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PMID: 24019428 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Identification of cyclic GMP-activated nonselective Ca2+-permeable cation channels and associated CNGC5 and CNGC6 genes in Arabidopsis guard cells.

Plant physiology ·Vol. 163 ·No. 2 ·2013-10-00 ·Pages 578-90

Wang YF, Munemasa S, Nishimura N, Ren HM, Robert N, Han M, Puzõrjova I, Kollist H, Lee S, Mori I, Schroeder JI

Abstract

Cytosolic Ca(2+) in guard cells plays an important role in stomatal movement responses to environmental stimuli. These cytosolic Ca(2+) increases result from Ca(2+) influx through Ca(2+)-permeable channels in the plasma membrane and Ca(2+) release from intracellular organelles in guard cells. However, the genes encoding defined plasma membrane Ca(2+)-permeable channel activity remain unknown in guard cells and, with some exceptions, largely unknown in higher plant cells. Here, we report the identification of two Arabidopsis (Arabidopsis thaliana) cation channel genes, CNGC5 and CNGC6, that are highly expressed in guard cells. Cytosolic application of cyclic GMP (cGMP) and extracellularly applied membrane-permeable 8-Bromoguanosine 3',5'-cyclic monophosphate-cGMP both activated hyperpolarization-induced inward-conducting currents in wild-type guard cells using Mg(2+) as the main charge carrier. The cGMP-activated currents were strongly blocked by lanthanum and gadolinium and also conducted Ba(2+), Ca(2+), and Na(+) ions. cngc5 cngc6 double mutant guard cells exhibited dramatically impaired cGMP-activated currents. In contrast, mutations in CNGC1, CNGC2, and CNGC20 did not disrupt these cGMP-activated currents. The yellow fluorescent protein-CNGC5 and yellow fluorescent protein-CNGC6 proteins localize in the cell periphery. Cyclic AMP activated modest inward currents in both wild-type and cngc5cngc6 mutant guard cells. Moreover, cngc5 cngc6 double mutant guard cells exhibited functional abscisic acid (ABA)-activated hyperpolarization-dependent Ca(2+)-permeable cation channel currents, intact ABA-induced stomatal closing responses, and whole-plant stomatal conductance responses to darkness and changes in CO2 concentration. Furthermore, cGMP-activated currents remained intact in the growth controlled by abscisic acid2 and abscisic acid insensitive1 mutants. This research demonstrates that the CNGC5 and CNGC6 genes encode unique cGMP-activated nonselective Ca(2+)-permeable cation channels in the plasma membrane of Arabidopsis guard cells.

MeSH Terms
Abscisic Acid/pharmacology Arabidopsis/cytology,drug effects,genetics,radiation effects Arabidopsis Proteins/genetics,metabolism Calcium/metabolism Calcium Channel Blockers/pharmacology Calcium Channels/metabolism Carbon Dioxide/pharmacology Cations Cell Membrane Permeability/drug effects Cyclic GMP/analogs & derivatives,pharmacology Cyclic Nucleotide-Gated Cation Channels/genetics,metabolism Ecotype Gene Expression Regulation, Plant/drug effects Genes, Plant/genetics Ion Channel Gating/drug effects,genetics,radiation effects Light Mutation/genetics Plant Stomata/cytology,drug effects,genetics,radiation effects Protoplasts/drug effects,metabolism RNA, Messenger/genetics,metabolism Recombinant Fusion Proteins/metabolism Signal Transduction/drug effects,genetics,radiation effects Subcellular Fractions/drug effects,metabolism,radiation effects Time Factors Tobacco/drug effects,metabolism
Chemicals
Arabidopsis Proteins CNGC5 protein, Arabidopsis CNGC6 protein, Arabidopsis Calcium Channel Blockers Calcium Channels Cations Cyclic Nucleotide-Gated Cation Channels RNA, Messenger Recombinant Fusion Proteins Carbon Dioxide 8-bromocyclic GMP Abscisic Acid Cyclic GMP Calcium
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Wang Yong-Fei
National Key Laboratory of Plant Molecular Genetics, Institute of Plant Physiology and Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China.
Munemasa Shintaro
Nishimura Noriyuki
Ren Hui-Min
Robert Nadia
Han Michelle
Puzõrjova Irina
Kollist Hannes
Lee Stephen
Mori Izumi
Schroeder Julian I
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Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
DOI
10.1104/pp.113.225045
Published
2013-10-00
Epub
2013-00-09
Pages
578-90
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC3793039
Subset
IM
Grants
NIGMS NIH HHS · R01 GM060396 · United States
NIGMS NIH HHS · R01GM060396 · United States
External Links
PubMed source DOI: 10.1104/pp.113.225045 PMC Full Text View journal details
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