PYR/PYL/RCAR family members are major in‐vivo ABI1 protein phosphatase 2C‐interacting proteins in Arabidopsis

Abstract

Abscisic acid (ABA) mediates resistance to abiotic stress and controls developmental processes in plants. The group-A PP2Cs, of which ABI1 is the prototypical member, are protein phosphatases that play critical roles as negative regulators very early in ABA signal transduction. Because redundancy is thought to limit the genetic dissection of early ABA signalling, to identify redundant and early ABA signalling proteins, we pursued a proteomics approach. We generated YFP-tagged ABI1 Arabidopsis expression lines and identified in vivo ABI1-interacting proteins by mass-spectrometric analyses of ABI1 complexes. Known ABA signalling components were isolated including SnRK2 protein kinases. We confirm previous studies in yeast and now show that ABI1 interacts with the ABA-signalling kinases OST1, SnRK2.2 and SnRK2.3 in plants. Interestingly, the most robust in planta ABI1-interacting proteins in all LC-MS/MS experiments were nine of the 14 PYR/PYL/RCAR proteins, which were recently reported as ABA-binding signal transduction proteins, providing evidence for in vivo PYR/PYL/RCAR interactions with ABI1 in Arabidopsis. ABI1-PYR1 interaction was stimulated within 5 min of ABA treatment in Arabidopsis. Interestingly, in contrast, PYR1 and SnRK2.3 co-immunoprecipitated equally well in the presence and absence of ABA. To investigate the biological relevance of the PYR/PYLs, we analysed pyr1/pyl1/pyl2/pyl4 quadruple mutant plants and found strong insensitivities in ABA-induced stomatal closure and ABA-inhibition of stomatal opening. These findings demonstrate that ABI1 can interact with several PYR/PYL/RCAR family members in Arabidopsis, that PYR1-ABI1 interaction is rapidly stimulated by ABA in Arabidopsis and indicate new SnRK2 kinase-PYR/PYL/RCAR interactions in an emerging model for PYR/PYL/RCAR-mediated ABA signalling.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 59

1. 1.

   Allan AC, Fricker MD, Ward JL, Beale MH, Trewavas AJ. Two transduction pathways mediate rapid effects of abscisic acid in commelina guard cells. Plant Cell. 1994;6:1319-1328.

   Not in our library10.1105/tpc.6.9.1319

2. 2.

   Allen GJ, Kuchitsu K, Chu SP, Murata Y, Schroeder JI. Arabidopsis abi1-1 and abi2-1 phosphatase mutations reduce abscisic acid-induced cytoplasmic calcium rises in guard cells. Plant Cell. 1999;11:1785-1798.

   Not in our library10.1105/tpc.11.9.1785

3. 3.

   Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, Grill E, Schroeder JI. A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature. 2001;411:1053-1067.

   Not in our library10.1038/35082575

4. 4.

   Batistic O, Kudla J. Plant calcineurin B-like proteins and their interacting protein kinases. Biochim. Biophys. Acta. 2009;1793:985-992.

   Not in our library10.1016/j.bbamcr.2008.10.006

5. 5.

   Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1998;16:735-743.

   Not in our library10.1046/j.1365-313x.1998.00343.x

6. 6.

   Finkelstein RR, Gampala SS, Rock CD. Abscisic acid signalling in seeds and seedlings. Plant Cell. 2002;14:S15-S45.

   Not in our library10.1105/tpc.010441

7. 7.

   Fujii H, Zhu JK. Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction and stress. Proc. Natl Acad. Sci. USA. 2009;106:8380-8385.

   Not in our library10.1073/pnas.0903144106

8. 8.

   Fujii H, Verslues PE, Zhu JK. Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth and gene expression in Arabidopsis. Plant Cell. 2007;19:485-494.

   Not in our library10.1105/tpc.106.048538

9. 9.

   Furihata T, Maruyama K, Fujita Y, Umezawa T, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K. Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc. Natl Acad. Sci. USA. 2006;103:1988-1993.

   Not in our library10.1073/pnas.0505667103

10. 10.

    Goda H, Sasaki E, Akiyama K, et al. The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J. 2008;55:526-542.

    Not in our library10.1111/j.0960-7412.2008.03510.x

11. 11.

    Gosti F, Beaudoin N, Serizet C, Webb AA, Vartanian N, Giraudat J. ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signalling. Plant Cell. 1999;11:1897-1910.

    Not in our library10.1105/tpc.11.10.1897

12. 12.

    Guo Y, Xiong L, Song CP, Gong D, Halfter U, Zhu JK. A calcium sensor and its interacting protein kinase are global regulators of abscisic acid signalling in Arabidopsis. Dev. Cell. 2002;3:233-244.

    Not in our library10.1016/s1534-5807(02)00229-0

13. 13.

    Himmelbach A, Hoffmann T, Leube M, Hohener B, Grill E. Homeodomain protein ATHB6 is a target of the protein phosphatase ABI1 and regulates hormone responses in Arabidopsis. EMBO J. 2002;21:3029-3038.

    Not in our library10.1093/emboj/cdf316

14. 14.

    Hrabak EM, Chan CW, Gribskov M, et al. The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol. 2003;132:666-680.

    Not in our library10.1104/pp.102.011999

15. 15.

    Israelsson M, Siegel RS, Young J, Hashimoto M, Iba K, Schroeder JI. Guard cell ABA and CO2 signalling network updates and Ca2+ sensor priming hypothesis. Curr. Opin. Plant Biol. 2006;9:654-663.

    Not in our library10.1016/j.pbi.2006.09.006

16. 16.

    Koornneef M, Reulling G, Karssen C. The isolation and characterization of abscisic acid-insensitive mutants of Arabidopsis thaliana. Physiol. Plant. 1984;74:377-383.

    Not in our library

17. 17.

    Kuhn JM, Boisson-Dernier A, Dizon MB, Maktabi MH, Schroeder JI. The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in Arabidopsis and effects of abh1 on AtPP2CA mRNA. Plant Physiol. 2006;140:127-139.

    Not in our library10.1104/pp.105.070318

18. 18.

    Leonhardt N, Kwak JM, Robert N, Waner D, Leonhardt G, Schroeder JI. Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant. Plant Cell. 2004;16:596-615.

    Not in our library10.1105/tpc.019000

19. 19.

    Leung J, Bouvier-Durand M, Morris PC, Guerrier D, Chefdor F, Giraudat J. Arabidopsis ABA response gene ABI1: features of a calcium-modulated protein phosphatase. Science. 1994;264:1448-1452.

    Not in our library10.1126/science.7910981

20. 20.

    Leung J, Merlot S, Giraudat J. The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell. 1997;9:759-771.

    Not in our library10.1105/tpc.9.5.759

21. 21.

    Li J, Wang XQ, Watson MB, Assmann SM. Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase. Science. 2000;287:300-303.

    Not in our library10.1126/science.287.5451.300

22. 22.

    Luan S. The CBL–CIPK network in plant calcium signalling. Trends Plant Sci. 2009;14:37-42.

    Not in our library10.1016/j.tplants.2008.10.005

23. 23.

    Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E. Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science. 2009;324:1064-1068.

    Not in our library10.1126/science.1172408

24. 24.

    McCourt P, Creelman R. The ABA receptors—we report you decide. Curr. Opin. Plant Biol. 2008;11:474-478.

    Not in our library10.1016/j.pbi.2008.06.014

25. 25.

    Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J. The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J. 2001;25:295-303.

    Not in our library10.1046/j.1365-313x.2001.00965.x

26. 26.

    Merlot S, Leonhardt N, Fenzi F, et al. Constitutive activation of a plasma membrane H+-ATPase prevents abscisic acid-mediated stomatal closure. EMBO J. 2007;26:3216-3226.

    Not in our library10.1038/sj.emboj.7601750

27. 27.

    Meyer K, Leube MP, Grill E. A protein phosphatase 2C involved in ABA signal transduction in Arabidopsis thaliana. Science. 1994;264:1452-1455.

    Not in our library10.1126/science.8197457

28. 28.

    Miao Y, Lv D, Wang P, Wang XC, Chen J, Miao C, Song CP. An Arabidopsis glutathione peroxidase functions as both a redox transducer and a scavenger in abscisic acid and drought stress responses. Plant Cell. 2006;18:2749-2766.

    Not in our library10.1105/tpc.106.044230

29. 29.

    Mochizuki N, Brusslan JA, Larkin R, Nagatani A, Chory J. Arabidopsis genomes uncoupled 5 (GUN5) mutant reveals the involvement of Mg-chelatase H subunit in plastid-to-nucleus signal transduction. Proc. Natl Acad. Sci. USA. 2001;98:2053-2058.

    Not in our library10.1073/pnas.98.4.2053

30. 30.

    Moes D, Himmelbach A, Korte A, Haberer G, Grill E. Nuclear localization of the mutant protein phosphatase abi1 is required for insensitivity towards ABA responses in Arabidopsis. Plant J. 2008;54:806-819.

    Not in our library10.1111/j.1365-313x.2008.03454.x

31. 31.
    CDPKs CPK6 and CPK3 Function in ABA Regulation of Guard Cell S-Type Anion- and Ca2+- Permeable Channels and Stomatal Closure · 2006

    No notice
32. 32.

    Murata Y, Pei ZM, Mori IC, Schroeder J. Abscisic acid activation of plasma membrane Ca2+ channels in guard cells requires cytosolic NAD(P)H and is differentially disrupted upstream and downstream of reactive oxygen species production in abi1-1 and abi2-1 protein phosphatase 2C mutants. Plant Cell. 2001;13:2513-2523.

    Not in our library10.1105/tpc.010210

33. 33.

    Mustilli AC, Merlot S, Vavasseur A, Fenzi F, Giraudat J. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell. 2002;14:3089-3099.

    Not in our library10.1105/tpc.007906

34. 34.

    Nakashima K, Fujita Y, Kanamori N, et al. Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signalling are essential for the control of seed development and dormancy. Plant Cell Physiol. 2009;50:1345-1363.

    Not in our library10.1093/pcp/pcp083

35. 35.

    Nambara E, Marion-Poll A. Abscisic acid biosynthesis and catabolism. Annu. Rev. Plant Biol. 2005;56:165-185.

    Not in our library10.1146/annurev.arplant.56.032604.144046

36. 36.

    Negi J, Matsuda O, Nagasawa T, Oba Y, Takahashi H, Kawai-Yamada M, Uchimiya H, Hashimoto M, Iba K. CO2 regulator SLAC1 and its homologs are essential for anion homeostasis in plant cells. Nature. 2008;452:483-486.

    Not in our library10.1038/nature06720

37. 37.

    Nishimura N, Yoshida T, Murayama M, Asami T, Shinozaki K, Hirayama T. Isolation and characterization of novel mutants affecting the abscisic acid sensitivity of Arabidopsis germination and seedling growth. Plant Cell Physiol. 2004;45:1485-1499.

    Not in our library10.1093/pcp/pch171

38. 38.

    Nishimura N, Yoshida T, Kitahata N, Asami T, Shinozaki K, Hirayama T. ABA-Hypersensitive Germination1 encodes a protein phosphatase 2C, an essential component of abscisic acid signalling in Arabidopsis seed. Plant J. 2007;50:935-949.

    Not in our library10.1111/j.1365-313x.2007.03107.x

39. 39.

    Ohta M, Guo Y, Halfter U, Zhu JK. A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc. Natl Acad. Sci. USA. 2003;100:11771-11776.

    Not in our library10.1073/pnas.2034853100

40. 40.

    Pandey S, Nelson DC, Assmann SM. Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis. Cell. 2009;136:136-148.

    Not in our library10.1016/j.cell.2008.12.026

Cited by papers we hold 16

• ABSCISIC ACID INSENSITIVE5 Interacts With RIBOSOMAL S6 KINASE2 to Mediate ABA Responses During Seedling Growth in Arabidopsis · 2021
  Not checked
• Functional Study of BpPP2C1 Revealed Its Role in Salt Stress in Betula platyphylla · 2021
  Not checked
• Control of seed dormancy and germination by DOG1-AHG1 PP2C phosphatase complex via binding to heme · 2018
  No notice
• Overexpression of the PeaT1 Elicitor Gene from Alternaria tenuissima Improves Drought Tolerance in Rice Plants via Interaction with a Myo-Inositol Oxygenase · 2017
  Not checked
• Post‐translational control of ABA signalling: the roles of protein phosphorylation and ubiquitination · 2016
  No notice
• Abscisic Acid and Abiotic Stress Tolerance in Crop Plants · 2016
  No notice
• An ABA-increased interaction of the PYL6 ABA receptor with MYC2 Transcription Factor: A putative link of ABA and JA signaling · 2016
  Corrected
• Calcium specificity signaling mechanisms in abscisic acid signal transduction in Arabidopsis guard cells · 2015
  Corrected
• Elevated CO 2 -Induced Responses in Stomata Require ABA and ABA Signaling · 2015
  No notice
• 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 · 2014
  No notice
• OPT3 Is a Component of the Iron-Signaling Network between Leaves and Roots and Misregulation of OPT3 Leads to an Over-Accumulation of Cadmium in Seeds · 2014
  No notice
• FRET-based reporters for the direct visualization of abscisic acid concentration changes and distribution in Arabidopsis · 2014
  No notice
• Cytokinin cross-talking during biotic and abiotic stress responses · 2013
  No notice
• Open or Close the Gate – Stomata Action Under the Control of Phytohormones in Drought Stress Conditions · 2013
  No notice
• Common and unique elements of the ABA-regulated transcriptome of Arabidopsis guard cells · 2011
  No notice
• The Arabidopsis ABA-Activated Kinase OST1 Phosphorylates the bZIP Transcription Factor ABF3 and Creates a 14-3-3 Binding Site Involved in Its Turnover · 2010
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.