NRGA1, a Putative Mitochondrial Pyruvate Carrier, Mediates ABA Regulation of Guard Cell Ion Channels and Drought Stress Responses in Arabidopsis

• Published in: Molecular plant 2014-10, Vol.7 (10), p.1508-1521
• Main Authors: Li, Chun-Long, Wang, Mei, Ma, Xiao-Yan, Zhang, Wei
• Format: Article
• Language: English
• Subjects: ABA; Abscisic Acid - pharmacology; Adaptation, Physiological - drug effects; Amino Acid Sequence; Anion Transport Proteins - chemistry; Anion Transport Proteins - genetics; Anion Transport Proteins - metabolism; Arabidopsis - drug effects; Arabidopsis - genetics; Arabidopsis - physiology; Arabidopsis Proteins - chemistry; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Cell Movement - drug effects; drought stress; Droughts; Genetic Complementation Test; guard cell; inward K+ channel; Ion Channel Gating - drug effects; Membrane Transport Proteins - metabolism; Mitochondria - drug effects; Mitochondria - metabolism; Mitochondrial Membrane Transport Proteins - chemistry; Mitochondrial Membrane Transport Proteins - genetics; Mitochondrial Membrane Transport Proteins - metabolism; Mitochondrial Proteins; mitochondrial pyruvate carrier; Models, Biological; Molecular Sequence Data; Monocarboxylic Acid Transporters; Mutation - genetics; NRGA1; Phylogeny; Plant Stomata - cytology; Plants, Genetically Modified; Potassium Channels - metabolism; Protein Transport - drug effects; Saccharomyces cerevisiae - metabolism; Saccharomyces cerevisiae Proteins; slow anion channel; stomata; Stress, Physiological - drug effects; Subcellular Fractions - drug effects; Subcellular Fractions - metabolism; Transcription, Genetic - drug effects
• ISSN: 1674-2052; 1752-9867
• DOI: 10.1093/mp/ssu061

Abscisic acid (ABA) regulates ion channel activity and stomatal movements in response to drought and other stresses. Here, we show that the Arabidopsis thaliana gene NRGA1 is a putative mitochondrial pyruvate carrier which negatively regulates ABA-induced guard cell signaling. NRGA1 transcript was abundant in the A. thaliana leaf and particularly in the guard cells, and its product was directed to the mitochondria. The heterologous co-expression of NRGA1 and AtMPC1 in yeast complemented a loss-of-function mitochondrial pyruvate carrier (MPC) mutant. The nrga1 loss-of-function mutant was very sensitive to the presence of ABA in the context of stomatal movements, and exhibited a heightened tolerance to drought stress. Disruption of NRGA1 gene resulted in increased ABA inhibition of inward K+ currents and ABA activation of slow anion currents in guard cells. The nrga1/NRGA1 functional complementation lines restored the mutant's phenotypes. Furthermore, transgenic lines of constitutively overexpressing NRGA1 showed opposite stomatal responses, reduced drought tolerance, and ABA sensitivity of guard cell inward K+ channel inhibition and anion channel activation. Our findings highlight a putative role for the mitochondrial pyruvate carrier in guard cell ABA signaling in response to drought. The phytohormone abscisic acid (ABA) is the most well known regulator of guard cell ion channels and stomatal movements in plant stress response. Mitochondrial pyruvate carriers transport pyruvate, the final product of glycolysis, from the cytosol into mitochondrion for consequent cellular substance and energy metabolism. Here, we show that the NRGA1, a putative mitochondrial pyruvate carrier of Arabidopsis, is a negative player in drought- and ABA-induced stomatal movements.