CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells

The continuing rise in atmospheric [ CO2] is predicted to have diverse and dramatic effects on the productivity of agriculture, plant ecosystems and gas exchange(1-3). Stomatal pores in the epidermis provide gates for the exchange of CO2 and water between plants and the atmosphere, processes vital to plant life(4-6). Increased [ CO2] has been shown to enhance anion channel activity(7) proposed to mediate efflux of osmoregulatory anions ( Cl- and malate(2-)) from guard cells during stomatal closure(8,9). However, the genes encoding anion efflux channels in plant plasma membranes remain unknown. Here we report the isolation of an Arabidopsis gene, SLAC1 ( SLOW ANION CHANNEL-ASSOCIATED 1, At1g12480), which mediates CO2 sensitivity in regulation of plant gas exchange. The SLAC1 protein is a distant homologue of bacterial and fungal C4- dicarboxylate transporters, and is localized specifically to the plasma membrane of guard cells. It belongs to a protein family that in Arabidopsis consists of four structurally related members that are common in their plasma membrane localization, but show distinct tissue- specific expression patterns. The loss- of- function mutation in SLAC1 was accompanied by an over- accumulation of the osmoregulatory anions in guard cell protoplasts. Guard- cell- specific expression of SLAC1 or its family members resulted in restoration of the wild- type stomatal responses, including CO2 sensitivity, and also in the dissipation of the over- accumulated anions. These results suggest that SLAC1-family proteins have an evolutionarily conserved function that is required for the maintenance of organic/ inorganic anion homeostasis on the cellular level.