A Raf-like protein kinase BHP mediates blue light-dependent stomatal opening

Abstract

Stomata in the plant epidermis open in response to blue light and affect photosynthesis and plant growth by regulating CO2 uptake and transpiration. In stomatal guard cells under blue light, plasma membrane H+-ATPase is phosphorylated and activated via blue light-receptor phototropins and a signaling mediator BLUS1, and H+-ATPase activation drives stomatal opening. However, details of the signaling between phototropins and H+-ATPase remain largely unknown. In this study, through a screening of specific inhibitors for the blue light-dependent H+-ATPase phosphorylation in guard cells, we identified a Raf-like protein kinase, BLUE LIGHT-DEPENDENT H+-ATPASE PHOSPHORYLATION (BHP). Guard cells in the bhp mutant showed impairments of stomatal opening and H+-ATPase phosphorylation in response to blue light. BHP is abundantly expressed in the cytosol of guard cells and interacts with BLUS1 both in vitro and in vivo. Based on these results, BHP is a novel signaling mediator in blue light-dependent stomatal opening, likely downstream of BLUS1.

Fluence rate dependence of red light-induced phosphorylation of plasma membrane H+-ATPase in stomatal guard cells

“…[2][3][4][5][6][7] Thus, disruption of the process of phosphorylation of PM H + -ATPase results in suppression of stomatal opening. [8][9][10][11][12] Blue light-induced phosphorylation of PM H + -ATPase is detectable by biochemical analyses using guard cell protoplasts (GCPs) 3,4,13 or immunohistochemistry using isolated epidermis, 14 indicating that it is a guard cell-autonomous reaction. Red light-induced stomatal opening is considered to depend on photosynthesis.…”

Does Molecular and Structural Evolution Shape the Speedy Grass Stomata?

“…PHOTs to phosphorylate plasma membrane H + -ATPase (Hayashi et al, 2017), driving H + pumping and causing the hyperpolarization of the plasma membrane, activation of inward rectifying K + channels, and water uptake for stomatal opening (Shimazaki et al, 2007;Marten et al, 2010;Babla et al, 2019). Blue light is one of the most FIGURE 3 | Comparison of gene and gene family distribution for stomatal development and epidermal patterning in a large range of angiosperms.…”

Arabidopsis thaliana Raf22 protein kinase maintains growth capacity during postgerminative growth arrest under stress

“…A growing body of evidence suggests that Raf‐type MAP3Ks play significant roles in plant growth/development and in stress response signalling. Examples of Raf‐type MAP3Ks with well‐established roles include A. thaliana CONSTITUTIVE TRIPLE RESPONSE1, which functions in the ethylene signal transduction pathway (Kieber, Rothenberg, Roman, Feldmann, & Ecker, ); A. thaliana ENHANCED DISEASE RESISTANCE1, which negatively regulates disease resistance (Frye & Innes, ), stress tolerance, and cell death (Tang, Christiansen, & Innes, ); Oryza sativa (rice) DROUGHT HYPERSENSITIVE MUTANT1, which mediates drought resistance through reactive oxygen species scavenging (Ning, Li, Hicks, & Xiong, ); A. thaliana MAP3Kδ4, which is involved in resistance to salt stress and in ABA signalling (Shitamichi, Matsuoka, Sasayama, Furuya, & Nanmori, ); rice INCREASED LEAF ANGLE1, which regulates mechanical tissue formation in the lamina joint (Ning, Zhang, Wang, Zhou, & Xiong, ); A. thaliana Raf43, which regulates seed germination and seedling growth upon exposure to stresses (Virk et al, ); A. thaliana Raf10 and Raf11, which regulate seed germination and ABA sensitivity (Lee, Lee, Kim, & Kim, ); A. thaliana BLUE LIGHT‐DEPENDENT H+‐ATPASE PHOSPHORYLATION, which mediates stomatal opening in response to blue light (Hayashi, Inoue, Ueno, & Kinoshita, ); and A. thaliana HYDRAULIC CONDUCTIVITY ROOT1, which negatively controls root hydraulic conductivity (Shahzad et al, ). Despite these examples, most Raf kinases remain functionally uncharacterized.…”

“…thaliana Raf43, which regulates seed germination and seedling growth upon exposure to stresses (Virk et al, 2015); A. thaliana Raf10 and Raf11, which regulate seed germination and ABA sensitivity (Lee, Lee, Kim, & Kim, 2014); A. thaliana BLUE LIGHT-DEPENDENT H+-ATPASE PHOSPHORYLATION, which mediates stomatal opening in response to blue light (Hayashi, Inoue, Ueno, & Kinoshita, 2017); and A. thaliana HYDRAULIC CONDUCTIVITY ROOT1, which negatively controls root hydraulic conductivity (Shahzad et al, 2016). Despite these examples, most Raf kinases remain functionally uncharacterized.…”