Letter

Nature 452, 483-486 (27 March 2008) | doi:10.1038/nature06720; Received 22 August 2007; Accepted 14 January 2008; Published online 27 February 2008

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

Juntaro Negi1, Osamu Matsuda1, Takashi Nagasawa1, Yasuhiro Oba1, Hideyuki Takahashi2, Maki Kawai-Yamada3, Hirofumi Uchimiya2,3, Mimi Hashimoto1 & Koh Iba1

  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).

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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