Aluminum-Activated Malate Transporters Can Facilitate GABA Transport

• Published in: The Plant cell Vol. 30; no. 5; pp. 1147 - 1164
• Main Authors: Ramesh, Sunita A., Kamran, Muhammad, Sullivan, Wendy, Chirkova, Larissa, Okamoto, Mamoru, Degryse, Fien, McLaughlin, Michael, Gilliham, Matthew, Tyerman, Stephen D.
• Format: Journal Article
• Language: English
• Published: United States American Society of Plant Biologists 01.05.2018
• Subjects: Activation; Aluminum; Amino acids; Anion channels; Anions; Binding sites; Carbon 14; Communication; Complementation; Efflux; Ion channels; Malate; Metabolism; Oocytes; Physiological responses; Proteins; Receptors; Tips; Transport; Wheat; Yeast; Yeasts; γ-Aminobutyric acid A receptors
• ISSN: 1040-4651; 1532-298X
• DOI: 10.1105/tpc.17.00864

Plant aluminum-activated malate transporters (ALMTs) are currently classified as anion channels; they are also known to be regulated by diverse signals, leading to a range of physiological responses. Gamma-aminobutyric acid (GABA) regulation of anion flux through ALMT proteins requires a specific amino acid motif in ALMTs that shares similarity with a GABA binding site in mammalian GABAA receptors. Here, we explore why TaALMT1 activation leads to a negative correlation between malate efflux and endogenous GABA concentrations ([GABA]i) in both wheat (Triticum aestivum) root tips and in heterologous expression systems. We show that TaALMT1 activation reduces [GABA]i because TaALMT1 facilitates GABA efflux but GABA does not complex Al3+. TaALMT1 also leads to GABA transport into cells, demonstrated by a yeast complementation assay and via 14C-GABA uptake into TaALMT1-expressing Xenopus laevis oocytes; this was found to be a general feature of all ALMTs we examined. Mutation of the GABA motif (TaALMT1F213C) prevented both GABA influx and efflux, and resulted in no correlation between malate efflux and [GABA]i. We conclude that ALMTs are likely to act as both GABA and anion transporters in planta. GABA and malate appear to interact with ALMTs in a complex manner to regulate each other’s transport, suggestive of a role for ALMTs in communicating metabolic status.