Aluminium activated malate transporters facilitate GABA transport in plants

Ramesh SA, Gilliham M and Tyerman SD

ARC Centre of Excellence in Plant Energy Biology, School of Agriculture, Food and Wine, Waite Research Institute, University of Adelaide, Glen Osmond, SA 5064 Australia.

Gamma-aminobutyric acid (GABA) is a neurotransmitter regulating membrane potential in nerve cells. GABA rapidly accumulates in plant tissues in response to various stresses, and regulates growth. We identified GABA-binding sites within plant Aluminium-activated Malate Transporter (ALMT) proteins with homology to GABA-binding motifs of mammalian GABAA receptors (GABA-gated anion channels). The ALMTs are currently classified as anion channels but are also regulated by diverse signals leading to a range of physiological responses. We have previously demonstrated that anion flux through ALMTs is negatively regulated by GABA and its analogs with an EC50 in the low micromolar range[1]. We also observed that activation of wheat ALMT (TaALMT1) led to a negative correlation between malate efflux and endogenous GABA concentrations in root tips and heterologous expression systems. Recently we have shown that this negative correlation is a result of GABA efflux facilitated by TaALMT1[2]. Activation of TaALMT1 leads to GABA transport into the cells demonstrated by yeast complementation and 14C[GABA] uptake into Xenopus oocytes. GABA transport into yeast was observed for all ALMTs we examined. Interestingly, mutation of residue (TaALMT1F213C) in the GABA motif prevented GABA influx and efflux in the multiple test systems we used, and abolished the negative correlation between anion efflux and GABA concentration. GABA and malate thus appear to interact with ALMTs in a complex manner to regulate each others transport and this is suggestive of a role for ALMTs in communicating metabolic status of cells. 1. Ramesh, S., et al., GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters. Nature Communications, 2015. 6: p. 7879. 2. Ramesh, S.A., et al., Aluminium-Activated Malate Transporters Can Facilitate GABA Transport. Plant Cell, 2018. 30 (5) 1147-1164; DOI: https://doi.org/10.1105/tpc.17.00864.