Metabolic and physiological coordination of drought response and recovery in Porlieria chilensis

Abstract

During drought stress and subsequent recovery, plants adjust their water–carbon dynamics, typically increasing intrinsic water-use efficiency (iWUE) and mobilizing non-structural carbohydrate (NSC) pools. However, in tree species, the physiological and metabolic changes underlying these adjustments remains poorly understood because their larger size, slower turnover rates, and complex compartmentalization of carbon and water fluxes make difficult to capture coordinated whole-plant responses under natural drought–recovery cycles. In Porlieria chilensis, a species currently classified as vulnerable, we performed short- and long-term drought experiments, followed by recovery conditions in juvenile trees to investigate sugar-mediated responses associated with the dynamics of NSC, iWUE and primary metabolites by combining enzymatic activities, δ¹³C and δ¹⁸O, respiration rates and omics technologies. Long-term drought increased significantly iWUEmes (integrating mesophyll conductance and δ¹³C) due to stomatal closure, and decreased starch content coinciding with an inactivation of ADP-glucose pyrophosphorylase (AGPase) activity. Short-term recovery restored photosynthetic activities to pre-stress levels, while long-term recovery triggered the upregulation of several sugar-related enzymes to replenish NSC pools, and the accumulation of metabolites involved in osmotic regulation and polyamine metabolism. We concluded that a sugar futile cycle may help to sustain leaf carbon metabolism, supporting osmotic balance and carbon reserves during prolonged drought and recovery in this species. Overall, these findings improved understanding of carbon dynamics and stress-induced metabolic imprinting in woody species, providing insights for restoration strategies and predicting plant responses to climate change.