GABA signalling in guard cells acts as a ‘stress memory’ to optimise plant water loss

AbstractThe non-protein amino acid γ-aminobutyric acid (GABA) has been proposed to be an ancient messenger for cellular communication conserved across biological kingdoms. GABA has well-defined signalling roles in animals; however, whilst GABA accumulates in plants under stress it has not been determined if, how, where and when GABA acts as an endogenous plant signalling molecule. Here, we establish that endogenous GABA is a bona fide plant signal, acting via a mechanism not found in animals. GABA antagonises stomatal movement in response to opening and closing stimuli in multiple plant families including dicot and monocot crops. Using Arabidopsis thaliana, we show guard cell GABA production is necessary and sufficient to influence stomatal aperture, transpirational water loss and drought tolerance via inhibition of stomatal guard cell plasma membrane and tonoplast-localised anion transporters. This study proposes a novel role for GABA – as a ‘stress memory’ – opening new avenues for improving plant stress tolerance.

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GABA signalling modulates stomatal opening to enhance plant water use efficiency and drought resilience

Nature Communications ◽

10.1038/s41467-021-21694-3 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Bo Xu ◽

Yu Long ◽

Xueying Feng ◽

Xujun Zhu ◽

Na Sai ◽

...

Keyword(s):

Water Use Efficiency ◽

Water Use ◽

Guard Cell ◽

Plant Stress ◽

Stomatal Opening ◽

Fine Tuning ◽

Protein Amino Acid ◽

Gaba Production ◽

Anion Transporter ◽

Use Efficiency

AbstractThe non-protein amino acid γ-aminobutyric acid (GABA) has been proposed to be an ancient messenger for cellular communication conserved across biological kingdoms. GABA has well-defined signalling roles in animals; however, whilst GABA accumulates in plants under stress it has not been determined if, how, where and when GABA acts as an endogenous plant signalling molecule. Here, we establish endogenous GABA as a bona fide plant signal, acting via a mechanism not found in animals. Using Arabidopsis thaliana, we show guard cell GABA production is necessary and sufficient to reduce stomatal opening and transpirational water loss, which improves water use efficiency and drought tolerance, via negative regulation of a stomatal guard cell tonoplast-localised anion transporter. We find GABA modulation of stomata occurs in multiple plants, including dicot and monocot crops. This study highlights a role for GABA metabolism in fine tuning physiology and opens alternative avenues for improving plant stress resilience.

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

Nature Communications ◽

10.1038/ncomms8879 ◽

2015 ◽

Vol 6 (1) ◽

Cited By ~ 130

Author(s):

Sunita A. Ramesh ◽

Stephen D. Tyerman ◽

Bo Xu ◽

Jayakumar Bose ◽

Satwinder Kaur ◽

...

Keyword(s):

Plant Growth ◽

Root Growth ◽

Site Directed Mutagenesis ◽

Plant Tissues ◽

Physiological Effects ◽

Gamma Aminobutyric Acid ◽

Biotic And Abiotic Stress ◽

Protein Amino Acid ◽

Anion Transporters ◽

Signalling Molecule

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.

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Broad and Complex Roles of NBR1-Mediated Selective Autophagy in Plant Stress Responses

Cells ◽

10.3390/cells9122562 ◽

2020 ◽

Vol 9 (12) ◽

pp. 2562

Author(s):

Yan Zhang ◽

Zhixiang Chen

Keyword(s):

Stress Responses ◽

Mammalian Cells ◽

Plant Stress ◽

Protein Aggregates ◽

Degradation Pathway ◽

Plant Responses ◽

Stress Memory ◽

Selective Autophagy ◽

Cargo Proteins ◽

Plant Stress Responses

Selective autophagy is a highly regulated degradation pathway for the removal of specific damaged or unwanted cellular components and organelles such as protein aggregates. Cargo selectivity in selective autophagy relies on the action of cargo receptors and adaptors. In mammalian cells, two structurally related proteins p62 and NBR1 act as cargo receptors for selective autophagy of ubiquitinated proteins including aggregation-prone proteins in aggrephagy. Plant NBR1 is the structural and functional homolog of mammalian p62 and NBR1. Since its first reports almost ten years ago, plant NBR1 has been well established to function as a cargo receptor for selective autophagy of stress-induced protein aggregates and play an important role in plant responses to a broad spectrum of stress conditions including heat, salt and drought. Over the past several years, important progress has been made in the discovery of specific cargo proteins of plant NBR1 and their roles in the regulation of plant heat stress memory, plant-viral interaction and special protein secretion. There is also new evidence for a possible role of NBR1 in stress-induced pexophagy, sulfur nutrient responses and abscisic acid signaling. In this review, we summarize these progresses and discuss the potential significance of NBR1-mediated selective autophagy in broad plant responses to both biotic and abiotic stresses.

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Analysis of the Phosphorylation Level in Guard-Cell Plasma Membrane H+-ATPase in Response to Fusicoccin

Plant and Cell Physiology ◽

10.1093/pcp/pce055 ◽

2001 ◽

Vol 42 (4) ◽

pp. 424-432 ◽

Cited By ~ 65

Author(s):

Toshinori Kinoshita ◽

Ken-ichiro Shimazaki

Keyword(s):

Plasma Membrane ◽

Guard Cell ◽

Cell Plasma Membrane ◽

Phosphorylation Level ◽

Cell Plasma

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Nitric oxide as a bioactive signalling molecule in plant stress responses

Plant Science ◽

10.1016/j.plantsci.2007.02.005 ◽

2007 ◽

Vol 172 (5) ◽

pp. 876-887 ◽

Cited By ~ 278

Author(s):

Magdalena Arasimowicz ◽

Jolanta Floryszak-Wieczorek

Keyword(s):

Nitric Oxide ◽

Stress Responses ◽

Plant Stress ◽

Signalling Molecule ◽

Plant Stress Responses

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The Permeability of the Guard Cell Plasma Membrane and Tonoplast

Journal of Experimental Botany ◽

10.1093/jxb/41.3.351 ◽

1990 ◽

Vol 41 (3) ◽

pp. 351-358 ◽

Cited By ~ 23

Author(s):

M. BAIER ◽

H. GIMMLER ◽

W. HARTUNG

Keyword(s):

Plasma Membrane ◽

Guard Cell ◽

Cell Plasma Membrane ◽

Cell Plasma

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Investigating the effect of pH, different concentrations of glutamate acid and salt on production in low-fat probiotic cheese

Iranian Journal of Microbiology ◽

10.18502/ijm.v13i3.6402 ◽

2021 ◽

Author(s):

Sharmineh Sharafi ◽

Leila Nateghi ◽

Shahriyar Yousefi

Keyword(s):

Lactic Acid ◽

Lactic Acid Bacteria ◽

Glutamic Acid ◽

Pathogenic Bacteria ◽

Probiotic Bacteria ◽

Gamma Aminobutyric Acid ◽

Low Fat ◽

Protein Amino Acid ◽

Gaba Production ◽

Ultra Filtration

Background and Objectives: Gamma-aminobutyric acid (GABA) is a non-protein amino acid produced by lactic acid bacteria. Among GABA-producing bacteria, lactic acid bacteria have received more attention due to their probiotic nature and properties such as inhibiting pathogenic bacteria, strengthening the immune system, and so on. Materials and Methods: Investigation on the effect of three independent variables including pH (4.7, 4.9 and 5.1), glutamic acid (1, 2 and 3 mgg-1) and salt (2, 2.5 and 3%) on GABA production in low fat cheese by probiotic bacteria. Results: By increasing the amount of glutamic acid and decreasing the pH from 5.1 to 4.7, the amount of GABA production in ultra-filtration cheese significantly increased on the 15th and 30th days of production (p≤0.05), while by increasing the amount of salt the production GABA decreased on the 15th and 30th days. Simultaneous optimal conditions to achieve maximum GABA production in cheese on the 15th and 30th production day was respectively 167.7917 mg/kg-1 and 220.125 mg/ kg-1 using 3 mg/g glutamic acid, 2% salt at pH 4.7. Conclusion: The results showed that by identifying probiotic bacteria with the highest potential for GABA production and optimizing the culture medium, more GABA can be produced in food products and a positive step can be taken to produce pragmatic products and promote consumer health.

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