Genomic and evolutionary evidence for drought adaptation of allopolyploid Brachypodium hybridum

Climate change is increasing 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 responses using allotetraploid Brachypodium hybridum (B. hybridum) and its progenitor diploid species Brachypodium stacei (B. stacei). Our findings suggest that progenitor species’ genomic legacies resulting from hybridization and whole-genome duplications conferred greater ecological adaptive advantages to B. hybridum compared with B. stacei. Genes related to stomatal regulation and the 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 and B. distachyon-type) 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 intrinsic water-use efficiency than B. stacei, driven by a highly correlated coexpression network involving genes in the circadian rhythm pathway. In summary, our study shows 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.