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

Abstract

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 22 UV-B induces stomatal closure in Arabidopsis (Arabidopsis thaliana) by eliciting a cascade of intracellular signaling events including Ga protein, hydrogen peroxide (H 2 O 2 ), and nitric oxide (NO). UV-B triggered a significant increase in H 2 O 2 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 H 2 O 2 and NO generation are regulated by GPA1, the Ga-subunit of heterotrimeric G proteins. UV-B-dependent H 2 O 2 and NO accumulation were nullified in gpa1 knockout mutants but enhanced by overexpression of a constitutively active form of GPA1 (cGa). In addition, exogenously applied H 2 O 2 or NO rescued the defect in UV-B-mediated stomatal closure in gpa1 mutants, whereas cGa AtrbohD/AtrbohF and cGa nia1 constructs exhibited a similar response to AtrbohD/ AtrbohF and Nia1, respectively. Finally, we demonstrated that Ga activation of NO production depends on H 2 O 2 . The mutants of AtrbohD and AtrbohF had impaired NO generation in response to UV-B, but UV-B-induced H 2 O 2 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 H 2 O 2 production and subsequent Nia1-dependent NO accumulation.

Ultraviolet-B-Induced Stomatal Closure in Arabidopsis Is Regulated by the UV RESISTANCE LOCUS8 Photoreceptor in a Nitric Oxide-Dependent Mechanism

“…Neither of these effects were readily reversed 24 h after the end of irradiation, consistent with our finding that stomatal closure is maintained by the high levels of NO remaining almost 24 h after UV-B exposure. It has been demonstrated that low levels of UV-B induce NO and ROS in some tissues and plant species (Zhang et al, 2003;An et al, 2005;He et al, 2005He et al, , 2013Qu et al, 2006). However, in our work, the low UV-B radiation used did not induce NO and H 2 O 2 production, explaining the lack of stomata closure.…”

“…Jansen and Noort (2000) found that UV-B may induce closure or opening in Vicia faba stomata, depending on the dose. Similarly, in Arabidopsis (Arabidopsis thaliana), very low fluence rates of UV-B stimulate stomatal opening (Eisinger et al, 2003), whereas a higher irradiance induces stomatal closure in the wild-type ecotype Wassilewskija (Ws; He et al, 2013). However, it is unknown whether UVR8 participates in the regulation of stomatal aperture by UV-B.…”

“…Stomatal movements are regulated by a variety of factors that stimulate opening and closure (Kim et al, 2010;Araújo et al, 2011;Chen et al, 2012). It has been reported that stomatal movement may be influenced by UV-B, and the response observed (opening or closure) is dependent on the fluence rate (Nogues et al, 1999;Jansen and Noort, 2000;Eisinger et al, 2003;He et al, 2005He et al, , 2013. Jansen and Noort (2000) found that UV-B may induce closure or opening in Vicia faba stomata, depending on the dose.…”

Signal mediators at induction of heat resistance of wheat plantlets by short-term heating

“…However the treatment of these plants with the donor of NO led to the ability of implication to close stomas. On the other hand, the treatment with hydrogen peroxide of mutants nia1-2, defective in nitric oxide synthesis, did not cause similar effect [6].…”

“…The given effects were suppressed both by the catalase, and the scavenger of nitric oxide PTIO (2-phenyl-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide) [5]. There is a reason to suppose that the hydrogen peroxide plays the role of an inducer, causing the accumulation of NO, which is directly involved in the regulation of the state of stomas [6]. In Arabidopsis mutants atrbohD/F, defective in the activity of NADPH oxidase and not producing enough hydrogen peroxide, the closing of stomas, induced by the action of UF-B, did not take place.…”