Dynamic evolution of eukaryotic mitochondrial and nuclear genomes: a case study in the gourmet pine mushroom Tricholoma matsutake

Summary Fungi, as eukaryotic organisms, contain two genomes, the mitochondrial genome and the nuclear genome, in their cells. How the two genomes evolve and correlate to each other is debated. Herein, taking the gourmet pine mushroom Tricholoma matsutake as an example, we performed comparative mitog...

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Published inEnvironmental microbiology Vol. 23; no. 11; pp. 7214 - 7230
Main Authors Zhang, Shu, Bai, Xue, Ren, Li‐Yuan, Sun, Hui‐Hui, Tang, Hui‐Ping, Vaario, Lu‐Min, Xu, Jianping, Zhang, Yong‐Jie
Format Journal Article
LanguageEnglish
Published Hoboken, USA John Wiley & Sons, Inc 01.11.2021
Wiley Subscription Services, Inc
Subjects
Agaricales
Deoxyribonucleic acid
DNA
Eukaryota - genetics
Evolution
Evolutionary genetics
Fungi
Gene sequencing
Genes
Genome, Mitochondrial
Genomes
Heteroplasmy
Introns
Mitochondrial DNA
Mushrooms
Mutation
Mutation rates
Nucleotide sequence
PCR
Phylogeny
Tricholoma - genetics
Tricholoma matsutake
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Summary:Summary Fungi, as eukaryotic organisms, contain two genomes, the mitochondrial genome and the nuclear genome, in their cells. How the two genomes evolve and correlate to each other is debated. Herein, taking the gourmet pine mushroom Tricholoma matsutake as an example, we performed comparative mitogenomic analysis using samples collected from diverse locations and compared the evolution of the two genomes. The T. matsutake mitogenome encodes 49 genes and is rich of repetitive and non‐coding DNAs. Six genes were invaded by up to 11 group I introns, with one cox1 intron cox1P372 showing presence/absence dynamics among different samples. Bioinformatic analyses suggested limited or no evidence of mitochondrial heteroplasmy. Interestingly, hundreds of mitochondrial DNA fragments were found in the nuclear genome, with several larger than 500 nt confirmed by PCR assays and read count comparisons, indicating clear evidence of transfer of mitochondrial DNA into the nuclear genome. Nuclear DNA of T. matsutake showed a higher mutation rate than mitochondrial DNA. Furthermore, we found evidence of incongruence between phylogenetic trees derived from mitogenome and nuclear DNA sequences. Together, our results reveal the dynamic genome evolution of the gourmet pine mushroom.
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ISSN:1462-2912
1462-2920
DOI:10.1111/1462-2920.15792