wayne T, Juenger TE. 2012. Physiological genomics of response to soil drying in diverse Arabidopsis accessions. The Plant Cell 24, 893-914.
15. Donella DA, Mac Gowan CH, Cohen P, Marchiori F, Meyer HE, Pinna LA. 1990. An investigation of the substrate specifcity of protein phosphatase 2C using synthetic peptide substrates; comparison with protein phosphatase 2A. Biochimica et Biophysica Acta 1051, 199-202.
16. Duan L, Dietrich D, Ng CH, Chan PM, Bhalerao R, Bennett MJ, Dinneny JR. 2013. Endodermal ABA signalling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. The Plant Cell 25, 324-341.
17. Dupeux F, Antoni R, Betz K, et al. 2011b. Modulation of abscisic acid signalling in vivo by an engineered receptor-insensitive protein phosphatase type 2C allele. Plant Physiology 156, 106-116.
18. Dupeux F, Santiago J, Betz K, et al. 2011a. A thermodynamic switch modulates abscisic acid receptor sensitivity. EMBO Journal 30, 4171-4184.
19. Finkelstein R. 2013. Abscisic acid synthesis and response. Arabidopsis Book 11, e0166.
20. Hao Q, Yin P, Li W, Wang L, Yan C, Lin Z, Wu JZ, Wang J, Yan SF, Yan N. 2011. The molecular basis of ABA-independent inhibition of PP2Cs by a subclass of PYL proteins. Molecular Cell 42, 662-672.
21. Hauser F, Waadt R, Schroeder JI. 2011. Evolution of abscisic acid synthesis and signalling mechanisms. Current Biology 21, R346-R355.
22. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP. 2003. Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Research 31, e15.
23. Kim H, Hwang H, Hong JW, Lee YN, Ahn IP, Yoon IS, Yoo SD, Lee S, Lee SC, Kim BG. 2012. A rice orthologue of the ABA receptor, OsPYL/RCAR5, is a positive regulator of the ABA signal transduction pathway in seed germination and early seedling growth. Journal of Experimental Botany 63, 1013-1024.
24. Kim H, Lee K, Hwang H, Bhatnagar N, Kim DY, Yoon IS, Byun MO, Kim ST, Jung KH, Kim BG. 2014. Overexpression of PYL5 in rice enhances drought tolerance, inhibits growth, and modulates gene expression. Journal of Experimental Botany 65, 453-464.
25. Lackman P, Gonzalez-Guzman M, Tilleman S, et al. 2011. Jasmonate signalling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proceedings of the National Academy of Sciences, USA 108, 5891-5896.
26. 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.
27. Melcher K, Ng LM, Zhou XE, et al. 2009. A gate-latch-lock mechanism for hormone signalling by abscisic acid receptors. Nature 462, 602-608.
28. Miyazono K, Miyakawa T, Sawano Y, et al. 2009. Structural basis of abscisic acid signalling. Nature 462, 609-614.
29. Mosquna A, Peterson FC, Park SY, Lozano-Juste J, Volkman BF, Cutler SR. 2011. Potent and selective activation of abscisic acid receptors in vivo by mutational stabilization of their agonist-bound conformation. Proceedings of the National Academy of Sciences, USA 108, 20838-20843.
30. Nishimura N, Hitomi K, Arvai AS, Rambo RP, Hitomi C, Cutler SR, Schroeder JI, Getzoff ED. 2009. Structural mechanism of abscisic acid binding and signalling by dimeric PYR1. Science 326, 1373-1379.
31. Nishimura N, Sarkeshik A, Nito K, et al. 2010. PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. The Plant Journal 61, 290-299.
32. Okabe Y, Asamizu E, Ariizumi T, Shirasawa K, Tabata S, Ezura H. 2012. Availability of Micro-Tom mutant library combined with TILLING in molecular breeding of tomato fruit shelf-life. Breeding Science 62, 202-208.
33. Okamoto M, Peterson FC, Defries A, Park SY, Endo A, Nambara E, Volkman B F, Cutler SR. 2013. Activation of dimeric ABA receptors elicits guard cell closure, ABA-regulated gene expression, and drought tolerance. Proceedings of the National Academy of Sciences, USA 110, 12132-12137.
34. Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS. 2014. ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytologist 202, 35-49.
35. Park SY, 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.
36. Pizzio GA, Rodriguez L, Antoni R, Gonzalez-Guzman M, Yunta C, Merilo E, Kollist H, Albert A, Rodriguez PL. 2013. The PYL4 A194T mutant uncovers a key role of PYR1-LIKE4/PROTEIN PHOSPHATASE 2CA interaction for abscisic acid signalling and plant drought resistance. Plant Physiology 163, 441-455.
37. Powell AL, Nguyen CV, Hill T, et al. 2012. Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336, 1711-1715.
38. Rodrigues A, Adamo M, Crozet P, et al. 2013. ABI1 and PP2CA phosphatases are negative regulators of Snf1-related protein kinase1 signalling in Arabidopsis. The Plant Cell 25, 3871-3884.
39. Romero P, Lafuente MT, Rodrigo MJ. 2012. The Citrus ABA signalosome: identifcation and transcriptional regulation during sweet orange fruit ripening and leaf dehydration. Journal of Experimental Botany 63, 4931-4945.
40. Saavedra X, Modrego A, Rodriguez D, Gonzalez-Garcia MP, Sanz L, Nicolas G, Lorenzo O. 2010. The nuclear interactor PYL8/RCAR3 of Fagus sylvatica FsPP2C1 is a positive regulator of abscisic acid signalling in seeds and stress. Plant Physiology 152, 133-150.
41. Saez A, Robert N, Maktabi MH, Schroeder JI, Serrano R, Rodriguez PL. 2006. Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases type 2C ABI1 and HAB1. Plant Physiology 141, 1389-1399.
42. Saez A, Rodrigues A, Santiago J, Rubio S, Rodriguez PL. 2008. HAB1-SWI3B interaction reveals a link between abscisic acid signalling and putative SWI/SNF chromatin-remodeling complexes in Arabidopsis. The Plant Cell 20, 2972-2988.
43. Santiago J, Dupeux F, Round A, Antoni R, Park SY, Jamin M, Cutler SR, Rodriguez PL, Marquez JA. 2009b. The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462, 665-668.
44. Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park SY, Marquez JA, Cutler SR, Rodriguez PL. 2009a. Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. The Plant Journal 60, 575-588.
45. Sharp RE, LeNoble ME. 2002. ABA, ethylene, and the control of shoot and root growth under water stress. Journal of Experimental Botany 53, 33-37.
46. Sharp RE, Poroyko V, Hejlek LG, Spollen WG, Springer GK, Bohnert HJ, Nguyen HT. 2004. Root growth maintenance during water defcits: physiology to functional genomics. Journal of Experimental Botany 55, 2343-2351.
47. Shi JX, Adato A, Alkan N, et al. 2013. The tomato SlSHINE3 transcription factor regulates fruit cuticle formation and epidermal patterning. New Phytologist 197, 468-480.
48. Sun L, Sun Y, Zhang M, et al. 2012. Suppression of 9-cis-epoxycarotenoid dioxygenase, which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomato. Plant Physiology 158, 283-298.
49. Sun L, Wang YP, Chen P, Ren J, Ji K, Li Q, Li P, Dai SJ, Leng P. 2011. Transcriptional regulation of SlPYL, SlPP2C, and SlSnRK2 gene families encoding ABA signal core components during tomato fruit development and drought stress. Journal of Experimental Botany 62, 5659-5669.
50. Tomato Genome Consortium. 2012. The tomato genome sequence provides insights into feshy fruit evolution. Nature 485, 635-641.
51. Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Ishihama Y, Hirayama T, Shinozaki K. 2009. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proceedings of the National Academy of Sciences, USA 106, 17588-17593.
52. 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. The Plant Journal 45, 523-539.
53. Vlad F, Rubio S, Rodrigues A, Sirichandra C, Belin C, Robert N, Leung J, Rodriguez PL, Lauriere C, Merlot S. 2009. Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis. The Plant Cell 21, 3170-3184.
54. Wang ZY, Xiong L, Li W, Zhu JK, Zhu J. 2011. The plant cuticle is required for osmotic stress regulation of abscisic acid biosynthesis and osmotic stress tolerance in Arabidopsis. The Plant Cell 23, 1971-1984.
55. Wang Y, Tao X, Tang XM, Xiao L, Sun JL, Yan XF, Li D, Deng HY, Ma XR. 2013. Comparative transcriptome analysis of tomato (Solanum lycopersicum) in response to exogenous abscisic acid. BMC Genomics 14, 841.
56. 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.
57. Zhang M, Yuan B, Leng P. 2009. The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. Journal of Experimental Botany 60, 1579-1588.
58. Zhang X, Jiang L, Wang G, Yu L, Zhang Q, Xin Q, Wu W, Gong Z, Chen Z. 2013. Structural insights into the abscisic acid stereospecifcity by the ABA receptors PYR/PYL/RCAR. PLoS One 8, e67477.
59. Zhang X, Zhang Q, Xin Q, et al. 2012. Complex structures of the abscisic acid receptor PYL3/RCAR13 reveal a unique regulatory mechanism. Structure 20, 780-790.