Role and Interrelationship of Gα Protein, Hydrogen Peroxide, and Nitric Oxide in Ultraviolet B-Induced Stomatal Closure in Arabidopsis Leaves

• Published in: Plant physiology (Bethesda) Vol. 161; no. 3; pp. 1570 - 1583
• Main Authors: He, Jun-Min, Ma, Xian-Ge, Zhang, Ying, Sun, Tie-Feng, Xu, Fei-Fei, Chen, Yi-Ping, Liu, Xiao, Yue, Ming
• Format: Journal Article
• Language: English
• Published: Rockville, MD American Society of Plant Biologists 01.03.2013
• Subjects: Arabidopsis - enzymology; Arabidopsis - physiology; Arabidopsis - radiation effects; Arabidopsis Proteins - metabolism; Biological and medical sciences; Fluorescence; Fundamental and applied biological sciences. Psychology; GTP-Binding Protein alpha Subunits - metabolism; Guard cells; Hydrogen Peroxide - metabolism; Hydrogen Peroxide - pharmacology; Leaves; NADPH Oxidases - metabolism; Nitric Oxide - biosynthesis; Nitric Oxide - metabolism; Oxidases; Oxides; Peroxides; Physiological regulation; Plant cells; Plant physiology and development; Plant Stomata - cytology; Plant Stomata - drug effects; Plant Stomata - physiology; Plant Stomata - radiation effects; Plants; Signal Transduction - drug effects; SIGNALING AND RESPONSE; Stomatal movement; Ultraviolet Rays; Hydrogen peroxide; UVB radiation; Stomatal conductance; Plant leaf; Protein; Arabidopsis thaliana; Plant physiology; Cruciferae; Dicotyledones; Nitric oxide; Angiospermae; Stomatal movement; Spermatophyta; Experimental plant
• ISSN: 0032-0889; 1532-2548; 1532-2548
• DOI: 10.1104/pp.112.211623

Heterotrimeric G proteins have been shown to transmit ultraviolet B (UV-B) signals in mammalian cells, but whether they also transmit UV-B signals in plant cells is not clear. In this paper, we report that 0.5 W m⁻² UV-B induces stomatal closure in Arabidopsis (Arabidopsis thaliana) by eliciting a cascade of intraceflular signaling events including Gα protein, hydrogen peroxide (H₂O₂), and nitric oxide (NO). UV-B triggered a significant increase in H₂O₂ or NO levels associated with stomatal closure in the wild type, but these effects were abolished in the single and double mutants of AtrbohD and AtrbohF or in the Nia1 mutants, respectively. Furthermore, we found that UV-B-mediated H₂O₂ and NO generation are regulated by GPA1, the Gα-subunit of heterotrimeric G proteins. UV-B-dependent H₂O₂ and NO accumulation were nullified in gpa1 knockout mutants but enhanced by overexpression of a constitutively active form of GPA1 (cGα). In addition, exogenously applied H₂O₂ or NO rescued the defect in UV-B-mediated stomatal closure in gpa1 mutants, whereas cGα AtrbohD/AtrbohF and cGα nia1 constructs exhibited a similar response to AtrbohD/AtrbohF and Nia1, respectively. Finally, we demonstrated that Gα activation of NO production depends on H₂O₂. The mutants of AtrbohD and AtrbohF had impaired NO generation in response to UV-B, but UV-B-induced H₂O₂ accumulation was not impaired in Nia1. Moreover, exogenously applied NO rescued the defect in UV-B-mediated stomatal closure in the mutants of AtrbohD and AtrbohF. These findings establish a signaling pathway leading to UV-B-induced stomatal closure that involves GPA1-dependent activation of H₂O₂ production and subsequent Nia1-dependent NO accumulation.