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PMID: 28986421 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Stomatal VPD Response: There Is More to the Story Than ABA.

Plant physiology ·Vol. 176 ·No. 1 ·2018-00-00 ·Pages 851-864

Merilo E, Yarmolinsky D, Jalakas P, Parik H, Tulva I, Rasulov B, Kilk K, Kollist H

Abstract

Guard cells shrink and close stomatal pores when air humidity decreases (i.e. when the difference between the vapor pressures of leaf and atmosphere [VPD] increases). The role of abscisic acid (ABA) in VPD-induced stomatal closure has been studied using ABA-related mutants that respond to VPD in some studies and not in others. The importance of ABA biosynthesis in guard cells versus vasculature for whole-plant stomatal regulation is unclear as well. Here, we show that Arabidopsis (Arabidopsis thaliana) lines carrying mutations in different steps of ABA biosynthesis as well as pea (Pisum sativum) wilty and tomato (Solanum lycopersicum) flacca ABA-deficient mutants had higher stomatal conductance compared with wild-type plants. To characterize the role of ABA production in different cells, we generated transgenic plants where ABA biosynthesis was rescued in guard cells or phloem companion cells of an ABA-deficient mutant. In both cases, the whole-plant stomatal conductance, stunted growth phenotype, and leaf ABA level were restored to wild-type values, pointing to the redundancy of ABA sources and to the effectiveness of leaf ABA transport. All ABA-deficient lines closed their stomata rapidly and extensively in response to high VPD, whereas plants with mutated protein kinase OST1 showed stunted VPD-induced responses. Another strongly ABA-insensitive mutant, defective in the six ABA PYR/RCAR receptors, responded to changes in VPD in both directions strongly and symmetrically, indicating that its VPD-induced closure could be passive hydraulic. We discuss that both the VPD-induced passive hydraulic stomatal closure and the stomatal VPD regulation of ABA-deficient mutants may be conditional on the initial pretreatment stomatal conductance.

MeSH Terms
Abscisic Acid/metabolism,pharmacology Air Arabidopsis/cytology,drug effects,genetics,physiology Biosynthetic Pathways/drug effects Green Fluorescent Proteins/metabolism Humidity Models, Biological Mutation/genetics Phenotype Phloem/cytology,drug effects Plant Stomata/cytology,drug effects,physiology Plants, Genetically Modified Signal Transduction/drug effects Vapor Pressure
Chemicals
Green Fluorescent Proteins Abscisic Acid
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Merilo Ebe ORCID
Plant Signal Research Group, Institute of Technology, University of Tartu, Tartu 50411, Estonia ebe.merilo@ut.ee.
Yarmolinsky Dmitry ORCID
Plant Signal Research Group, Institute of Technology, University of Tartu, Tartu 50411, Estonia.
Jalakas Pirko
Plant Signal Research Group, Institute of Technology, University of Tartu, Tartu 50411, Estonia.
Parik Helen ORCID
Plant Signal Research Group, Institute of Technology, University of Tartu, Tartu 50411, Estonia.
Tulva Ingmar
Plant Signal Research Group, Institute of Technology, University of Tartu, Tartu 50411, Estonia.
Rasulov Bakhtier
Plant Signal Research Group, Institute of Technology, University of Tartu, Tartu 50411, Estonia.
Kilk Kalle ORCID
Institute of Biomedicine and Translational Medicine, Faculty of Medicine, University of Tartu, Tartu 50411, Estonia.
Kollist Hannes ORCID
Plant Signal Research Group, Institute of Technology, University of Tartu, Tartu 50411, Estonia.
References (68)
68 references, click to expand
  1. Arabidopsis thaliana floral dip transformation method.
    Methods Mol Biol. 2006;343:87-103 PMID: 16988336
  2. Fern Stomatal Responses to ABA and CO2 Depend on Species and Growth Conditions.
    Plant Physiol. 2017 Jun;174(2):672-679 PMID: 28351911
  3. The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) heynh.
    Theor Appl Genet. 1982 Dec;61(4):385-93 PMID: 24270501
  4. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins.
    Science. 2009 May 22;324(5930):1068-71 PMID: 19407142
  5. Identification of features regulating OST1 kinase activity and OST1 function in guard cells.
    Plant Physiol. 2006 Aug;141(4):1316-27 PMID: 16766677
  6. Different phosphorylation mechanisms are involved in the activation of sucrose non-fermenting 1 related protein kinases 2 by osmotic stresses and abscisic acid.
    Plant Mol Biol. 2007 Mar;63(4):491-503 PMID: 17103012
  7. The control of stomata by water balance.
    New Phytol. 2005 Nov;168(2):275-92 PMID: 16219068
  8. Central functions of bicarbonate in S-type anion channel activation and OST1 protein kinase in CO2 signal transduction in guard cell.
    EMBO J. 2011 Apr 20;30(8):1645-58 PMID: 21423149
  9. Closely related receptor complexes differ in their ABA selectivity and sensitivity.
    Plant J. 2010 Jan;61(1):25-35 PMID: 19769575
  10. Land plants acquired active stomatal control early in their evolutionary history.
    Curr Biol. 2011 Jun 21;21(12):1030-5 PMID: 21658945
  11. Stomatal responses to vapour pressure deficit are regulated by high speed gene expression in angiosperms.
    Plant Cell Environ. 2016 Mar;39(3):485-91 PMID: 26353082
  12. PYR/RCAR receptors contribute to ozone-, reduced air humidity-, darkness-, and CO2-induced stomatal regulation.
    Plant Physiol. 2013 Jul;162(3):1652-68 PMID: 23703845
  13. Sulphate as a xylem-borne chemical signal precedes the expression of ABA biosynthetic genes in maize roots.
    J Exp Bot. 2010 Jul;61(12):3395-405 PMID: 20566566
  14. Two new alleles of the abscisic aldehyde oxidase 3 gene reveal its role in abscisic acid biosynthesis in seeds.
    Plant Physiol. 2004 May;135(1):325-33 PMID: 15122034
  15. The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis.
    Proc Natl Acad Sci U S A. 1991 Sep 1;88(17):7496-9 PMID: 11607209
  16. Phosphatidic acid inhibits blue light-induced stomatal opening via inhibition of protein phosphatase 1 [corrected].
    Plant Physiol. 2010 Aug;153(4):1555-62 PMID: 20498335
  17. The dual effect of abscisic acid on stomata.
    New Phytol. 2013 Jan;197(1):65-72 PMID: 23106390
  18. Light regulation of stomatal movement.
    Annu Rev Plant Biol. 2007;58:219-47 PMID: 17209798
  19. The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis.
    Curr Biol. 2013 Jan 7;23(1):53-7 PMID: 23219726
  20. Regulators of PP2C phosphatase activity function as abscisic acid sensors.
    Science. 2009 May 22;324(5930):1064-8 PMID: 19407143
  21. ABA inhibits entry into stomatal-lineage development in Arabidopsis leaves.
    Plant J. 2013 May;74(3):448-57 PMID: 23373882
  22. The regulatory domain of SRK2E/OST1/SnRK2.6 interacts with ABI1 and integrates abscisic acid (ABA) and osmotic stress signals controlling stomatal closure in Arabidopsis.
    J Biol Chem. 2006 Feb 24;281(8):5310-8 PMID: 16365038
  23. Shoot-derived abscisic acid promotes root growth.
    Plant Cell Environ. 2016 Mar;39(3):652-9 PMID: 26514625
  24. The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin to abscisic aldehyde.
    Plant Cell. 2002 Aug;14(8):1833-46 PMID: 12172025
  25. The Arabidopsis ABA-deficient mutant aba4 demonstrates that the major route for stress-induced ABA accumulation is via neoxanthin isomers.
    Plant J. 2007 Jun;50(5):810-24 PMID: 17470058
  26. Abscisic acid signal transduction in guard cells is mediated by phospholipase D activity.
    Proc Natl Acad Sci U S A. 1999 Oct 12;96(21):12192-7 PMID: 10518598
  27. Evolutionary Conservation of ABA Signaling for Stomatal Closure.
    Plant Physiol. 2017 Jun;174(2):732-747 PMID: 28232585
  28. The evolution of mechanisms driving the stomatal response to vapor pressure deficit.
    Plant Physiol. 2015 Mar;167(3):833-43 PMID: 25637454
  29. Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying.
    J Exp Bot. 2002 Jun;53(373):1503-14 PMID: 12021298
  30. Linking Turgor with ABA Biosynthesis: Implications for Stomatal Responses to Vapor Pressure Deficit across Land Plants.
    Plant Physiol. 2016 Jul;171(3):2008-16 PMID: 27208264
  31. Inhibition of blue light-dependent H+ pumping by abscisic acid through hydrogen peroxide-induced dephosphorylation of the plasma membrane H+-ATPase in guard cell protoplasts.
    Plant Physiol. 2004 Dec;136(4):4150-8 PMID: 15563626
  32. Passive origins of stomatal control in vascular plants.
    Science. 2011 Feb 4;331(6017):582-5 PMID: 21163966
  33. Engineered GFP as a vital reporter in plants.
    Curr Biol. 1996 Mar 1;6(3):325-30 PMID: 8805250
  34. Molecular characterization of a mutation affecting abscisic acid biosynthesis and consequently stomatal responses to humidity in an agriculturally important species.
    AoB Plants. 2015 Jul 27;7:null PMID: 26216469
  35. Developmental priming of stomatal sensitivity to abscisic acid by leaf microclimate.
    Curr Biol. 2013 Sep 23;23(18):1805-11 PMID: 24035546
  36. Regulatory mechanism controlling stomatal behavior conserved across 400 million years of land plant evolution.
    Curr Biol. 2011 Jun 21;21(12):1025-9 PMID: 21658944
  37. Regulation of osmotic stress-responsive gene expression by the LOS6/ABA1 locus in Arabidopsis.
    J Biol Chem. 2002 Mar 8;277(10):8588-96 PMID: 11779861
  38. 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
  39. Ozone-triggered rapid stomatal response involves the production of reactive oxygen species, and is controlled by SLAC1 and OST1.
    Plant J. 2010 May;62(3):442-53 PMID: 20128877
  40. Increased vapor pressure deficit due to higher temperature leads to greater transpiration and faster mortality during drought for tree seedlings common to the forest-grassland ecotone.
    New Phytol. 2013 Oct;200(2):366-74 PMID: 23718199
  41. Up-regulation of NCED3 and ABA biosynthesis occur within minutes of a decrease in leaf turgor but AHK1 is not required.
    J Exp Bot. 2017 May 17;68(11):2913-2918 PMID: 28449122
  42. 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
  43. The identification of genes involved in the stomatal response to reduced atmospheric relative humidity.
    Curr Biol. 2006 May 9;16(9):882-7 PMID: 16682349
  44. 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
  45. Stomatal responses to humidity: has the 'black box' finally been opened?
    Plant Cell Environ. 2016 Mar;39(3):482-4 PMID: 26485479
  46. ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis.
    Plant Cell Physiol. 2002 Dec;43(12):1473-83 PMID: 12514244
  47. Arabidopsis PYR/PYL/RCAR receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid.
    Plant Cell. 2012 Jun;24(6):2483-96 PMID: 22739828
  48. The midday depression of CO2 assimilation in leaves of Arbutus unedo L.: diurnal changes in photosynthetic capacity related to changes in temperature and humidity.
    Planta. 1986 Sep;168(4):546-58 PMID: 24232332
  49. The promoter of the Arabidopsis thaliana SUC2 sucrose-H+ symporter gene directs expression of beta-glucuronidase to the phloem: evidence for phloem loading and unloading by SUC2.
    Planta. 1995;196(3):564-70 PMID: 7647685
  50. Separating active and passive influences on stomatal control of transpiration.
    Plant Physiol. 2014 Apr;164(4):1578-86 PMID: 24488969
  51. The role of ABA recycling and transporter proteins in rapid stomatal responses to reduced air humidity, elevated CO2, and exogenous ABA.
    Mol Plant. 2015 Apr;8(4):657-9 PMID: 25620768
  52. Putting the brakes on: abscisic acid as a central environmental regulator of stomatal development.
    New Phytol. 2014 Apr;202(2):376-91 PMID: 24611444
  53. Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci.
    Plant J. 1996 Oct;10(4):655-61 PMID: 8893542
  54. The absence of molybdenum cofactor sulfuration is the primary cause of the flacca phenotype in tomato plants.
    Plant J. 2002 Aug;31(3):305-17 PMID: 12164810
  55. A hydraulic signal in root-to-shoot signalling of water shortage.
    Plant J. 2007 Oct;52(1):167-74 PMID: 17711416
  56. Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry.
    Nat Protoc. 2010 Jun;5(6):986-92 PMID: 20448544
  57. Does ozone increase ABA levels by non-enzymatic synthesis causing stomata to close?
    Plant Cell Environ. 2017 May;40(5):741-747 PMID: 28042679
  58. Nitric oxide inhibits blue light-specific stomatal opening via abscisic acid signaling pathways in Vicia guard cells.
    Plant Cell Physiol. 2007 May;48(5):715-23 PMID: 17389607
  59. ABA induces H2O2 production in guard cells, but does not close the stomata on Vicia faba leaves developed at high air humidity.
    Plant Signal Behav. 2014;9(7):e29192 PMID: 25763494
  60. Phospho-site mapping, genetic and in planta activation studies reveal key aspects of the different phosphorylation mechanisms involved in activation of SnRK2s.
    Plant J. 2010 Sep;63(5):778-90 PMID: 20561261
  61. Intertissue signal transfer of abscisic acid from vascular cells to guard cells.
    Plant Physiol. 2014 Apr;164(4):1587-92 PMID: 24521878
  62. ABA transport and transporters.
    Trends Plant Sci. 2013 Jun;18(6):325-33 PMID: 23453706
  63. Elevated CO2-Induced Responses in Stomata Require ABA and ABA Signaling.
    Curr Biol. 2015 Oct 19;25(20):2709-16 PMID: 26455301
  64. Isolation of a strong Arabidopsis guard cell promoter and its potential as a research tool.
    Plant Methods. 2008 Feb 19;4:6 PMID: 18284694
  65. Most stomatal closure in woody species under moderate drought can be explained by stomatal responses to leaf turgor.
    Plant Cell Environ. 2016 Sep;39(9):2014-26 PMID: 27255698
  66. Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members.
    Plant J. 2012 May;70(3):501-12 PMID: 22171989
  67. Drought induction of Arabidopsis 9-cis-epoxycarotenoid dioxygenase occurs in vascular parenchyma cells.
    Plant Physiol. 2008 Aug;147(4):1984-93 PMID: 18550687
  68. Abscisic Acid Transport and Homeostasis in the Context of Stomatal Regulation.
    Mol Plant. 2015 Sep;8(9):1321-33 PMID: 26099923
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2018-00-00
Epub
2017-00-06
Pages
851-864
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC5761775
Subset
IM
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