1. Department of Biology, Faculty of Sciences, Kyushu University, Fukuoka 812-8581, Japan
2. Iwate Biotechnology Center, Kitakami, Iwate 024-0003, Japan
3. Institute of Molecular and Cellular Biosciences, The University of Tokyo, Tokyo 113-0032, Japan

Correspondence to: Koh Iba¹ Correspondence and requests for materials should be addressed to K.I. (Email: koibascb@mbox.nc.kyushu-u.ac.jp).

Abstract

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, 2, 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, 5, 6}. Increased [CO₂] has been shown to enhance anion channel activity⁷ 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.

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