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

Abstract

The continuing rise in atmospheric [CO2] is predicted to have diverse and dramatic effects on the productivity of agriculture, plant ecosystems and gas exchange1,2,3. Stomatal pores in the epidermis provide gates for the exchange of CO2 and water between plants and the atmosphere, processes vital to plant life4,5,6. Increased [CO2] has been shown to enhance anion channel activity7 proposed to mediate efflux of osmoregulatory anions (Cl and malate2–) from guard cells during stomatal closure8,9. 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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Figure 1: The slac1 mutations impair CO 2 -, ABA- and dark-induced stomatal closure.
Figure 2: Tissue-specific expression and subcellular localization of SLAC1-family proteins.
Figure 3: Implication of SLAC1-family proteins in the maintenance of ion homeostasis across the plant plasma membranes.

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Acknowledgements

We thank M. H. Sato for providing the tonoplast control plants, I. C. Mori for technical advice, and N. Kawahara for technical assistance. This research was supported by a Core Research for Evolution and Technology (CREST)-type JST grant and a JSPS grant, and by the Ministry of Agriculture, Forestry and Fisheries of Japan (Rice Genome Project IP-5005) grants (K.I.). J.N. is the recipient of scholarships from JSPS and Nara Institute of Science and Technology (NAIST). M.H. is the JST post-doctoral fellow.

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Correspondence to Koh Iba.

Additional information

Arabidopsis Genome Initiative (AGI) identifiers for SLAC1-family members are: SLAC1, At1g12480; SLAH1, At1g62280; SLAH2, At4g27970; and SLAH3, At5g24030.

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Negi, J., Matsuda, O., Nagasawa, T. et al. CO2 regulator SLAC1 and its homologues are essential for anion homeostasis in plant cells. Nature 452, 483–486 (2008). https://doi.org/10.1038/nature06720

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