The PYL4 A194T mutant uncovers a key role of PYR1-LIKE4/PROTEIN PHOSPHATASE 2CA interaction for abscisic acid signaling and plant drought resistance

Plant Physiology

Volumn 163, Issue 1, 2013, Pages 441-455

  Pizzio, Gaston A ^a   Rodriguez, Lesia ^a   Antoni, Regina ^a   Gonzalez Guzman, Miguel ^a   Yunta, Cristina ^b   Merilo, Ebe ^c   Kollist, Hannes ^c   Albert, Armando ^b   Rodriguez, Pedro L ^a  

^a CSIC   (Spain)

^b INSTITUTO DE QUÍMICA FÍSICA ROCASOLANO   (Spain)

^c UNIVERSITY OF TARTU   (Estonia)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ABSCISIC ACID; AHG3 PROTEIN, ARABIDOPSIS; ARABIDOPSIS PROTEIN; CELL SURFACE RECEPTOR; PHOSPHOPROTEIN PHOSPHATASE; PYL4 PROTEIN, ARABIDOPSIS; WATER;

AMINO ACID SEQUENCE; ARTICLE; DROUGHT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSGENIC PLANT;

ABSCISIC ACID; AMINO ACID SEQUENCE; ARABIDOPSIS PROTEINS; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; MUTATION; PHOSPHOPROTEIN PHOSPHATASES; PLANTS, GENETICALLY MODIFIED; PROTEIN INTERACTION MAPS; RECEPTORS, CELL SURFACE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; WATER;

EID: 84883255166     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.113.224162     Document Type: Article

References (44)

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 Physiol 158: 970-980
2. Antoni R, Gonzalez-Guzman M, Rodriguez L, Peirats-Llobet M, Pizzio GA, Fernandez MA, De Winne N, De Jaeger G, Dietrich D, Bennett MJ, et al (2013) PYRABACTIN RESISTANCE1-LIKE8 plays an important role for the regulation of abscisic acid signaling in root. Plant Physiol 161: 931-941
3. Barrero JM, Piqueras P, González-Guzmán M, Serrano R, Rodríguez PL, Ponce MR, Micol JL (2005) A mutational analysis of the ABA1 gene of Arabidopsis thaliana highlights the involvement of ABA in vegetative development. J Exp Bot 56: 2071-2083
4. Belda-Palazón B, Ruiz L, Martí E, Tárraga S, Tiburcio AF, Culiáñez F, Farràs R, Carrasco P, Ferrando A (2012) Aminopropyltransferases involved in polyamine biosynthesis localize preferentially in the nucleus of plant cells. PLoS ONE 7: e46907
5. 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 Lett 561: 127-131
6. Bhaskara GB, Nguyen TT, Verslues PE (2012) Unique drought resistance functions of the highly ABA-induced clade A protein phosphatase 2Cs. Plant Physiol 160: 379-395
7. Chitrakar R, MelottoM(2010) Assessing stomatal response to live bacterial cells using whole leaf imaging. J Vis Exp 44: e2185
8. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61: 651-679
9. Deblaere R, Bytebier B, De Greve H, Deboeck F, Schell J, Van Montagu M, Leemans J (1985) Efficient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants. Nucleic Acids Res 13: 4777-4788
10. Dupeux F, Antoni R, Betz K, Santiago J, Gonzalez-Guzman M, Rodriguez L, Rubio S, Park SY, Cutler SR, Rodriguez PL, et al (2011b) Modulation of abscisic acid signaling in vivo by an engineered receptor-insensitive protein phosphatase type 2C allele. Plant Physiol 156: 106-116
11. Dupeux F, Santiago J, Betz K, Twycross J, Park SY, Rodriguez L, Gonzalez-Guzman M, Jensen MR, Krasnogor N, Blackledge M, et al (2011a) A thermodynamic switch modulates abscisic acid receptor sensitivity. EMBO J 30: 4171-4184
12. Fujii H, Chinnusamy V, Rodrigues A, Rubio S, Antoni R, Park SY, Cutler SR, Sheen J, Rodriguez PL, Zhu JK (2009) In vitro reconstitution of an abscisic acid signalling pathway. Nature 462: 660-664
13. Gampala SS, Kim TW, He JX, Tang W, Deng Z, Bai MY, Guan S, Lalonde S, Sun Y, Gendron JM, et al (2007) An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev Cell 13: 177-189
14. Gonzalez-Guzman M, Pizzio GA, Antoni R, Vera-Sirera F, Merilo E, Bassel GW, Fernández MA, Holdsworth MJ, Perez-Amador MA, Kollist H, et al (2012) Arabidopsis PYR/PYL/RCAR receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid. Plant Cell 24: 2483-2496
15. 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. Mol Cell 42: 662-672
16. Hugouvieux V, Kwak JM, Schroeder JI (2001) An mRNA cap binding protein, ABH1, modulates early abscisic acid signal transduction in Arabidopsis. Cell 106: 477-487
17. Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27: 325-333
18. Jakab G, Ton J, Flors V, Zimmerli L, Métraux JP, Mauch-Mani B (2005) Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiol 139: 267-274
19. Kollist T, Moldau H, Rasulov B, Oja V, Ramma H, Huve K, Jaspers P, Kangasjarvi J, Kollist H (2007) A novel device detects a rapid ozoneinduce transient stomatal closure in intact Arabidopsis and its absence in abi2 mutant. Physiol Plant 129: 796-803
20. Kuhn JM, Boisson-Dernier A, Dizon MB, Maktabi MH, Schroeder JI (2006) The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in Arabidopsis, and effects of abh1 on AtPP2CA mRNA. Plant Physiol 140: 127-139
21. Lackman P, González-Guzmán M, Tilleman S, Carqueijeiro I, Pérez AC, Moses T, Seo M, Kanno Y, Häkkinen ST, Van Montagu MC, et al (2011) Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proc Natl Acad Sci USA 108: 5891-5896
22. Lee SC, Lan W, Buchanan BB, Luan S (2009) A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells. Proc Natl Acad Sci USA 106: 21419-21424
23. 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
24. 2-induced stomatal regulation. Plant Physiol 162: 1652-1668
25. 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. Proc Natl Acad Sci USA 108: 20838-20843
26. Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow TFF, et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324: 1068-1071
27. Pei ZM, Ghassemian M, Kwak CM, McCourt P, Schroeder JI (1998) Role of farnesyltransferase in ABA regulation of guard cell anion channels and plant water loss. Science 282: 287-290
28. Qin X, Zeevaart JA (2002) Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol 128: 544-551
29. Saavedra X, Modrego A, Rodríguez D, González-García MP, Sanz L, Nicolás G, Lorenzo O (2010) The nuclear interactor PYL8/RCAR3 of Fagus sylvatica FsPP2C1 is a positive regulator of abscisic acid signaling in seeds and stress. Plant Physiol 152: 133-150
30. 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. Plant J 37: 354-369
31. 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 Physiol 141: 1389-1399
32. Saez A, Rodrigues A, Santiago J, Rubio S, Rodriguez PL (2008) HAB1-SWI3B interaction reveals a link between abscisic acid signaling and putative SWI/SNF chromatin-remodeling complexes in Arabidopsis. Plant Cell 20: 2972-2988
33. Santiago J, Dupeux F, Betz K, Antoni R, Gonzalez-Guzman M, Rodriguez L, Márquez JA, Rodriguez PL (2012) Structural insights into PYR/PYL/ RCAR ABA receptors and PP2Cs. Plant Sci 182: 3-11
34. Santiago J, Dupeux F, Round A, Antoni R, Park SY, Jamin M, Cutler SR, Rodriguez PL, Márquez JA (2009a) The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462: 665-668
35. Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park SY, Márquez JA, Cutler SR, Rodriguez PL (2009b) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J 60: 575-588
36. Soon FF, Ng LM, Zhou XE, West GM, Kovach A, Tan MH, Suino-Powell KM, He Y, Xu Y, ChalmersMJ, et al (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335: 85-88
37. 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. Plant J 61: 25-35
38. Tallman G (2004) Are diurnal patterns of stomatal movement the result of alternating metabolism of endogenous guard cell ABA and accumulation of ABA delivered to the apoplast around guard cells by transpiration? J Exp Bot 55: 1963-1976
39. Vahisalu T, Kollist H, Wang YF, Nishimura N, Chan WY, Valerio G, Lamminmäki A, Brosché M, Moldau H, Desikan R, et al (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452: 487-491
40. Vahisalu T, Puzõrjova I, Brosché M, Valk E, Lepiku M, Moldau H, Pechter P, Wang YS, Lindgren O, Salojärvi J, et al (2010) Ozonetriggered rapid stomatal response involves the production of reactive oxygen species, and is controlled by SLAC1 and OST1. Plant J 62: 442-453
41. Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33: 949-956
42. Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C, et al (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40: 428-438
43. 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 signaling during germination among Arabidopsis protein phosphatase 2Cs. Plant Physiol 140: 115-126
44. Zhang X, Zhang Q, Xin Q, Yu L, Wang Z, Wu W, Jiang L, Wang G, TianW, Deng Z, et al (2012) Complex structures of the abscisic acid receptor PYL3/ RCAR13 reveal a unique regulatory mechanism. Structure 20: 780-790