Domestication reduces drought tolerance in watermelon through loss of root plasticity traits

Abstract

Wild plants, particularly those native to xeric environments, are highly adapted to survive under harsh conditions. These adaptive strategies primarily ensure the successful transfer of genetic material to subsequent generations, often independently of fruit size or quality. In contrast, more than 10,000 years of domestication have shifted plant strategies away from survival-oriented traits toward increase in yield and fruit quality. In this study, we characterized both shared and divergent physiological traits contributing to drought tolerance in wild and domesticated watermelon genotypes. Specifically, we compared above- and belowground responses to water limitation in desert watermelon (Citrullus colocynthis) versus these in a watermelon cultivar (Citrullus lanatus). While aboveground responses to water scarcity were largely similar between the two genotypes, pronounced differences emerged belowground. Root biomass and surface area in the cultivated watermelon were predominantly concentrated in the upper soil layers. In contrast, desert watermelon displayed substantial root system plasticity under drought conditions. Although total root biomass remained largely distributed in the upper soil layers, root surface area shifted toward deeper soil layers, indicating enhanced water acquisition from deeper soil layers without additional biomass investment. These findings suggest that domesticated watermelon, despite originating from desert-adapted ancestors, has largely lost the capacity for dynamic root system adjustment in response to spatial and temporal variation in soil water availability.