Insight into the evolutionary and domesticated history of the most widely cultivated mushroom Agaricus bisporus via mitogenome sequences of 361 global strains

Abstract

Agaricus bisporus is the most widely cultivated edible mushroom in the world with a only around three hundred years known history of cultivation. Therefore, it represents an ideal organism not only to investigate the natural evolutionary history but also the understanding on the evolution going back to the early era of domestication. In this study, we generated the mitochondrial genome sequences of 352 A. bisporus strains and 9 strains from 4 closely related species around the world. The population mitogenomic study revealed all A. bisporus strains can be divided into seven clades, and all domesticated cultivars present only in two of those clades. The molecular dating analysis showed this species origin in Europe on 4.6 Ma and we proposed the main dispersal routes. The detailed mitogenome structure studies showed that the insertion of the plasmid-derived dpo gene caused a long fragment (MIR) inversion, and the distributions of the fragments of dpo gene were strictly in correspondence with these seven clades. Our studies also showed A. bisporus population contains 30 intron distribution patterns (IDPs), while all cultivars contain only two IDPs, which clearly exhibit intron loss compared to the others. Either the loss occurred before or after domestication, that could suggest that the change facilitates their adaptation to the cultivated environment.

Keywords: Button mushroom; Domestication; Mitogenome; Phylogenomic; Population genomics.

Fig. 1

Mitogenomes of four outgroup species and seven clades of A. bisporus. A representative strain for each of the four outgroup species and seven clades of A. bisporus are selected for display (A. sinodilicious: ZRL20160001, A. cf. subfloccosus: BS716, A. qilianensis: QL20170217, A. sinotetrasporus: QL20170258, Clade eurotetrasporus: BS423, Clade China: ZRL20170159, Clade America I: BS305-05, Clade America II: BS109, Clade European I: BS226, Clade European II: BS134, Clade European III: BS175). The mitogenome size, and annotation information are shown in this figure. Homologous regions between genomes are connected by lines

Fig. 2

Phylogenomic and population structure analysis. 1666 SNP data from the mitochondrial genomes of 361 strains were used. The Outgroup and the seven clades in which A. bisporus are divided are marked in the figure. The genuine wild strains, cultivar-like strains and cultivar strains are distinguished by a different color on the strain name. The outer circles show the results of the population structure analysis for K values of 3 to 9, respectively

Fig. 3

Principal component analysis. The same SNP data as for Fig. 2 were used for principal component analysis and a 3-dimensional stereogram was constructed using the first three principal components. The four outgroup species and the seven clades of A. bisporus strains are represented using different shapes and colors

Fig. 4

Haplotype network structure analysis. The same SNP data as for Fig. 2 were used for haplotype network structure analysis. The four outgroup species and the seven clades of A. bisporus strains are represented using different colors of Circles. Each circle represents a haplotype, with larger diameter circles representing more strains with this haplotype

Fig. 5

Inference of divergence time, transmission routes. The diagram on the left shows the inferred divergence times and migration events of A. bisporus. The divergence times of each branch are indicated. The diagram on the right shows the presumed route of its spread

Fig. 6

Structural differences in the mitogenomes of the four outgroup species and the seven clades of A. bisporus. The mitogenomes of seven clades of A. bisporus and four outgroup species have distinct structural differences in the region between atp9 and rrnS. Each genome has two segments with the same sequence and in opposite directions, named IRS. A segment between IRS has different direction in different clades, named MIR

Fig. 7

dpo fragments distribution in each Clades. A total of eight different fragments of the dpo gene were found in A. bisporus. The diagram shows the length of each dpo fragments and its distribution in each clade. Green blocks indicate the presence of the dpo fragment and, conversely, yellow blocks indicate the absence of the fragment. Site* indicates the ranking of the dpo fragment in the genome of the clade

Fig. 8

IDP in each Clades of A. bisporus. A total of 30 different IDPs (intron distribution patterns) were found in A. bisporus. The diagram shows introns that differed among the clades and identical introns were removed. The diagram shows the IDPs for each clade, the origin of the strains and its number in each IDP, and the number of introns in cox1