A CO₂ regulator CDI3 and its homologues are essential for anion homeostasis in plant cells

Abstract

Regulation of stomatal aperture relies on turgor changes within a pair of guard cells. The main solutes involved in the osmoregulation are K⁺, Cl^- and malate^2-. Through a high-throughput leaf thermal imaging screen, we isolated the Arabidopsis mutant cdi3 (carbon dioxide insensitive 3) that overaccumulates these osmoregulatory ions in guard cells, leading to CO₂ insensitivity in plant gas exchange regulation. The CDI3 protein is a distant homologue of bacterial and fungal C4-dicarboxylate transporters, and is localized specifically to the plasma membrane of guard cells. Our results identify CDI3 as a regulator of guard cell ion balance essential for stomatal movement. Arabidopsis CDI3 homologues, which are expressed in different tissues, but not in guard cells, complemented the cdi3 phenotypes when expressed ectopically in guard cells. Thus CDI3 family members have an evolutionarily conserved function in distinct Arabidopsis tissues.