Home LiteratureArticle Details
PMID: 17142476 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Ca2+-dependent and -independent abscisic acid activation of plasma membrane anion channels in guard cells of Nicotiana tabacum.

Plant physiology ·Vol. 143 ·No. 1 ·2007-01-00 ·Pages 28-37

Marten H, Konrad KR, Dietrich P, Roelfsema MR, Hedrich R

Abstract

Drought induces stomatal closure, a response that is associated with the activation of plasma membrane anion channels in guard cells, by the phytohormone abscisic acid (ABA). In several species, this response is associated with changes in the cytoplasmic free Ca(2+) concentration. In Vicia faba, however, guard cell anion channels activate in a Ca(2+)-independent manner. Because of potential differences between species, Nicotiana tabacum guard cells were studied in intact plants, with simultaneous recordings of the plasma membrane conductance and the cytoplasmic free Ca(2+) concentration. ABA triggered transient rises in cytoplasmic Ca(2+) in the majority of the guard cells (14 out of 19). In seven out of 14 guard cells, the change in cytoplasmic free Ca(2+) closely matched the activation of anion channels, while the Ca(2+) rise was delayed in seven other cells. In the remaining five cells, ABA stimulated anion channels without a change in the cytoplasmic Ca(2+) level. Even though ABA could activate anion channels in N. tabacum guard cells independent of a rise in the cytoplasmic Ca(2+) concentration, patch clamp experiments showed that anion channels in these cells are stimulated by elevated Ca(2+) in an ATP-dependent manner. Guard cells thus seem to have evolved both Ca(2+)-independent and -dependent ABA signaling pathways. Guard cells of N. tabacum apparently utilize both pathways, while ABA signaling in V. faba seems to be restricted to the Ca(2+)-independent pathway.

MeSH Terms
Abscisic Acid/pharmacology Calcium/metabolism,physiology Ion Channels/metabolism Patch-Clamp Techniques Plant Growth Regulators/pharmacology Plant Proteins/metabolism Plant Transpiration Signal Transduction Species Specificity Tobacco/cytology,drug effects,metabolism
Chemicals
Ion Channels Plant Growth Regulators Plant Proteins Abscisic Acid Calcium
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Marten Holger
University of Wurzburg, Biocenter, Molecular Plant Physiology and Biophysics, Julius-von-Sachs Institute for Biosciences, D-97082 Wurzburg, Germany.
Konrad Kai R
Dietrich Petra
Roelfsema M Rob G
Hedrich Rainer
References (44)
44 references, click to expand
  1. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches.
    Pflugers Arch. 1981 Aug;391(2):85-100 PMID: 6270629
  2. Strong regulation of slow anion channels and abscisic acid signaling in guard cells by phosphorylation and dephosphorylation events.
    Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9535-9 PMID: 11607582
  3. The role of calcium in ABA-induced gene expression and stomatal movements.
    Plant J. 2001 May;26(3):351-62 PMID: 11439123
  4. The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway.
    Plant J. 2001 Feb;25(3):295-303 PMID: 11208021
  5. Inhibition of Blue Light-Dependent H+ Pumping by Abscisic Acid in Vicia Guard-Cell Protoplasts.
    Plant Physiol. 1996 Jun;111(2):433-440 PMID: 12226299
  6. Guard cells possess a calcium-dependent protein kinase that phosphorylates the KAT1 potassium channel.
    Plant Physiol. 1998 Feb;116(2):785-95 PMID: 9489023
  7. The generation of Ca(2+) signals in plants.
    Annu Rev Plant Biol. 2004;55:401-27 PMID: 15377226
  8. Arabidopsis abi1-1 and abi2-1 phosphatase mutations reduce abscisic acid-induced cytoplasmic calcium rises in guard cells.
    Plant Cell. 1999 Sep;11(9):1785-98 PMID: 10488243
  9. Protein phosphorylation activates the guard cell Ca2+ channel and is a prerequisite for gating by abscisic acid.
    Plant J. 2002 Oct;32(2):185-94 PMID: 12383084
  10. Sensitivity to abscisic acid of guard-cell K+ channels is suppressed by abi1-1, a mutant Arabidopsis gene encoding a putative protein phosphatase.
    Proc Natl Acad Sci U S A. 1995 Oct 10;92(21):9520-4 PMID: 7568166
  11. Voltage-dependent anion channel of Arabidopsis hypocotyls: nucleotide regulation and pharmacological properties.
    J Membr Biol. 1997 Sep 1;159(1):71-82 PMID: 9309212
  12. Alteration of stimulus-specific guard cell calcium oscillations and stomatal closing in Arabidopsis det3 mutant.
    Science. 2000 Sep 29;289(5488):2338-42 PMID: 11009417
  13. GUARD CELL SIGNAL TRANSDUCTION.
    Annu Rev Plant Physiol Plant Mol Biol. 2001 Jun;52:627-658 PMID: 11337411
  14. Increases in cytosolic Ca2+ are not required for abscisic acid-inhibition of inward K+ currents in guard cells of Vicia faba L.
    Planta. 2000 Jul;211(2):209-17 PMID: 10945215
  15. Stomatal conductance does not correlate with photosynthetic capacity in transgenic tobacco with reduced amounts of Rubisco.
    J Exp Bot. 2004 May;55(400):1157-66 PMID: 15107451
  16. Protein phosphatase activity of abscisic acid insensitive 1 (ABI1) protein from Arabidopsis thaliana.
    Eur J Biochem. 1996 Oct 1;241(1):193-200 PMID: 8898906
  17. 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
  18. Phospholipase C is required for the control of stomatal aperture by ABA.
    Plant J. 2003 Apr;34(1):47-55 PMID: 12662308
  19. Ca2+ and nucleotide dependent regulation of voltage dependent anion channels in the plasma membrane of guard cells.
    EMBO J. 1990 Dec;9(12):3889-92 PMID: 1701140
  20. A tobacco syntaxin with a role in hormonal control of guard cell ion channels.
    Science. 1999 Jan 22;283(5401):537-40 PMID: 9915701
  21. ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis.
    Plant Cell Physiol. 2002 Dec;43(12):1473-83 PMID: 12514244
  22. A new generation of Ca2+ indicators with greatly improved fluorescence properties.
    J Biol Chem. 1985 Mar 25;260(6):3440-50 PMID: 3838314
  23. In the light of stomatal opening: new insights into 'the Watergate'.
    New Phytol. 2005 Sep;167(3):665-91 PMID: 16101906
  24. A defined range of guard cell calcium oscillation parameters encodes stomatal movements.
    Nature. 2001 Jun 28;411(6841):1053-7 PMID: 11429606
  25. Two types of anion channel currents in guard cells with distinct voltage regulation.
    Proc Natl Acad Sci U S A. 1992 Jun 1;89(11):5025-9 PMID: 1375754
  26. ABA depolarizes guard cells in intact plants, through a transient activation of R- and S-type anion channels.
    Plant J. 2004 Feb;37(4):578-88 PMID: 14756768
  27. Membrane voltage initiates Ca2+ waves and potentiates Ca2+ increases with abscisic acid in stomatal guard cells.
    Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4778-83 PMID: 9539815
  28. Calcium signaling networks channel plant K+ uptake.
    Cell. 2006 Jun 30;125(7):1221-3 PMID: 16814705
  29. CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca(2+)-permeable channels and stomatal closure.
    PLoS Biol. 2006 Oct;4(10):e327 PMID: 17032064
  30. The Arabidopsis CDPK-SnRK superfamily of protein kinases.
    Plant Physiol. 2003 Jun;132(2):666-80 PMID: 12805596
  31. A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis.
    Cell. 2006 Jun 30;125(7):1347-60 PMID: 16814720
  32. A slow anion channel in guard cells, activating at large hyperpolarization, may be principal for stomatal closing.
    FEBS Lett. 1992 Nov 16;313(1):27-30 PMID: 1385219
  33. Ultrastructural and histochemical studies on guard cells.
    Planta. 1984 Feb;160(2):129-42 PMID: 24258415
  34. Cytosolic abscisic acid activates guard cell anion channels without preceding Ca2+ signals.
    Proc Natl Acad Sci U S A. 2005 Mar 15;102(11):4203-8 PMID: 15753314
  35. Immunosuppressants implicate protein phosphatase regulation of K+ channels in guard cells.
    Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2202-6 PMID: 7681590
  36. Abscisic acid maintains S-type anion channel activity in ATP-depleted Vicia faba guard cells.
    FEBS Lett. 1998 May 29;428(3):177-82 PMID: 9654130
  37. Single guard cell recordings in intact plants: light-induced hyperpolarization of the plasma membrane.
    Plant J. 2001 Apr;26(1):1-13 PMID: 11359605
  38. Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production.
    Plant Cell. 2002 Dec;14(12):3089-99 PMID: 12468729
  39. A novel chloride channel in Vicia faba guard cell vacuoles activated by the serine/threonine kinase, CDPK.
    EMBO J. 1996 Dec 2;15(23):6564-74 PMID: 8978683
  40. Integration and channeling of calcium signaling through the CBL calcium sensor/CIPK protein kinase network.
    Planta. 2004 Oct;219(6):915-24 PMID: 15322881
  41. The multisensory guard cell. Stomatal responses to blue light and abscisic acid
    Plant Physiol. 1999 Mar;119(3):809-16 PMID: 10069820
  42. Regulation of abscisic acid-induced stomatal closure and anion channels by guard cell AAPK kinase.
    Science. 2000 Jan 14;287(5451):300-3 PMID: 10634783
  43. Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells.
    Nature. 2000 Aug 17;406(6797):731-4 PMID: 10963598
  44. Role of Calcium in Signal Transduction of Commelina Guard Cells.
    Plant Cell. 1991 Apr;3(4):333-344 PMID: 12324599
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
0032-0889
Published
2007-01-00
Epub
2006-00-01
Pages
28-37
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC1761993
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com