Metabolomics of red‐light‐induced stomatal opening in Arabidopsis thaliana: Coupling with abscisic acid and jasmonic acid metabolism

Abstract

Summary Environmental stimuli‐triggered stomatal movement is a key physiological process that regulates CO2 uptake and water loss in plants. Stomata are defined by pairs of guard cells that perceive and transduce external signals, leading to cellular volume changes and consequent stomatal aperture change. Within the visible light spectrum, red light induces stomatal opening in intact leaves. However, there has been debate regarding the extent to which red‐light‐induced stomatal opening arises from direct guard cell sensing of red light versus indirect responses as a result of red light influences on mesophyll photosynthesis. Here we identify conditions that result in red‐light‐stimulated stomatal opening in isolated epidermal peels and enlargement of protoplasts, firmly establishing a direct guard cell response to red light. We then employ metabolomics workflows utilizing gas chromatography mass spectrometry and liquid chromatography mass spectrometry for metabolite profiling and identification of Arabidopsis guard cell metabolic signatures in response to red light in the absence of the mesophyll. We quantified 223 metabolites in Arabidopsis guard cells, with 104 found to be red light responsive. These red‐light‐modulated metabolites participate in the tricarboxylic acid cycle, carbon balance, phytohormone biosynthesis and redox homeostasis. We next analyzed selected Arabidopsis mutants, and discovered that stomatal opening response to red light is correlated with a decrease in guard cell abscisic acid content and an increase in jasmonic acid content. The red‐light‐modulated guard cell metabolome reported here provides fundamental information concerning autonomous red light signaling pathways in guard cells.

Influence of Environmental Factors Light, CO2, Temperature, and Relative Humidity on Stomatal Opening and Development: A Review

“…Red light pulses (500 µmole/m 2 s) on a red background did not cause a similar reaction. In line with these findings, Zhu et al [48] found that blue light-induced stomatal opening required low light intensity and a short duration of illumination as compared with red light-induced stomatal opening [48].…”

“…Red light induces stomatal opening via photosynthesis in the mesophyll and guard cell chloroplasts and decreases the intercellular CO 2 concentration, therefore, red light acts both as a signal and an energy source [47]. The red-light-induced stomatal opening may result from a combination of both guard cell responses to the reduction in intercellular CO 2 and a direct response of the chloroplasts located in the guard cells to red light [46,48,49]. It has been thought to be the main mechanism that coordinates stomatal behaviour in relation to photosynthesis [50].…”

“…Blue-light irradiation of guard cells activates phototropins, which are blue light photoreceptor protein kinases, through autophosphorylation ( Figure 3). Blue light primarily is perceived by photoreceptors PHOT1 and PHOT2, which activate the guard cell PM H + -ATPase and CBC (CONVERGENCE OF BLUE LIGHT (BL) AND CO 2 ) kinases, inhibiting S-type anion channels [48,56,57]. Phototropins are light-activated serine/threonine protein kinases.…”

Light-Mediated Signaling and Metabolic Changes Coordinate Stomatal Opening and Closure

“…It is suggested that TAGs are used as a vital energy source, stimulating ATP and malate production through β-oxidation and TCA cycle (Vavasseur and Raghavendra, 2005;Daloso et al, 2017). Furthermore, a recent study systematically examined red light-induced metabolic changes in GCs of Arabidopsis, showing that red light-induced stomatal opening is correlated with decreased contents of ABA and jasmonic acid (JA) in GCs in addition to TCA cycle and carbon homeostasis (Zhu et al, 2020). It will be interesting to investigate how light and phytohormone signaling cross-talk in regulating stomatal movement.…”

Atavistic Stomatal Responses to Blue Light in Marsileaceae

“…It is also unclear whether this function is conserved across angiosperms. The angiosperm PAR response might reflect a combination of 4 mesophyll signals and largely unknown pathways involving guard cell photosynthesis and/or metabolism (Lawson et al, 2008;Messinger et al, 2006;Olsen et al, 2002;Zhu et al, 2020), although the mesophyll component is often dominant (Fujita et al, 2013;Mott et al, 2008;Roelfsema et al, 2002). In seed-free plants, the mesophyll-based response to light is apparently absent and the PAR stomatal response is entirely dependent on guard cell photosynthesis and/or metabolism (Doi and Shimazaki, 2008;McAdam and Brodribb, 2012).…”