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

Abstract

Stomata are valves on the leaf surface controlling carbon dioxide (CO₂) influx for photosynthesis and water loss by transpiration. Thus, plants have to evolve elaborate mechanisms controlling stomatal aperture to allow efficient photosynthesis while avoid excessive water loss. Light is not only the energy source for photosynthesis but also an important signal regulating stomatal movement during dark-to-light transition. Our knowledge concerning blue and red light signaling and light-induced metabolite changes that contribute to stomatal opening are accumulating. This review summarizes recent advances on the signaling components that lie between the perception of blue/red light and activation of the PM H⁺-ATPases, and on the negative regulation of stomatal opening by red light-activated phyB signaling and ultraviolet (UV-B and UV-A) irradiation. Besides, light-regulated guard cell (GC)-specific metabolic levels, mesophyll-derived sucrose, and CO₂ concentration within GCs also play dual roles in stomatal opening. Thus, light-induced stomatal opening is tightly accompanied by brake mechanisms, allowing plants to coordinate carbon gain and water loss. Knowledge on the mechanisms regulating the trade-off between stomatal opening and closure may have potential applications toward generating superior crops with improved water use efficiency (CO₂ gain vs. water loss).

Keywords: Arabidopsis thaliana; guard cell metabolism; light signaling; negative mechanism; stomatal movement; trade-off.

Figure 1

Light-mediated signaling and metabolic changes coordinate stomatal movements. (A) Stomatal aperture increases during dark-to-light transition. Blue and red light cooperatively induce stomatal opening through mediating different signaling pathways, yet converging on activation of the plasma membrane (PM) H⁺-ATPases in guard cells (GCs). Skotomorphogenesis regulators, such as CONSTITUTIVE PHOTOMORPHOGENIC (COP1), SUPPRESSOR OF PHYTOCHROME A (SPA), and PHYTOCHROME-INTERACTING FACTORS (PIFs) proteins, whose activities are inactivated by light, act as central regulators of stomatal closure. Besides, light-induced stomatal opening is closely related to mesophyll photosynthesis and GC-specific metabolic changes including the breakdown of sucrose, starch and lipids, which provide carbon skeletons for ATP synthesis via glycolysis and mitochondrial respiration. (B) Negative regulation of stomatal opening by red light, ultraviolet (UV-B), and UV-A signaling pathways. Mesophyll-derived sucrose acts as a signal to trigger stomatal closure in periods of high photosynthetic rate, which involves hexokinase (HXK)-mediated ABA signaling. Carbon dioxide (CO₂) concentration [CO₂] within GCs is constantly controlled by the stomatal aperture and photosynthetic rate. Since low [CO₂] promotes stomatal opening while high internal [CO₂] induces stomatal closing. The crosstalk between light‐ and CO₂-mediated signaling deserves further investigation. Collectively, light signaling coupled with mesophyll-derived sucrose and internal [CO₂] coordinates the trade-off between stomatal opening and closure.

Figure 2

Different light signaling pathways coordinate stomatal opening and closure trade-off. (A) In darkness, the COP1/SPA protein complexes act in concert with PIF4/5 to suppress stomata opening. COP1 acts through disrupting microtubule organization and inhibiting S-type anion channels (SLAC1). MYB60 is a positive regulator of light-induced stomatal opening and it acts downstream of COP1 in an unidentified mechanism. (B) Different light signaling pathways involved in regulating stomatal opening and closure. In light or upon dark-to-light transition, different light photoreceptors act in concert to promote stomatal opening through inactivating COP1/SPA and PIFs. Blue and red light signaling converges on the activation of PM H⁺-ATPase, resulting in proton extrusion, K⁺ uptake, and ultimately water influx into GCs. Red light-activated phyB signaling also mediates a brake mechanism comprised of the ROPGEF2-ROP2/7-RIC7 signal cascade to suppress stomatal opening. RIC7 suppresses the activity of Exo70B1, a component of the vesicle trafficking machinery. UV-B and UV-A irradiance prevents blue/red light-mediated stomatal opening. UV-B promotes the production of abscisic acid (ABA) and in turn hydrogen peroxide (H₂O₂) and nitric oxide (NO). In parallel, UV-B perception by the UVR8 dimer induces the interaction of UVR8 monomer with COP1 in the nucleus, resulting in upregulated expression of ELONGATED HYPOCOTYL5 (HY5) and HY5 HOMOLOG (HYH) that stimulate NO production. NO stimulates stomatal closure through activating SLAC1 and inhibiting K⁺ channels. UV-A induces decrease in the level of cyclic guanosine monophosphate (cGMP) dependent on the cGMP phosphodiesterase (AtCN-PDE1). phyB, phytochrome B; CRY, cryptochrome; PHOT, phototropin; BLUS1, BLUE LIGHT SIGNALING 1; BHP, BLUE LIGHT-DEPENDENT H⁺-ATPASE PHOSPHORYLATION; PP1, PROTEIN PHOSPHATASE 1; PRSL1, PP1 REGULATORY SUBUNITS2-LIKE PROTEIN 1; SLAC1, SLOW ANION CHANNEL 1; ROP, Plant Rho-type GTPase; ROPGEF2, ROP GUANINE NUCLEOTIDE EXCHANGE FACTOR 2; RIC7, ROP-interactive Cdc42‐ and Rac-interactive binding motif-containing protein 7. Arrow and bar-ended lines represent activation and inhibition, respectively. Dotted lines denote indirect regulation. Question mark denotes unclear mechanism.

Figure 3

Light-induced metabolic changes and CO₂ concentration [CO₂] within GCs coordinate stomatal opening and closure trade-off. Light-induced stomatal opening are tightly associated with GC metabolic changes including the breakdown of sucrose, starch, and triacylglycerols (TAGs; ①–③) to provide carbon skeletons for ATP synthesis via glycolysis and mitochondrial metabolism. Particularly, degradation of TAGs and starch are dependent on blue light signaling. Glucose (Glc) is the major intermediate of starch degradation. In periods of strong light intensity, mesophyll-derived sucrose (Suc) is translocated to the apoplastic space by transpirational stream. Suc is either transported into the GC or cleaved by inverse (INV) in the apoplast to produce Glc and fructose (Frc). Then Glc is uptaken into GCs via the monosaccharide/proton symporters Sugar Transport Protein 1/4 (STP 1/4). Within the GC, sucrose-derived Glc stimulates stomatal closure through hexokinase (HXK)-induced ABA signaling under carbon-replete conditions (④). In addition, CONVERGENCE OF BLUE LIGHT AND CO₂ 1 (CBC1) and CBC2 that act as positive regulators of blue light‐ and low CO₂ concentration [CO₂]-mediated stomatal opening through inactivating the SLAC1 (⑤). By contrast, high [CO₂] signaling activates OPEN STOMATA1 (OST1), a well-established component of ABA signaling to bring about stomatal closure through activating SLAC1 and the R-type AtALUMINUM ACTIVATED MALATE TRANSPORTER 12/QUICK ANION CHANNEL 1 (AtALMT12/QUAC1) channels (⑥). Thus [CO₂] within GCs provides another layer of mechanisms coordinating stomatal opening and closure. Arrow and bar-ended lines represent activation and inhibition, respectively. Dotted lines denote indirect regulation or involvement of several steps. Question mark denotes unclear mechanism. SuSy, sucrose synthase; TCA, tricarboxylic acid; Cit, citrate; IsoC, isocitrate; 2-OG, 2-oxoglutarate; Succ, succinate; Fum, fumarate; Mal, Malate; OAA, oxaloacetate; Glu, glutamate; Gln, glutamine.