Heterotrimeric Gβ subunit orchestrates flavonoid metabolism governing drought-tolerance in groundnut ( Arachis hypogaea L.)

Groundnut ( Arachis hypogaea ) is an important oilseed crop, and its production is severely affected by drought worldwide. Improving the drought-tolerance of groundnut without compromising its agronomic traits is a major challenge for researchers. Here, a meta-transcriptome analysis identified tandemly duplicated Gβ subunits ( AhGβ1 and AhGβ3 ) as early signaling genes under water deficit conditions. Heterotrimeric G-protein β-subunit is a major signaling element that can regulate diverse responses in plants. Heterologous complementation studies in Arabidopsis Gβ mutant ( agb1-2 ) demonstrated evolutionary conservation of AhGβ function, while the transgenic overexpression and RNAi knockdown in groundnut established AhGβ1 as a positive regulator of plant growth, yield, and drought tolerance. Integrated transcriptomic, transcription factor regulatory network, and metabolomic analyses demonstrated that AhGβ1 coordinates drought-responsive transcriptional and metabolic reprogramming characterized by suppression of cell wall-associated processes and activation of phenylpropanoid, flavonoid, and isoflavonoid biosynthesis. This reprogramming resulted in enhanced accumulation of antioxidant flavonoids, including quercetin and rutin, reduced ROS accumulation, and improved drought tolerance. Furthermore, exogenous application of these flavonoids enhanced drought recovery, highlighting their role as protective downstream metabolites. Collectively, our findings establish AhGβ1 as a conserved regulator linking early G-protein signaling with transcriptional and metabolic reprogramming to maintain redox homeostasis during drought stress and identify promising molecular and metabolic targets for improving drought resilience in groundnut.