Bi-directional Selection in Upland Rice Leads to Its Adaptive Differentiation from Lowland Rice in Drought Resistance and Productivity.

Drought resistance is required in rice breeding to address the challenge of frequent droughts. However, the evolutionary mechanism of rice drought resistance is not fully understood. We investigated the genetic differentiation between upland and lowland rice domesticated in agro-ecosystems with contrasting water-soil conditions using genome-wide SNPs. We estimated morphological differences among upland and lowland rice in drought resistance and productivity through common garden experiments. Upland rice had better drought resistance but poorer productivity. The negative correlations between traits of drought resistance and productivity are attributed to the underlying genetic trade-offs through tight linkages (e.g., DCA1 and OsCesA7) or pleiotropic effects (e.g., LAX1). The genetic trade-offs are common and greatly shape the evolution of drought resistance in upland rice. In genomic regions associated with both productivity and drought resistance, signs of balancing selection were detected in upland rice, while signs of directional selection were detected in lowland rice, potentially contributing to their adaptive differentiation. Signs of balancing selection in upland rice resulted from bi-directional selection during its domestication in drought-prone upland agro-ecosystems. Using genome-wide association analysis, we identified several valuable quantitative trait loci associated with drought resistance, for which highly differentiated genes should be considered candidates. Bi-directional selection breaking tight linkages by accumulating recombination events would be applicable in breeding water-saving and drought-resistance rice.