Gamma-aminobutyric acid (GABA) alleviates salt damage in tomato by modulating Na+ uptake, the GAD gene, amino acid synthesis and reactive oxygen species metabolism

Abstract

Background Salt stress is a serious abiotic stress that caused crop growth inhibition and yield decline. Previous studies have reported on the the synthesis of gamma-aminobutyric acid (GABA) and its relationship with plant resistance under various abiotic stress. However, the relationship between exogenous GABA alleviating plant salt stress damage and ion flux, amino acid synthesis, and key enzyme expression remains largely unclear. We investigated plant growth, Na+ transportation and accumulation, reactive oxygen species (ROS) metabolism and evaluated the effect of GABA on amino acids, especially SlGADs gene expression and the endogenous GABA content of tomato (Solanum lycopersicum L.) seedlings treated with or without 5 mmol·L− 1 GABA under 175 mmol·L− 1 NaCl stress. Results Exogenous application of GABA significantly reduced the salt damage index and increased plant height, chlorophyll content and the dry and fresh weights of tomato plants exposed to NaCl stress. GABA significantly reduced Na+ accumulation in leaves and roots by preventing Na+ influx in roots and transportation to leaves. The transcriptional expression of SlGAD1–3 genes were induced by NaCl stress especially with GABA application. Among them, SlGAD1 expression was the most sensitive and contributed the most to the increase in glutamate decarboxylase (GAD) activity induced by NaCl and GABA application; Exogenous GABA increased GAD activity and amino acid contents in tomato leaves compared with the levels under NaCl stress alone, especially the levels of endogenous GABA, proline, glutamate and eight other amino acids. These results indicated that SlGADs transcriptional expression played an important role in tomato plant resistance to NaCl stress with GABA application by enhancing GAD activity and amino acid contents. GABA significantly alleviated the active oxygen-related injury of leaves under NaCl stress by increasing the activities of antioxidant enzymes and decreasing the contents of active oxygen species and malondialdehyde. Conclusion Exogenous GABA had a positive effect on the resistance of tomato seedlings to salt stress, which was closely associated with reducing Na+ flux from root to leaves, increasing amino acid content and strengthening antioxidant metabolism. Endogenous GABA content was induced by salt and exogenous GABA at both the transcriptional and metabolic levels.

Comparative Transcriptomics and Metabolomics Reveal an Intricate Priming Mechanism Involved in PGPR-Mediated Salt Tolerance in Tomato

“…In Arabidopsis, knockout mutants with T-DNA insertion in asparagine synthetase 2 gene exhibited limited salt tolerance and impaired nitrogen assimilation and translocation by the NaCl treatment relative to the wild-type (Maaroufi-Dguimi et al, 2011). In spite of the fact that GABA has been reported to alleviate salt stress injury in tomato seedlings by modifications in ion flux, amino acid synthesis and key enzyme expression (Wu et al, 2020), no similar relation was found in this study. Moreover, the increased levels of threonine and serine after AXSa06 inoculation revealed the modification of "glycine, serine, and threonine metabolism" pathway in response to inoculum at control conditions.…”

The versatile GABA in plants

“… 115 , 116 In salt-treated wheat leaves, key metabolic enzymes required for the cyclic operation of the TCA cycle reportedly were physiochemically inhibited by salt, but the increase in GABA shunt activity provided an alternative carbon source for the TCA cycle to function in mitochondria and bypassed salt-sensitive enzymes to facilitate the increase in leaf respiration in wheat plants. 117 Further, the application of exogenous GABA to maize, 118 white clover, 119 muskmelon, 120 germinated hull-less barley, 121 and tomato 122 increases endogenous GABA content, activates enzymatic antioxidant activity, alleviates salt damage to plants, and enhances plant salt-tolerance.…”

γ-Aminobutyrate (GABA) Regulated Plant Defense: Mechanisms and Opportunities

“…Table 4 briefly summarizes many examples from the literature wherein tolerance to hypoxia, drought, salinity, chilling, heat, osmotic stress and proton stress, as well as heavy metals (i.e., aluminum, arsenic and chromium) is improved in vegetative organs by the application of exogenous GABA [ 39 , 150 , 151 , 152 , 153 , 154 , 155 , 156 , 157 , 158 , 159 , 160 , 161 , 162 , 163 , 164 , 165 , 166 , 167 , 168 , 169 , 170 , 171 , 172 , 173 , 174 , 175 , 176 , 177 , 178 , 179 , 180 , 181 , 182 , 183 , 184 ]. The application of exogenous GABA typically increases the level of endogenous GABA, and elicits a diverse range of biochemical, molecular and physiological responses.…”