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Published on March 25, 2009; 10.1104/pp.109.137067

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Received February 15, 2009
Accepted March 19, 2009

A Signaling Pathway Linking Nitric Oxide Production to Heterotrimeric G Protein and H2O2 Regulates Extracellular Calmodulin Induction of Stomatal Closure in Arabidopsis

Jian-Hua Li , Yin-Qian Liu , Pin Lu , Hai-Fei Lin , Yang Bai , Xue-Chen Wang , and Yu-Ling Chen *

Hebei Key Laboratory of Molecular and Cellular Biology, College of Life Science, Hebei Normal University, Shijiazhuang 050016, China; School of Basic Medical Sciences, Hebei Medical University, Shijiazhuang 050017, China; National Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100094, China

* Corresponding author; email: yulingchen{at}mail.hebtu.edu.cn.

Extracellular calmodulin (ExtCaM) regulates stomatal movement by eliciting a cascade of intracellular signaling events including heterotrimeric G protein, H2O2 and Ca2+. However, the ExtCaM-mediated guard cell signaling pathway remains poorly understood. In this report, we show that Arabidopsis (Arabidopsis thaliana) NITRIC OXIDE ASSOCIATED 1 (AtNOA1)-dependent nitric oxide (NO) accumulation plays a crucial role in ExtCaM-induced stomatal closure. ExtCaM triggered a significant increase in NO levels associated with stomatal closure in wild type, but both effects were abolished in the Atnoa1 mutant. Furthermore, we found that ExtCaM-mediated NO generation is regulated by GPA1, the G{alpha}-subunit of heterotrimeric G protein. The ExtCaM-dependent NO accumulation was nullified in gpa1 knockout mutants, but enhanced by overexpression of a constitutively active form of GPA1 (cG{alpha}). In addition, cG{alpha} Atnoa1 and gpa1-2 Atnoa1 double mutants exhibited a similar response as did Atnoa1. The defect in gpa1 was rescued by overexpression of AtNOA1. Finally, we demonstrated that G protein activation of NO production depends on hydrogen peroxide (H2O2). Reduced H2O2 levels in guard cells blocked stomatal response of cG{alpha} lines, whereas exogenous applied H2O2 rescued the defect in ExtCaM-mediated stomatal closure in gpa1 mutants. Moreover, atrbohD/F mutant, which lacks the NADPH oxidase activity in guard cells, had impaired NO generation in response to ExtCaM; and H2O2-induced stomatal closure and NO accumulation were greatly impaired in Atnoa1. These findings have established a signaling pathway leading to ExtCaM-induced stomatal closure, which involves GPA1-dependent activation of H2O2 production and subsequent AtNOA1-dependent NO accumulation.






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