A C4 plant K+ channel accelerates stomata to enhance C3 photosynthesis and water use efficiency

Accelerating stomatal kinetics through synthetic optogenetics and mutations that enhance guard cell K+ flux has proven a viable strategy to improve water use efficiency and biomass production. Stomata of the model C4 species Gynandropsis gynandra, a relative of the C3 plant Arabidopsis thaliana, are similarly fast to open and close. We identified and cloned the guard cell rectifying outward K+ channel (GROK) of Gynandropsis and showed that GROK is preferentially expressed in stomatal guard cells. GROK is homologous to the Arabidopsis guard cell K+ channel GORK and, expressed in oocytes, yields a K+ current consistent with that of Gynandropsis guard cells. Complementing the Arabidopsis gork mutant with GROK promoted K+ channel gating and K+ flux, increasing stomatal kinetics and yielding gains in water use efficiency and biomass with varying light, especially under water limitation. Our findings demonstrate the potential for engineering a C4 K+ channel into guard cells of a C3 species, and they speak to the puzzle of how C4 species have evolved mechanisms that enhance water use efficiency and growth under stress.