Genomic signatures of evolution and domestication in the button mushroom Agaricus bisporus

The evolutionary and domestication history of mushroom-forming fungi remains poorly understood despite their ecological and economic significance. Here, we present the first large-scale population genomic study of the button mushroom (Agaricus bisporus), the world's most cultivated edible mushroom, integrating resequencing data from 482 global wild and commercial strains. Our analyses reveal a complex evolutionary history shaped by Quaternary glacial cycles. We find that geographic isolation caused by the Quaternary glaciation likely drove A. bisporus divergence around 2 mya centered in North America and Europe, with three distinct varieties, while interglacial expansions facilitated extensive gene flow between populations, promoting mixed origins in current A. bisporus var. bisporus populations. Our analyses demonstrated the white cap trait was the key artificial selective trait for domestication, and we successfully connected this domestication trait and its functional gene and found that cap-color evolution might be associated with the diverse function of AbPPO1, whose allele frequency trajectories supported a similar complex evolution process as the A. bisporus var. bisporus populations. By bridging evolutionary genomics with domestication genetics, our findings underscore the role of historical climate dynamics in shaping the biodiversity of mushroom-forming fungi, illustrate the genetic complexity of the button mushroom domestication, and provide a genomic framework for the utilization and improvement of A. bisporus germplasm resources.