Aluminum-activated malate transporters can facilitate GABA transport

Sunita A. Ramesh, Muhammad Kamran, Wendy Sullivan, Larissa Chirkova, Mamoru Okamoto, Fien Degryse, Michael McLaughlin, Matthew Gilliham, Stephen D. Tyerman

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

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 via14C-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.

Original languageEnglish
Pages (from-to)1147-1164
Number of pages19
JournalPlant Cell
Volume30
Issue number5
DOIs
Publication statusPublished - May 2018
Externally publishedYes

Keywords

  • ALMTs
  • anion channels
  • malate efflux
  • endogenous GABA concentrations

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  • Cite this

    Ramesh, S. A., Kamran, M., Sullivan, W., Chirkova, L., Okamoto, M., Degryse, F., McLaughlin, M., Gilliham, M., & Tyerman, S. D. (2018). Aluminum-activated malate transporters can facilitate GABA transport. Plant Cell, 30(5), 1147-1164. https://doi.org/10.1105/tpc.17.00864