title: Control of vacuolar dynamics and regulation of stomatal aperture by tonoplast potassium uptake.
abstract: Stomatal movements rely on alterations in guard cell turgor. This requires massive K(+) bidirectional fluxes across the plasma and tonoplast membranes. Surprisingly, given their physiological importance, the transporters mediating the energetically uphill transport of K(+) into the vacuole remain to be identified. Here, we report that, in Arabidopsis guard cells, the tonoplast-localized K(+)/H(+) exchangers NHX1 and NHX2 are pivotal in the vacuolar accumulation of K(+) and that nhx1 nhx2 mutant lines are dysfunctional in stomatal regulation. Hypomorphic and complete-loss-of-function double mutants exhibited significantly impaired stomatal opening and closure responses. Disruption of K(+) accumulation in guard cells correlated with more acidic vacuoles and the disappearance of the highly dynamic remodelling of vacuolar structure associated with stomatal movements. Our results show that guard cell vacuolar accumulation of K(+) is a requirement for stomatal opening and a critical component in the overall K(+) homeostasis essential for stomatal closure, and suggest that vacuolar K(+) fluxes are also of decisive importance in the regulation of vacuolar dynamics and luminal pH that underlie stomatal movements.
authors.affiliation: Instituto de Recursos Naturales y Agrobiologia de Sevilla, Consejo Superior de Investigaciones Cientificas, 41012 Seville, Spain.
authors.forename: Zaida
authors.initials: Z
authors.lastname: Andrés
authors.forename: Javier
authors.initials: J
authors.lastname: Pérez-Hormaeche
authors.forename: Eduardo O
authors.initials: EO
authors.lastname: Leidi
authors.forename: Kathrin
authors.initials: K
authors.lastname: Schlücking
authors.forename: Leonie
authors.initials: L
authors.lastname: Steinhorst
authors.forename: Deirdre H
authors.initials: DH
authors.lastname: McLachlan
authors.forename: Karin
authors.initials: K
authors.lastname: Schumacher
authors.forename: Alistair M
authors.initials: AM
authors.lastname: Hetherington
authors.forename: Jörg
authors.initials: J
authors.lastname: Kudla
authors.forename: Beatriz
authors.initials: B
authors.lastname: Cubero
authors.forename: José M
authors.initials: JM
authors.lastname: Pardo
mesh_terms: D000143:Acids / Q000378:metabolism; D017360:Arabidopsis / Q000166:cytology / Q000187:drug effects / Q000235:genetics / Q000502:physiology*; D029681:Arabidopsis Proteins / Q000235:genetics; D027682:Cation Transport Proteins / Q000235:genetics; D002412:Cations / Q000378:metabolism; D048430:Cell Shape / Q000187:drug effects; D002940:Circadian Rhythm / Q000187:drug effects / Q000235:genetics; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D021621:Imaging, Three-Dimensional; D007259:Infrared Rays; D007425:Intracellular Membranes / Q000378:metabolism*; D009068:Movement; D009154:Mutation / Q000235:genetics; D054046:Plant Stomata / Q000166:cytology / Q000187:drug effects / Q000235:genetics / Q000502:physiology*; D018526:Plant Transpiration / Q000187:drug effects / Q000502:physiology; D011188:Potassium / Q000378:metabolism*; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D012964:Sodium / Q000494:pharmacology; D017923:Sodium-Hydrogen Exchangers / Q000235:genetics; D012987:Soil; D013817:Thermography; D014617:Vacuoles / Q000187:drug effects / Q000235:genetics / Q000378:metabolism*; D014867:Water
chemical_list: D000143:Acids; D029681:Arabidopsis Proteins; D027682:Cation Transport Proteins; D002412:Cations; C117751:NHX1 protein, Arabidopsis; D012333:RNA, Messenger; D017923:Sodium-Hydrogen Exchangers; D012987:Soil; D014867:Water; D012964:Sodium; D011188:Potassium
keywords: luminal pH control; stomata
references.citation: Mol Plant. 2011 May;4(3):428-41
references.pmid: 21459829
references.citation: Philos Trans R Soc Lond B Biol Sci. 1998 Sep 29;353(1374):1475-88
references.pmid: 9800209
references.citation: Plant Cell Environ. 2013 Feb;36(2):484-97
references.pmid: 22891733
references.citation: Plant J. 2010 Nov;64(4):563-76
references.pmid: 20822503
references.citation: Plant Physiol. 2003 Nov;133(3):1314-21
references.pmid: 14551331
references.citation: Plant Physiol. 2012 Jul;159(3):1235-51
references.pmid: 22635112
references.citation: Mol Plant. 2010 Mar;3(2):280-7
references.pmid: 20339156
references.citation: J Cell Sci. 2010 Oct 1;123(Pt 19):3266-75
references.pmid: 20826459
references.citation: Annu Rev Plant Biol. 2010;61:561-91
references.pmid: 20192751
references.citation: Plant J. 2002 Jun;30(5):601-9
references.pmid: 12047634
references.citation: Plant Cell Physiol. 2010 Feb;51(2):302-11
references.pmid: 20061305
references.citation: Nature. 2005 Mar 17;434(7031):404-8
references.pmid: 15772667
references.citation: New Phytol. 2005 Sep;167(3):665-91
references.pmid: 16101906
references.citation: Plant Mol Biol. 2002 Oct;50(3):543-50
references.pmid: 12369629
references.citation: Nature. 2000 Aug 17;406(6797):731-4
references.pmid: 10963598
references.citation: Plant Physiol. 2004 Apr;134(4):1536-45
references.pmid: 15064385
references.citation: Plant Cell. 2011 Sep;23(9):3482-97
references.pmid: 21954467
references.citation: PLoS Biol. 2007 Aug;5(8):e222
references.pmid: 17683202
references.citation: FEBS Lett. 2010 May 17;584(10):1982-8
references.pmid: 20188732
references.citation: Plant Physiol. 2013 Oct;163(2):591-9
references.pmid: 23922271
references.citation: Plant Physiol. 1969 Feb;44(2):230-4
references.pmid: 16657051
references.citation: Gene. 1996;173(1 Spec No):33-8
references.pmid: 8707053
references.citation: Plant Physiol. 1996 Aug;111(4):1051-1057
references.pmid: 12226347
references.citation: Plant J. 2010 Feb 1;61(3):495-506
references.pmid: 19912566
references.citation: New Phytol. 2013 Jan;197(1):88-98
references.pmid: 23126621
references.citation: Plant Cell Physiol. 2006 Mar;47(3):332-9
references.pmid: 16418232
references.citation: Nat Commun. 2013;4:1804
references.pmid: 23653216
references.citation: Science. 2007 Dec 14;318(5857):1789-92
references.pmid: 18084825
references.citation: Plant J. 2010 Jun 1;62(6):1072-82
references.pmid: 20345603
references.citation: Plant J. 2005 Feb;41(4):606-14
references.pmid: 15686523
references.citation: Plant Cell Physiol. 2007 Aug;48(8):1159-69
references.pmid: 17602189
references.citation: Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):8023-8
references.pmid: 20385816
references.citation: Proc Natl Acad Sci U S A. 2006 Jan 24;103(4):1135-40
references.pmid: 16418285
references.citation: Annu Rev Plant Biol. 2012;63:183-213
references.pmid: 22404463
references.citation: Proc Natl Acad Sci U S A. 2012 Jun 26;109(26):10593-8
references.pmid: 22689970
references.citation: Plant Physiol. 2001 Apr;125(4):1577-84
references.pmid: 11299339
references.citation: Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21425-30
references.pmid: 19955405
references.citation: Plant Cell. 2013 Sep;25(9):3434-49
references.pmid: 24014545
references.citation: Proc Natl Acad Sci U S A. 1996 Sep 17;93(19):10510-4
references.pmid: 11607707
references.citation: Plant Physiol. 2005 Nov;139(3):1207-16
references.pmid: 16244153
references.citation: BMC Bioinformatics. 2010 May 21;11:274
references.pmid: 20492697
references.citation: Science. 2010 Jun 11;328(5984):1401-3
references.pmid: 20430974
references.citation: Plant Cell. 2013 Jun;25(6):2202-16
references.pmid: 23757398
references.citation: Proc Natl Acad Sci U S A. 2008 Apr 1;105(13):5271-6
references.pmid: 18367672
references.citation: Proc Natl Acad Sci U S A. 2007 Jun 19;104(25):10726-31
references.pmid: 17563365
references.citation: New Phytol. 2003 Nov;160(2):281-303
references.pmid: 33832173
references.citation: Plant Cell. 2012 Mar;24(3):1127-42
references.pmid: 22438021
references.citation: Physiol Rev. 2012 Oct;92(4):1777-811
references.pmid: 23073631
references.citation: Plant Physiol. 2012 Dec;160(4):1956-67
references.pmid: 23090586