A large-scale population genomic study has shed new light on the evolutionary and domestication history of the button mushroom (Agaricus bisporus), one of the most widely cultivated edible fungi in the world.

Led by Prof. ZHAO Ruilin from the Institute of Microbiology of the Chinese Academy of Sciences, the researchers showed how climate dynamics and a key gene for adaptive evolution and domestication jointly shaped the mushroom's diversity.

This work was published in Current Biology on January 8.

By analyzing whole-genome resequencing data from 482 wild and commercial A. bisporus strains collected worldwide, the researchers revealed that geographic isolation caused by the Quaternary glaciation likely drove A. bisporus divergence around two million years ago (Mya), centered in North America and Europe. This led to the formation of three distinct varieties. Interglacial expansions subsequently facilitated extensive gene flow among populations, promoting mixed origins in today's A. bisporus var. bisporus populations.

The researchers also revealed a key genetic mechanism underlying the domestication of A. bisporus. Kinship inference demonstrated that the white cap was the key trait selected during button mushroom domestication.

Through selective sweeps and genome-wide association studies (GWAS), the researchers traced the cap color variation of A. bisporus to the polyphenol oxidase 1 gene (AbPPO1) on chromosome 8, which encodes a key enzyme in melanin biosynthesis. The evolution of a functional mutant haplotype of the AbPPO1 gene is positively associated with population evolution and cap color variation in A. bisporus. White strains have a unique haplotype, AbPPO1Hap-2, which is derived from a light-colored haplotype and forms the genetic basis of button mushroom domestication.

Additionally, protein structure analysis suggested that amino acid variations within AbPPO1Hap-2 caused structural changes in the protein, while transgenic experiments demonstrated that this haplotype carries a loss-of-function mutation in the AbPPO1 gene.

By integrating evolutionary genomics and domestication genetics, this study highlights the impact of historical climate dynamics on the biodiversity of mushroom-forming fungi. It illustrates the genetic complexity of button mushroom domestication and provides a genomic framework for utilizing and improving A. bisporus germplasm resources.

This work was supported by the National Key R&D Program of China, the National Natural Science Foundation of China and Beijing Innovation Consortium of Agriculture Research System.