GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters.

Sunita A Ramesh,Matthew Gilliham,Stephen D Tyerman,Jayakumar Bose,Peter R Ryan,Satwinder Kaur,Sergey Shabala,Patricia Domingos,Stefanie Wege,Sana Ullah,Vanessa Conn,José A Feijó,Bo Xu

doi:10.1038/ncomms8879

Abstract

The non-protein amino acid, gamma-aminobutyric acid (GABA) rapidly accumulates in plant tissues in response to biotic and abiotic stress, and regulates plant growth. Until now it was not known whether GABA exerts its effects in plants through the regulation of carbon metabolism or via an unidentified signalling pathway. Here, we demonstrate that anion flux through plant aluminium-activated malate transporter (ALMT) proteins is activated by anions and negatively regulated by GABA. Site-directed mutagenesis of selected amino acids within ALMT proteins abolishes GABA efficacy but does not alter other transport properties. GABA modulation of ALMT activity results in altered root growth and altered root tolerance to alkaline pH, acid pH and aluminium ions. We propose that GABA exerts its multiple physiological effects in plants via ALMT, including the regulation of pollen tube and root growth, and that GABA can finally be considered a legitimate signalling molecule in both the plant and animal kingdoms.

Highlights

The non-protein amino acid, gamma-aminobutyric acid (GABA) rapidly accumulates in plant tissues in response to biotic and abiotic stress, and regulates plant growth
Using near-isogenic lines (NILs) of bread wheat (Triticum aestivum, Ta) that differ in their Al3 þ tolerance, we found that GABA concentrations under acidic conditions were significantly higher in roots of the Al3 þ -tolerant NIL ET8 compared with those of ES8, the Al3 þ -sensitive NIL
We found that muscimol—a potent analogue of GABA and specific agonist of mammalian GABAA receptors5—selectively reduced malate efflux and root growth of ET8 (Fig. 1c)

Summary

Introduction

The non-protein amino acid, gamma-aminobutyric acid (GABA) rapidly accumulates in plant tissues in response to biotic and abiotic stress, and regulates plant growth. Elevated GABA concentrations reduce root growth[3], while GABA gradients are required in the female reproductive tissues to guide pollen tubes to the ovary to ensure successful fertilization[4] This has led to speculation that GABA signalling occurs in plants, as it does in mammals[1,2,5]. While examining the effect of combining stresses that can modulate plant growth individually[1,2,3], we observed an unexpected interplay between acidosis, trivalent aluminium ions (Al3 þ ) and GABA accumulation This finding has led us to the identification of aluminium-activated malate transporters (ALMT) as key transducers of GABA signalling in plants. Our findings reveal that GABA-mediated regulation of ALMT proteins underlies a novel signalling pathway that has the potential to translate changes in the concentration of this plant stress metabolite into physiological outputs throughout the plant

Methods

Results

Conclusion