Large-scale genome investigations reveal insights into domestication of cultivated mushrooms

Domestication and cultivation of edible and medicinal mushrooms are ongoing ~1,400-year old evolutionary experiments. There are roughly 55 commercially cultivated mushrooms worldwide; however, genomes for many species are lacking, as is our understanding of mushroom domestication. In this work, 22 high-quality reference genomes, along with 63 transcriptome and 381 re-sequencing data, were reported for the first time. Combined with public genome resources, an integrated omics database (MushDB, http://mushroomomics.com) were constructed including 50 reference genomes, 265 transcriptome and 621 whole-genome re-sequencing data, covering ~90% of the worldwide commercially cultivated mushroom species. Using multi-omics data in MushDB, whole-genome variations of the representative wild and cultivated populations were used for selective sweep analysis to identify putative functional genes contributing to the mushroom domestication. Key genes in the starch and sucrose metabolism and mitogen-activated protein kinase signaling pathway, such as chb1, cdc24 and hog1, were putatively selected in Auricularia cornea, Lentinula edodes, Pleurotus eryngii and Pleurotus tuoliensis, indicating those genes might play important roles during mushroom domestications. The function of hog1 in the low temperature stimulation adaptation and short growth period in cultivation environment, which could facilitate the successful domestication, was validated using CRISPR/Cas9 system. Our work offers valuable and abundant omics open resource for wide research communities and lays solid foundations for multi-purposes in mushroom evolution, genetics, and breeding studies.