Carbonic anhydrases are upstream regulators of C[O.sub.2]-controlled stomatal movements in guard cells

• Published in: Nature cell biology Vol. 12; no. 1; pp. 87 - 111
• Main Authors: Hu, Honghong, Boisson-Dernier, Aurelien, Israelsson-Nordstrom, Maria, Bohmer, Maik, Xue, Shaowu, Ries, Amber, Godoski, Jan, Kuhn, Josef M, Schroeder, Julian I
• Format: Journal Article
• Language: English
• Published: Nature Publishing Group 01-01-2010
• Subjects: Carbon dioxide; Cellular signal transduction; Genetic epistasis; Physiological aspects; Plants; Respiration; United States
• ISSN: 1465-7392
• DOI: 10.1038/ncb2009

The continuing rise in atmospheric C[O.sub.2] causes stomatal pores in leaves to close and thus globally affects C[O.sub.2] influx into plants, water use efficiency and leaf heat stress (1-4). However, the C[O.sub.2]-binding proteins that control this response remain unknown. Moreover, which cell type responds to C[O.sub.2], mesophyll or guard cells, and whether photosynthesis mediates this response are matters of debate (5-8). We demonstrate that Arabidopsis thaliana double-mutant plants in the β-carbonic anhydrases βCA1 and βCA4 show impaired C[O.sub.2]-regulation of stomatal movements and increased stomatal density, but retain functional abscisic-acid and blue-light responses. βCA-mediated C[O.sub.2]-triggered stomatal movements are not, in first-order, linked to whole leaf photosynthesis and can function in guard cells. Furthermore, guard cell βCA-overexpressing plants exhibit instantaneous enhanced water use efficiency. Guard cell expression of mammalian αCAII complements the reduced sensitivity of ca1 ca4 plants, showing that carbonic anhydrase-mediated catalysis is an important mechanism for βCA-mediated C[O.sub.2]-induced stomatal closure and patch clamp analyses indicate that C[O.sub.2]/[HCO.sub.3]--transfers the signal to anion channel regulation. These findings, together with ht1-2 (ref. 9) epistasis analysis demonstrate that carbonic anhydrases function early in the C[O.sub.2] signalling pathway, which controls gas-exchange between plants and the atmosphere.