Journal Article

SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling

Brosché, Mikael, Desikan, Radhika, Lamminmäki, Airi, Valerio, Gabriel, Vahisalu, Triin, Kollist, Hannes, Chan, Wai-Yin, Moldau, Heino, Wang, Yong-Fei, Nishimura, Noriyuki

2008

Overview

A stomatal ion channel The stomata on the undersides of leaves control the exchange of carbon dioxide and water between plants and the atmosphere. Stomatal pore aperture is regulated by transport of ions and metabolites across guard-cell membranes. Perhaps surprisingly, until now no plant plasma membrane anion channel subunits have been cloned — and the homologues of animal anion channels have been shown not to encode functional ion channels in plants. Now two groups working independently have identified a protein that is an essential component for S-type anion channel function and is required for stomatal closure in response to a variety of physiological and stress stimuli. Termed SLAC1, it is a distant homologue of fungal and bacterial dicarboxylate/malic acid transport proteins. One of two related studies that describe the identification of a protein which is an essential component for S-type anion channel function and is required for stomatal closure in response to a variety of physiological and stress stimuli including carbon dioxide and ozone. Stomatal pores, formed by two surrounding guard cells in the epidermis of plant leaves, allow influx of atmospheric carbon dioxide in exchange for transpirational water loss. Stomata also restrict the entry of ozone — an important air pollutant that has an increasingly negative impact on crop yields, and thus global carbon fixation 1 and climate change 2 . The aperture of stomatal pores is regulated by the transport of osmotically active ions and metabolites across guard cell membranes 3 , 4 . Despite the vital role of guard cells in controlling plant water loss 3 , 4 , ozone sensitivity 1 , 2 and CO 2 supply 2 , 5 , 6 , 7 , the genes encoding some of the main regulators of stomatal movements remain unknown. It has been proposed that guard cell anion channels function as important regulators of stomatal closure and are essential in mediating stomatal responses to physiological and stress stimuli 3 , 4 , 8 . However, the genes encoding membrane proteins that mediate guard cell anion efflux have not yet been identified. Here we report the mapping and characterization of an ozone-sensitive Arabidopsis thaliana mutant, slac1 . We show that SLAC1 ( SLOW ANION CHANNEL-ASSOCIATED 1 ) is preferentially expressed in guard cells and encodes a distant homologue of fungal and bacterial dicarboxylate/malic acid transport proteins. The plasma membrane protein SLAC1 is essential for stomatal closure in response to CO 2 , abscisic acid, ozone, light/dark transitions, humidity change, calcium ions, hydrogen peroxide and nitric oxide. Mutations in SLAC1 impair slow (S-type) anion channel currents that are activated by cytosolic Ca 2+ and abscisic acid, but do not affect rapid (R-type) anion channel currents or Ca 2+ channel function. A low homology of SLAC1 to bacterial and fungal organic acid transport proteins, and the permeability of S-type anion channels to malate 9 suggest a vital role for SLAC1 in the function of S-type anion channels.

• Publisher: Nature Publishing Group UK,Nature Publishing,Nature Publishing Group
• Subject: Abscisic Acid / Abscisic Acid - metabolism / Abscisic Acid - pharmacology / Air pollution / Animals / anions / Anions - metabolism / Arabidopsis / Arabidopsis - cytology / Arabidopsis - drug effects / Arabidopsis - metabolism / Arabidopsis - radiation effects / Arabidopsis Proteins / Arabidopsis Proteins - genetics / Arabidopsis Proteins - metabolism / Arabidopsis thaliana / Biological and medical sciences / Botany / Calcium / Calcium - metabolism / Calcium - pharmacology / Carbon dioxide / Carbon fixation / Cell physiology / Cellular biology / Climate change / Crop yield / cytology / Darkness / dicarboxylate malic acid transport proteins / drug effects / Environment / Epidermis / Fundamental and applied biological sciences. Psychology / Genetics / guard cells / Humanities and Social Sciences / Humidity / Hydrogen Peroxide / Hydrogen Peroxide - metabolism / Hydrogen Peroxide - pharmacology / Ion Channel Gating / Ion Channel Gating - drug effects / Ion Channel Gating - radiation effects / ion channels / Ion Channels - metabolism / ion transport / Ion Transport - drug effects / Ion Transport - radiation effects / Ions / Leaves / letter / Light / Membrane Proteins / Membrane Proteins - genetics / Membrane Proteins - metabolism / Membranes / metabolism / Metabolites / multidisciplinary / mutants / Mutation / Nicotiana - cytology / Nicotiana - metabolism / Nitric Oxide / Nitric Oxide - metabolism / Onions / Onions - metabolism / Oocytes / Organic acids / Ozone / Ozone - metabolism / Ozone - pharmacology / Permeability / pharmacology / Physiology / Plant Leaves / Plant Leaves - drug effects / Plant Leaves - metabolism / Plant physiology and development / Plant Stomata / Plant Stomata - drug effects / Plant Stomata - metabolism / Plant Stomata - radiation effects / Plants / Plasma membrane and permeation / Pollutants / Pores / Proteins / radiation effects / S-type anion channels / Science / Science (multidisciplinary) / Signal Transduction / Signal Transduction - drug effects / Signal Transduction - radiation effects / SLAC1 protein / Slow Anion Channel-Associated 1 protein / Stomata / stomatal movement / Tobacco / transporters / Water / Water - metabolism / Water loss / Xenopus