Large inverted repeats identified by intra-specific comparison of mitochondrial genomes provide insights into the evolution of Agrocybe aegerita

Genomic structure and content of Agrocybe aegerita mitochondrial DNA contain essential information regarding the evolution of this gourmet mushroom. In this study, eight isolates of A. aegerita were sequenced and assembled into complete mitochondrial genomes. The mtDNA of the isolate Ag0067 contained two genotypes, both of which were quadripartite architecture consisting of two identical inverted repeats, separated by a small single-copy region and a large single-copy region. The only difference was opposite directions of the small single-copy region. The mtDNAs ranged from 116,329 bp to 134,035 bp, harboring two large identical inverted repeats. Genes of plasmid-origin were present in regions flanked by inverted repeat ID2. Most of the core genes evolved at a relatively low rate, whereas five tRNA genes located in corresponding regions of Ag0002:1–14000 and Ag0002:50001–61000 showed higher diversity. A long fragment inversion (10 Kb) was suggested to have occurred during the differentiation of two main clades, leading to two different gene orders. The number and distribution of the introns varied greatly among the A. aegerita mtDNAs. Fast invasion of short insertions likely resulted in the diversity of introns as well as other non-coding regions, increasing the variation of the mtDNAs. We raised a model about the evolution of the large repeats to explain the unusual features of A. aegerita mtDNAs. This study constructed quadripartite architecture of A. aegerita mtDNAs analogous to chloroplast DNA, proposed an interconversion model of the divergent mitochondrial genotypes with large inverted repeats. The findings could increase our knowledge of fungal evolution.