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

Yong Fei Wang, Shintaro Munemasa, Noriyuki Nishimura, Hui Min Ren, Nadia Robert, Michelle Han, Irina Puzõrjova, Hannes Kollist, Stephen Lee, Izumi Mori, Julian I. Schroeder

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Abstract

Cytosolic Ca2+ in guard cells plays an important role in stomatal movement responses to environmental stimuli. These cytosolic Ca2+ increases result from Ca2+ influx through Ca2+-permeable channels in the plasma membrane and Ca2+ release from intracellular organelles in guard cells. However, the genes encoding defined plasma membrane Ca2+-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 39,59-cyclic monophosphate-cGMP both activated hyperpolarization-induced inward-conducting currents in wild-type guard cells using Mg2+ as the main charge carrier. The cGMP-activated currents were strongly blocked by lanthanum and gadolinium and also conducted Ba2+, Ca2+, 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 Ca2+-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 Ca2+-permeable cation channels in the plasma membrane of Arabidopsis guard cells.

Original languageEnglish
Pages (from-to)578-590
Number of pages13
JournalPlant Physiology
Volume163
Issue number2
DOIs
Publication statusPublished - Oct 2013

Fingerprint

cyclic GMP
Cyclic GMP
guard cells
Arabidopsis
Cations
cations
calcium
Genes
genes
Abscisic Acid
abscisic acid
mutants
plasma membrane
Cell Membrane
gadolinium
stomatal movement
lanthanum
Lanthanum
Proteins
cyclic AMP

ASJC Scopus subject areas

  • Plant Science
  • Genetics
  • Physiology

Cite this

Identification of cyclic GMP-activated nonselective Ca2+-permeable cation channels and associated CNGC5 and CNGC6 genes in Arabidopsis guard cells. / Wang, Yong Fei; Munemasa, Shintaro; Nishimura, Noriyuki; Ren, Hui Min; Robert, Nadia; Han, Michelle; Puzõrjova, Irina; Kollist, Hannes; Lee, Stephen; Mori, Izumi; Schroeder, Julian I.

In: Plant Physiology, Vol. 163, No. 2, 10.2013, p. 578-590.

Research output: Contribution to journalArticle

Wang, Yong Fei ; Munemasa, Shintaro ; Nishimura, Noriyuki ; Ren, Hui Min ; Robert, Nadia ; Han, Michelle ; Puzõrjova, Irina ; Kollist, Hannes ; Lee, Stephen ; Mori, Izumi ; Schroeder, Julian I. / Identification of cyclic GMP-activated nonselective Ca2+-permeable cation channels and associated CNGC5 and CNGC6 genes in Arabidopsis guard cells. In: Plant Physiology. 2013 ; Vol. 163, No. 2. pp. 578-590.
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AU - Nishimura, Noriyuki

AU - Ren, Hui Min

AU - Robert, Nadia

AU - Han, Michelle

AU - Puzõrjova, Irina

AU - Kollist, Hannes

AU - Lee, Stephen

AU - Mori, Izumi

AU - Schroeder, Julian I.

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