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PMID: 26163575 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Aquaporins Contribute to ABA-Triggered Stomatal Closure through OST1-Mediated Phosphorylation.

The Plant cell ·Vol. 27 ·No. 7 ·2015-07-00 ·Pages 1945-54

Grondin A, Rodrigues O, Verdoucq L, Merlot S, Leonhardt N, Maurel C

Abstract

Stomatal movements in response to environmental stimuli critically control the plant water status. Although these movements are governed by osmotically driven changes in guard cell volume, the role of membrane water channels (aquaporins) has remained hypothetical. Assays in epidermal peels showed that knockout Arabidopsis thaliana plants lacking the Plasma membrane Intrinsic Protein 2;1 (PIP2;1) aquaporin have a defect in stomatal closure, specifically in response to abscisic acid (ABA). ABA induced a 2-fold increase in osmotic water permeability (Pf) of guard cell protoplasts and an accumulation of reactive oxygen species in guard cells, which were both abrogated in pip2;1 plants. Open stomata 1 (OST1)/Snf1-related protein kinase 2.6 (SnRK2.6), a protein kinase involved in guard cell ABA signaling, was able to phosphorylate a cytosolic PIP2;1 peptide at Ser-121. OST1 enhanced PIP2;1 water transport activity when coexpressed in Xenopus laevis oocytes. Upon expression in pip2;1 plants, a phosphomimetic form (Ser121Asp) but not a phosphodeficient form (Ser121Ala) of PIP2;1 constitutively enhanced the Pf of guard cell protoplasts while suppressing its ABA-dependent activation and was able to restore ABA-dependent stomatal closure in pip2;1. This work supports a model whereby ABA-triggered stomatal closure requires an increase in guard cell permeability to water and possibly hydrogen peroxide, through OST1-dependent phosphorylation of PIP2;1 at Ser-121.

MeSH Terms
Abscisic Acid/pharmacology Animals Aquaporins/metabolism Arabidopsis Proteins/metabolism Cell Membrane Permeability/drug effects Enzyme Activation/drug effects Genetic Complementation Test Movement/drug effects Mutation/genetics Oocytes/drug effects,metabolism Phosphorylation/drug effects Phosphoserine/metabolism Plant Stomata/cytology,drug effects,physiology Protein Kinases/metabolism Protoplasts/drug effects,metabolism Reactive Oxygen Species/metabolism Xenopus
Chemicals
Aquaporins Arabidopsis Proteins Reactive Oxygen Species plasma membrane intrinsic protein 2 Arabidopsis Phosphoserine Abscisic Acid Protein Kinases OST1 protein, Arabidopsis
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Grondin Alexandre ORCID
Biochimie et Physiologie Moléculaire des Plantes, Unité Mixte de Recherche 5004, CNRS/INRA/Montpellier SupAgro/Université Montpellier, F-34060 Montpellier, Cedex 2, France.
Rodrigues Olivier
Biochimie et Physiologie Moléculaire des Plantes, Unité Mixte de Recherche 5004, CNRS/INRA/Montpellier SupAgro/Université Montpellier, F-34060 Montpellier, Cedex 2, France.
Verdoucq Lionel
Biochimie et Physiologie Moléculaire des Plantes, Unité Mixte de Recherche 5004, CNRS/INRA/Montpellier SupAgro/Université Montpellier, F-34060 Montpellier, Cedex 2, France.
Merlot Sylvain
Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, Université Paris-Sud, Sciences Plant Saclay, F-91198 Gif sur Yvette Cedex, France.
Leonhardt Nathalie ORCID
Laboratoire de Biologie du Développement des Plantes, CEA Cadarache, Unité Mixte de Recherche 7265, CNRS/CEA/Aix-Marseille Université, F-13108 Saint-Paul-lez-Durance, France.
Maurel Christophe ORCID
Biochimie et Physiologie Moléculaire des Plantes, Unité Mixte de Recherche 5004, CNRS/INRA/Montpellier SupAgro/Université Montpellier, F-34060 Montpellier, Cedex 2, France maurel@supagro.inra.fr.
References (56)
56 references, click to expand
  1. Plant plasma membrane water channels conduct the signalling molecule H2O2.
    Biochem J. 2008 Aug 15;414(1):53-61 PMID: 18462192
  2. Expression of the Vicia faba VfPIP1 gene in Arabidopsis thaliana plants improves their drought resistance.
    J Plant Res. 2008 Mar;121(2):207-14 PMID: 18193401
  3. Subunit stoichiometry of a mammalian K+ channel determined by construction of multimeric cDNAs.
    Neuron. 1992 Nov;9(5):861-71 PMID: 1419000
  4. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase.
    FEBS Lett. 2009 Sep 17;583(18):2982-6 PMID: 19716822
  5. Membrane trafficking and osmotically induced volume changes in guard cells.
    J Exp Bot. 2006;57(15):4123-31 PMID: 17088361
  6. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  7. Stomatal action directly feeds back on leaf turgor: new insights into the regulation of the plant water status from non-invasive pressure probe measurements.
    Plant J. 2010 Jun 1;62(6):1072-82 PMID: 20345603
  8. The dual effect of abscisic acid on stomata.
    New Phytol. 2013 Jan;197(1):65-72 PMID: 23106390
  9. Osmotic signaling in plants: multiple pathways mediated by emerging kinase families.
    Plant Physiol. 2005 Jul;138(3):1185-94 PMID: 16009994
  10. Threonine at position 306 of the KAT1 potassium channel is essential for channel activity and is a target site for ABA-activated SnRK2/OST1/SnRK2.6 protein kinase.
    Biochem J. 2009 Dec 15;424(3):439-48 PMID: 19785574
  11. The Arabidopsis ABA-activated kinase OST1 phosphorylates the bZIP transcription factor ABF3 and creates a 14-3-3 binding site involved in its turnover.
    PLoS One. 2010;5(11):e13935 PMID: 21085673
  12. Abscisic acid and hydraulic conductivity of maize roots: a study using cell- and root-pressure probes.
    Planta. 2000 Nov;211(6):874-82 PMID: 11144273
  13. A versatile strategy to define the phosphorylation preferences of plant protein kinases and screen for putative substrates.
    Plant J. 2008 Jul;55(1):104-17 PMID: 18363786
  14. Differential tissue-specific expression of NtAQP1 in Arabidopsis thaliana reveals a role for this protein in stomatal and mesophyll conductance of CO₂ under standard and salt-stress conditions.
    Planta. 2014 Feb;239(2):357-66 PMID: 24170337
  15. Sucrose-induced receptor kinase SIRK1 regulates a plasma membrane aquaporin in Arabidopsis.
    Mol Cell Proteomics. 2013 Oct;12(10):2856-73 PMID: 23820729
  16. Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action.
    Proc Natl Acad Sci U S A. 2012 Jun 26;109(26):10593-8 PMID: 22689970
  17. Regulation of Arabidopsis leaf hydraulics involves light-dependent phosphorylation of aquaporins in veins.
    Plant Cell. 2013 Mar;25(3):1029-39 PMID: 23532070
  18. Structure-function analysis of plant aquaporin AtPIP2;1 gating by divalent cations and protons.
    Biochem J. 2008 Nov 1;415(3):409-16 PMID: 18637793
  19. Two TIP-like genes encoding aquaporins are expressed in sunflower guard cells.
    Plant J. 1997 Nov;12(5):1103-11 PMID: 9418051
  20. The Arabidopsis outward K+ channel GORK is involved in regulation of stomatal movements and plant transpiration.
    Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5549-54 PMID: 12671068
  21. The role of tobacco Aquaporin1 in improving water use efficiency, hydraulic conductivity, and yield production under salt stress.
    Plant Physiol. 2010 Jan;152(1):245-54 PMID: 19939947
  22. Heteromerization of PIP aquaporins affects their intrinsic permeability.
    Proc Natl Acad Sci U S A. 2014 Jan 7;111(1):231-6 PMID: 24367080
  23. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair.
    Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21425-30 PMID: 19955405
  24. Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate- and abscisic acid-induced stomatal closure.
    Plant Physiol. 2004 Apr;134(4):1536-45 PMID: 15064385
  25. In planta changes in protein phosphorylation induced by the plant hormone abscisic acid.
    Proc Natl Acad Sci U S A. 2010 Sep 7;107(36):15986-91 PMID: 20733066
  26. Guard cell volume and pressure measured concurrently by confocal microscopy and the cell pressure probe.
    Plant Physiol. 2001 Apr;125(4):1577-84 PMID: 11299339
  27. Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling.
    Annu Rev Plant Biol. 2010;61:561-91 PMID: 20192751
  28. A proteomic study reveals novel insights into the diversity of aquaporin forms expressed in the plasma membrane of plant roots.
    Biochem J. 2003 Jul 1;373(Pt 1):289-96 PMID: 12678916
  29. Bundle-sheath cell regulation of xylem-mesophyll water transport via aquaporins under drought stress: a target of xylem-borne ABA?
    Plant J. 2011 Jul;67(1):72-80 PMID: 21401747
  30. Spatiotemporal patterning of reactive oxygen production and Ca(2+) wave propagation in fucus rhizoid cells.
    Plant Cell. 2002 Oct;14(10):2369-81 PMID: 12368492
  31. A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells.
    Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21419-24 PMID: 19955427
  32. Auxin regulates aquaporin function to facilitate lateral root emergence.
    Nat Cell Biol. 2012 Oct;14(10):991-8 PMID: 22983115
  33. Guard-cell signalling for hydrogen peroxide and abscisic acid.
    New Phytol. 2008;178(4):703-18 PMID: 18373649
  34. Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba.
    Plant Physiol. 2001 Aug;126(4):1438-48 PMID: 11500543
  35. A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis.
    Plant Physiol. 2010 Mar;152(3):1418-30 PMID: 20034965
  36. Expression and characterization of plasma membrane aquaporins in stomatal complexes of Zea mays.
    Plant Mol Biol. 2014 Oct;86(3):335-50 PMID: 25082269
  37. Osmotic water permeability of isolated protoplasts. Modifications during development
    Plant Physiol. 1999 Mar;119(3):885-96 PMID: 10069827
  38. A brand new START: abscisic acid perception and transduction in the guard cell.
    Sci Signal. 2011;4(201):re4 PMID: 22126965
  39. Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid.
    Plant Physiol. 2001 Apr;125(4):1591-602 PMID: 11299341
  40. The vacuolar membrane protein gamma-TIP creates water specific channels in Xenopus oocytes.
    EMBO J. 1993 Jun;12(6):2241-7 PMID: 8508761
  41. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth.
    Nature. 2003 Mar 27;422(6930):442-6 PMID: 12660786
  42. The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots.
    Plant Physiol. 2005 Jan;137(1):341-53 PMID: 15591439
  43. Structural mechanism of plant aquaporin gating.
    Nature. 2006 Feb 9;439(7077):688-94 PMID: 16340961
  44. FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization.
    Proc Natl Acad Sci U S A. 2007 Jul 24;104(30):12359-64 PMID: 17636130
  45. An abscisic acid-independent oxylipin pathway controls stomatal closure and immune defense in Arabidopsis.
    PLoS Biol. 2013;11(3):e1001513 PMID: 23526882
  46. Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities.
    Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):8023-8 PMID: 20385816
  47. Phosphorylation of the vacuolar anion exchanger AtCLCa is required for the stomatal response to abscisic acid.
    Sci Signal. 2014;7(333):ra65 PMID: 25005229
  48. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation.
    Plant Mol Biol. 2000 Apr;42(6):819-32 PMID: 10890530
  49. Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO2 in vivo.
    Plant J. 2006 Nov;48(3):427-39 PMID: 17010114
  50. Microarray expression analyses of Arabidopsis guard cells and isolation of a recessive abscisic acid hypersensitive protein phosphatase 2C mutant.
    Plant Cell. 2004 Mar;16(3):596-615 PMID: 14973164
  51. Overexpression of the barley aquaporin HvPIP2;1 increases internal CO(2) conductance and CO(2) assimilation in the leaves of transgenic rice plants.
    Plant Cell Physiol. 2004 May;45(5):521-9 PMID: 15169933
  52. Specific plasma membrane aquaporins of the PIP1 subfamily are expressed in sieve elements and guard cells.
    Biol Cell. 2005 Jul;97(7):519-34 PMID: 15898953
  53. Kinetic analyses of plant water relocation using deuterium as tracer - reduced water flux of Arabidopsis pip2 aquaporin knockout mutants.
    Plant Biol (Stuttg). 2010 Sep;12 Suppl 1:129-39 PMID: 20712628
  54. Multiple phosphorylations in the C-terminal tail of plant plasma membrane aquaporins: role in subcellular trafficking of AtPIP2;1 in response to salt stress.
    Mol Cell Proteomics. 2008 Jun;7(6):1019-30 PMID: 18234664
  55. NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis.
    EMBO J. 2003 Jun 2;22(11):2623-33 PMID: 12773379
  56. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells.
    Nature. 2000 Aug 17;406(6797):731-4 PMID: 10963598
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1532-298X
Published
2015-07-00
Epub
2015-00-10
Pages
1945-54
Language
English
Region
England
NLM ID
9208688
PMCID
PMC4531361
Subset
IM
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