Proteomic and Metabolomic Profilings Reveal Crucial Functions of γ‑Aminobutyric Acid in Regulating Ionic, Water, and Metabolic Homeostasis in Creeping Bentgrass under Salt Stress

The global emergence of soil salinization poses a serious challenge to many countries and regions. γ-Aminobutyric acid (GABA) is involved in systemic regulation of plant adaptation to salt stress but the underlying molecular and metabolic mechanism still remains largely unknown. The elevated endogenous GABA level by the application of exogenous GABA improved salt tolerance associated with the enhancement of antioxidant capacity, photosynthetic characteristics, osmotic adjustment (OA), and water use efficiency in creeping bentgrass. GABA strongly upregulated transcript levels of AsPPa2, AsATPaB2, AsNHX2/4/6, and AsSOS1/20 in roots involved in enhanced capacity of Na+ compartmentalization and mitigation of Na+ toxicity in the cytosol. Significant downregulation of AsHKT1/4 expression could be induced by GABA in leaves in relation to maintenance of the significantly lower Na+ content and higher K+/Na+ ratio. GABA-depressed aquaporin expression and accumulation induced declines in stomatal conductance and transpiration, thereby reducing water loss in leaves during salt stress. For metabolic regulation, GABA primarily enhanced sugar and amino acid accumulation and metabolism, largely contributing to improved salt tolerance through maintaining OA and metabolic homeostasis. Other major pathways could be related to GABA-induced salt tolerance including increases in antioxidant defense, heat shock proteins, and myo-inositol accumulation in leaves. Integrative analyses of molecular, protein, metabolic, and physiological changes reveal systemic functions of GABA in regulating ionic, water, and metabolic homeostasis in nonhalophytic creeping bentgrass under salt stress.