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We discuss the origin of 4-aminobutyrate (GABA) from glutamate and polyamines, and its subsequent catabolism to succinic semialdehyde and either succinate or 4-hydroxybutyrate. Promiscuous activities of GABA transaminase, glyoxylate/succinic semialdehyde reductases, and aldehyde dehydrogenase 10As appear to be important determinants of cross-talk among metabolic pathways during stress. Imposition of abiotic stress, as well as genetic or chemical disruption of glutamate decarboxylase, GABA transaminase, and tricarboxylic acid cycle reactions, results in non-cyclic carbon flux in the tricarboxylic acid cycle, demonstrating that stress-induced GABA metabolism is strongly linked with respiration. Metabolic generation of 4-hydroxybutyrate is probably linked to the stimulation of succinic semialdehyde reductase activity by an increasing NADPH/NADP+ ratio. We discuss the potential signaling role of GABA in various processes, including pollen tube guidance, interaction with fungal, bacterial, and invertebrate pests, and stomatal functioning, and argue that further research on short-term responses to stress is required to determine whether or not GABA functions by binding to or regulating the activity of GABA receptor molecules. Finally, we describe how emerging information about the metabolic and signaling roles of GABA is being used to improve plant defenses against biotic and abiotic stresses, and benefit human health.