Frequent heteroplasmy and recombination in the mitochondrial genomes of the basidiomycete mushroom Thelephora ganbajun

Pengfei Wang,Ke-Qin Zhang,Jianping Xu,Liam Yoell,Cunli Liu,Shanze Yoell,Tao Sha,Jianyong Dong,Fei Mi,Xiaozhao Tang,Dan Yang,Ying Zhang,Xiaoxia He,Jinyan Wu,Yunrun Zhang,Yang Cao

doi:10.1038/s41598-017-01823-z

Abstract

In the majority of sexual eukaryotes, the mitochondrial genomes are inherited uniparentally. As a result, individual organisms are homoplasmic, containing mitochondrial DNA (mtDNA) from a single parent. Here we analyzed the mitochondrial genotypes in Clade I of the gourmet mushroom Thelephora ganbajun from its broad geographic distribution range. A total of 299 isolates from 28 geographic locations were sequenced at three mitochondrial loci: the mitochondrial small ribosomal RNA gene, and the cytochrome c oxidase subunits I (COX1) and III (COX3) genes. Quantitative PCR analyses showed that the strains had about 60–160 copies of mitochondrial genomes per cell. Interestingly, while no evidence of heteroplasmy was found at the 12S rRNA gene, 262 of the 299 isolates had clear evidence of heterogeneity at either the COX1 (261 isolates) or COX3 (12 isolates) gene fragments. The COX1 heteroplasmy was characterized by two types of introns residing at different sites of the same region and at different frequencies among the isolates. Allelic association analyses of the observed mitochondrial polymorphic nucleotide sites suggest that mtDNA recombination is common in natural populations of this fungus. Our results contrast the prevailing view that heteroplasmy, if exists, is only transient in basidiomycete fungi.

Highlights

In the majority of sexual eukaryotes, the mitochondrial genomes are inherited uniparentally
Because the dikaryotic hyphae that come after anastomosis often need extended vegetative growth before fruiting, as expected, fruiting bodies formed by dikaryotic mycelia with homoplasmic mitochondria would contain only one mitochondrial genotype and be homoplasmic
In our preliminary screening of natural genetic variation in the basidiomycete fungus Th. ganbajun, we found that two mitochondrial genes contained sequence heterogeneity within several individual fruiting bodies

Summary

Introduction

In the majority of sexual eukaryotes, the mitochondrial genomes are inherited uniparentally. The dikaryotic mycelia of each mated colony would be a mosaic of mitochondrial genotypes, with most hyphae containing resident parental mtDNA and individual cells are generally homoplasmic. Heteroplasmic cells recovered at mating junctions often segregate quickly to form homoplasmic mycelia and fruiting bodies. In this process, recombination may occur between parental mitochondrial genomes during the segregation of the mitochondrial genotypes and produce fruiting bodies with recombinant mitochondrial genotypes. In our preliminary screening of natural genetic variation in the basidiomycete fungus Th. ganbajun, we found that two mitochondrial genes contained sequence heterogeneity within several individual fruiting bodies. The objective of this study is to characterize the variation pattern of mitochondrial DNA in this species

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Conclusion