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CELL BIOLOGY AND SIGNAL TRANSDUCTION

Extracellular Calmodulin-Induced Stomatal Closure Is Mediated by Heterotrimeric G Protein and H₂O₂¹

National Laboratory of Plant Physiology and Biochemistry, College of Biological Sciences, China Agricultural University, Beijing 100094, China (Y.-L.C., Y.-M.X., J.C., X.-C.W.); Biotechnology Research Institute, National Grand Scientific Engineering of Crop Gene Resources and Genetic Improvement, Chinese Academy of Agricultural Sciences, Beijing 100081, China (R.H.); and College of Life Sciences, Hebei Normal University, Shijiazhuang 050016, China (Y.-L.C., P.L.)

Extracellular calmodulin (ExtCaM) exerts multiple functions in animals and plants, but the mode of ExtCaM action is not well understood. In this paper, we provide evidence that ExtCaM stimulates a cascade of intracellular signaling events to regulate stomatal movement. Analysis of the changes of cytosolic free Ca²⁺ ([Ca²⁺]_cyt) and H₂O₂ in Vicia faba guard cells combined with epidermal strip bioassay suggests that ExtCaM induces an increase in both H₂O₂ levels and [Ca²⁺]_cyt, leading to a reduction in stomatal aperture. Pharmacological studies implicate heterotrimeric G protein in transmitting the ExtCaM signal, acting upstream of [Ca²⁺]_cyt elevation, and generating H₂O₂ in guard cell responses. To further test the role of heterotrimeric G protein in ExtCaM signaling in stomatal closure, we checked guard cell responses in the Arabidopsis (Arabidopsis thaliana) G-subunit-null gpa1 mutants and cG overexpression lines. We found that gpa1 mutants were insensitive to ExtCaM stimulation of stomatal closure, whereas cG overexpression enhanced the guard cell response to ExtCaM. Furthermore, gpa1 mutants are impaired in ExtCaM induction of H₂O₂ generation in guard cells. Taken together, our results strongly suggest that ExtCaM activates an intracellular signaling pathway involving activation of a heterotrimeric G protein, H₂O₂ generation, and changes in [Ca²⁺]_cyt in the regulation of stomatal movements.

² These authors contributed equally to the paper.

Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.047837.

^* Corresponding author; e-mail xcwang{at}cau.edu.cn; fax 86–10–62733450.

Received June 8, 2004; returned for revision September 20, 2004; accepted September 27, 2004.

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