Red light activates a chloroplast-dependent ion uptake mechanism for stomatal opening under reduced CO₂...

•  Under red light in ambient CO₂ guard cells of faba bean (Vicia faba) fix CO₂ and accumulate sucrose, causing stomata to open. We examined whether at [CO₂ ] low enough to limit guard cell photosynthesis stomata would open when illuminated with red (R) or far-red (FR) light. •  After illumination with R or FR in buffered KCl solutions, net stomatal opening was c. 3 µm (R and FR) in air containing 210-225 µl l^-1 CO₂ and was 5 µm (R) or 6.5 µm (FR) in air containing 40-50 µl l^-1 CO₂ . Opening was fully inhibited by 3-(3,4-dichlorophenyl)-1,1 dimethyl urea, the calmodulin antagonist W-7, the ser/thr kinase inhibitor ML-9, and sodium orthovanadate, but not by dithiothreitol, which inhibits formation of zeaxanthin, the blue light photoreceptor of guard cells. •  Stomatal opening was accompanied by K⁺ uptake and starch loss. Similar results were obtained when leaves were exposed to conditions designed to lower intercellular leaf [CO₂ ]. •  These data suggest that the guard cell chloroplasts transduce reduced [CO₂ ], activating stomatal opening through an ion uptake mechanism that depends on chloroplastic photosynthetic electron transport and that shares downstream components of the blue light signal transduction cascade.