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The non-protein amino acid γ-aminobutyric acid (GABA) rapidly accumulates in plant tissues in response to salinity. However, the physiological rationale for this elevation remains elusive. This study compared electrophysiological and whole-plant responses of salt-treated Arabidopsis mutants pop2-5 and gad1,2 , which have different abilities to accumulate GABA. The pop2-5 mutant, which was able to overaccumulate GABA in its roots, showed a salt-tolerant phenotype. On the contrary, the gad1,2 mutant, lacking the ability to convert glutamate to GABA, showed oversensitivity to salinity. The greater salinity tolerance of the pop2-5 line was explained by: (i) the role of GABA in stress-induced activation of H+-ATPase, thus leading to better membrane potential maintenance and reduced stress-induced K+ leak from roots; (ii) reduced rates of net Na+ uptake; (iii) higher expression of SOS1 and NHX1 genes in the leaves, which contributed to reducing Na+ concentration in the cytoplasm by excluding Na+ to apoplast and sequestering Na+ in the vacuoles; (iv) a lower rate of H2O2 production and reduced reactive oxygen species-inducible K+ efflux from root epidermis; and (v) better K+ retention in the shoot associated with the lower expression level of GORK channels in plant leaves. [ABSTRACT FROM AUTHOR]