CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+- permeable channels and stomatal closure

Izumi Mori, Yoshiyuki Murata, Yingzhen Yang, Shintaro Munemasa, Yong Fei Wang, Shannon Andreoli, Hervé Tiriac, Jose M. Alonso, Jeffery F. Harper, Joseph R. Ecker, June M. Kwak, Julian I. Schroeder

Research output: Contribution to journalArticle

335 Citations (Scopus)

Abstract

Abscisic acid (ABA) signal transduction has been proposed to utilize cytosolic Ca2+ in guard cell ion channel regulation. However, genetic mutants in Ca2+ sensors that impair guard cell or plant ion channel signaling responses have not been identified, and whether Ca2+- independent ABA signaling mechanisms suffice for a full response remains unclear. Calcium-dependent protein kinases (CDPKs) have been proposed to contribute to central signal transduction responses in plants. However, no Arabidopsis CDPK gene disruption mutant phenotype has been reported to date, likely due to overlapping redundancies in CDPKs. Two Arabidopsis guard cell-expressed CDPK genes, CPK3 and CPK6, showed gene disruption phenotypes. ABA and Ca2+ activation of slow-type anion channels and, interestingly, ABA activation of plasma membrane Ca2+-permeable channels were impaired in independent alleles of single and double cpk3cpk6 mutant guard cells. Furthermore, ABA- and Ca2+-induced stomatal closing were partially impaired in these cpk3cpk6 mutant alleles. However, rapid-type anion channel current activity was not affected, consistent with the partial stomatal closing response in double mutants via a proposed branched signaling network. Imposed Ca2+ oscillation experiments revealed that Ca 2+-reactive stomatal closure was reduced in CDPK double mutant plants. However, longlasting Ca2+-programmed stomatal closure was not impaired, providing genetic evidence for a functional separation of these two modes of Ca2+-induced stomatal closing. Our findings show important functions of the CPK6 and CPK3 CDPKs in guard cell ion channel regulation and provide genetic evidence for calcium sensors that transduce stomatal ABA signaling.

Original languageEnglish
Pages (from-to)1749-1762
Number of pages14
JournalPLoS Biology
Volume4
Issue number10
DOIs
Publication statusPublished - 2006

Fingerprint

Elongation Factor 2 Kinase
Abscisic Acid
guard cells
protein kinases
anions
Anions
abscisic acid
calcium
Ion Channels
Signal transduction
Genes
Arabidopsis
Signal Transduction
Chemical activation
Alleles
mutants
Phenotype
ion channels
Sensors
Plant Cells

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)

Cite this

CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+- permeable channels and stomatal closure. / Mori, Izumi; Murata, Yoshiyuki; Yang, Yingzhen; Munemasa, Shintaro; Wang, Yong Fei; Andreoli, Shannon; Tiriac, Hervé; Alonso, Jose M.; Harper, Jeffery F.; Ecker, Joseph R.; Kwak, June M.; Schroeder, Julian I.

In: PLoS Biology, Vol. 4, No. 10, 2006, p. 1749-1762.

Research output: Contribution to journalArticle

Mori, I, Murata, Y, Yang, Y, Munemasa, S, Wang, YF, Andreoli, S, Tiriac, H, Alonso, JM, Harper, JF, Ecker, JR, Kwak, JM & Schroeder, JI 2006, 'CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+- permeable channels and stomatal closure', PLoS Biology, vol. 4, no. 10, pp. 1749-1762. https://doi.org/10.1371/journal.pbio.0040327
Mori, Izumi ; Murata, Yoshiyuki ; Yang, Yingzhen ; Munemasa, Shintaro ; Wang, Yong Fei ; Andreoli, Shannon ; Tiriac, Hervé ; Alonso, Jose M. ; Harper, Jeffery F. ; Ecker, Joseph R. ; Kwak, June M. ; Schroeder, Julian I. / CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+- permeable channels and stomatal closure. In: PLoS Biology. 2006 ; Vol. 4, No. 10. pp. 1749-1762.
@article{9100a0096adf43009a8e9e1f0abafbce,
title = "CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+- permeable channels and stomatal closure",
abstract = "Abscisic acid (ABA) signal transduction has been proposed to utilize cytosolic Ca2+ in guard cell ion channel regulation. However, genetic mutants in Ca2+ sensors that impair guard cell or plant ion channel signaling responses have not been identified, and whether Ca2+- independent ABA signaling mechanisms suffice for a full response remains unclear. Calcium-dependent protein kinases (CDPKs) have been proposed to contribute to central signal transduction responses in plants. However, no Arabidopsis CDPK gene disruption mutant phenotype has been reported to date, likely due to overlapping redundancies in CDPKs. Two Arabidopsis guard cell-expressed CDPK genes, CPK3 and CPK6, showed gene disruption phenotypes. ABA and Ca2+ activation of slow-type anion channels and, interestingly, ABA activation of plasma membrane Ca2+-permeable channels were impaired in independent alleles of single and double cpk3cpk6 mutant guard cells. Furthermore, ABA- and Ca2+-induced stomatal closing were partially impaired in these cpk3cpk6 mutant alleles. However, rapid-type anion channel current activity was not affected, consistent with the partial stomatal closing response in double mutants via a proposed branched signaling network. Imposed Ca2+ oscillation experiments revealed that Ca 2+-reactive stomatal closure was reduced in CDPK double mutant plants. However, longlasting Ca2+-programmed stomatal closure was not impaired, providing genetic evidence for a functional separation of these two modes of Ca2+-induced stomatal closing. Our findings show important functions of the CPK6 and CPK3 CDPKs in guard cell ion channel regulation and provide genetic evidence for calcium sensors that transduce stomatal ABA signaling.",
author = "Izumi Mori and Yoshiyuki Murata and Yingzhen Yang and Shintaro Munemasa and Wang, {Yong Fei} and Shannon Andreoli and Herv{\'e} Tiriac and Alonso, {Jose M.} and Harper, {Jeffery F.} and Ecker, {Joseph R.} and Kwak, {June M.} and Schroeder, {Julian I.}",
year = "2006",
doi = "10.1371/journal.pbio.0040327",
language = "English",
volume = "4",
pages = "1749--1762",
journal = "PLoS Biology",
issn = "1544-9173",
publisher = "Public Library of Science",
number = "10",

}

TY - JOUR

T1 - CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+- permeable channels and stomatal closure

AU - Mori, Izumi

AU - Murata, Yoshiyuki

AU - Yang, Yingzhen

AU - Munemasa, Shintaro

AU - Wang, Yong Fei

AU - Andreoli, Shannon

AU - Tiriac, Hervé

AU - Alonso, Jose M.

AU - Harper, Jeffery F.

AU - Ecker, Joseph R.

AU - Kwak, June M.

AU - Schroeder, Julian I.

PY - 2006

Y1 - 2006

N2 - Abscisic acid (ABA) signal transduction has been proposed to utilize cytosolic Ca2+ in guard cell ion channel regulation. However, genetic mutants in Ca2+ sensors that impair guard cell or plant ion channel signaling responses have not been identified, and whether Ca2+- independent ABA signaling mechanisms suffice for a full response remains unclear. Calcium-dependent protein kinases (CDPKs) have been proposed to contribute to central signal transduction responses in plants. However, no Arabidopsis CDPK gene disruption mutant phenotype has been reported to date, likely due to overlapping redundancies in CDPKs. Two Arabidopsis guard cell-expressed CDPK genes, CPK3 and CPK6, showed gene disruption phenotypes. ABA and Ca2+ activation of slow-type anion channels and, interestingly, ABA activation of plasma membrane Ca2+-permeable channels were impaired in independent alleles of single and double cpk3cpk6 mutant guard cells. Furthermore, ABA- and Ca2+-induced stomatal closing were partially impaired in these cpk3cpk6 mutant alleles. However, rapid-type anion channel current activity was not affected, consistent with the partial stomatal closing response in double mutants via a proposed branched signaling network. Imposed Ca2+ oscillation experiments revealed that Ca 2+-reactive stomatal closure was reduced in CDPK double mutant plants. However, longlasting Ca2+-programmed stomatal closure was not impaired, providing genetic evidence for a functional separation of these two modes of Ca2+-induced stomatal closing. Our findings show important functions of the CPK6 and CPK3 CDPKs in guard cell ion channel regulation and provide genetic evidence for calcium sensors that transduce stomatal ABA signaling.

AB - Abscisic acid (ABA) signal transduction has been proposed to utilize cytosolic Ca2+ in guard cell ion channel regulation. However, genetic mutants in Ca2+ sensors that impair guard cell or plant ion channel signaling responses have not been identified, and whether Ca2+- independent ABA signaling mechanisms suffice for a full response remains unclear. Calcium-dependent protein kinases (CDPKs) have been proposed to contribute to central signal transduction responses in plants. However, no Arabidopsis CDPK gene disruption mutant phenotype has been reported to date, likely due to overlapping redundancies in CDPKs. Two Arabidopsis guard cell-expressed CDPK genes, CPK3 and CPK6, showed gene disruption phenotypes. ABA and Ca2+ activation of slow-type anion channels and, interestingly, ABA activation of plasma membrane Ca2+-permeable channels were impaired in independent alleles of single and double cpk3cpk6 mutant guard cells. Furthermore, ABA- and Ca2+-induced stomatal closing were partially impaired in these cpk3cpk6 mutant alleles. However, rapid-type anion channel current activity was not affected, consistent with the partial stomatal closing response in double mutants via a proposed branched signaling network. Imposed Ca2+ oscillation experiments revealed that Ca 2+-reactive stomatal closure was reduced in CDPK double mutant plants. However, longlasting Ca2+-programmed stomatal closure was not impaired, providing genetic evidence for a functional separation of these two modes of Ca2+-induced stomatal closing. Our findings show important functions of the CPK6 and CPK3 CDPKs in guard cell ion channel regulation and provide genetic evidence for calcium sensors that transduce stomatal ABA signaling.

UR - http://www.scopus.com/inward/record.url?scp=33750239010&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=33750239010&partnerID=8YFLogxK

U2 - 10.1371/journal.pbio.0040327

DO - 10.1371/journal.pbio.0040327

M3 - Article

VL - 4

SP - 1749

EP - 1762

JO - PLoS Biology

JF - PLoS Biology

SN - 1544-9173

IS - 10

ER -