Genomic and evolutionary evidence for drought adaptation of grass allopolyploid Brachypodium hybridum

Climate change increases the frequency and severity of drought worldwide, threatening the environmental resilience of cultivated grasses. However, the genetic diversity in many wild grasses could contribute to the development of climate-adapted varieties. Here, we elucidated the impact of polyploidy on drought response using allotetraploid Brachypodium hybridum (Bh) and its progenitor diploid species B. stacei (Bs). Our findings suggest that progenitor species genomic legacies resulting from hybridization and whole-genome duplications conferred greater ecological adaptive advantages to Bh over Bs. Genes related to stomatal regulation and immune response from S-subgenomes were under positive selection during speciation, underscoring their evolutionary importance in adapting to environmental stresses. Biased expression in polyploid subgenomes [B. stacei-type (Bhs) and B. distachyon-type (Bhd)] significantly influenced differential gene expression, with the dominant subgenome exhibiting more differential expression. B. hybridum adapted a drought escape strategy characterized by higher photosynthetic capacity and lower WUEi than Bs, driven by a highly correlated co-expression network involving genes in the circadian rhythm pathway. In summary, our study showed the influence of polyploidy on ecological and environmental adaptation and resilience in model Brachypodium grasses. These insights hold promise for informing the breeding of climate-resilient cereal crops and pasture grasses.