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

Wang, Pengfei; Tao, Sha; Zhang, Yunrun; Cao, Yang; Mi, Fei; Cun-li, Liu; Yang, Dan; Tang, Xiaozhao; He, Xiaoliang; Dong, Jianyong; Wu, Jian; Yoell, Shanze; Yoell, Liam; Zhang, Ke‐Qin; Zhang, Ying; Xu, Jianping

doi:10.1038/s41598-017-01823-z

Cited by 18 publications

(15 citation statements)

References 28 publications

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“…Our results add up to the expanding list of basidiomycete mitogenomes that have displayed evidences of hybridization and recombination (Xu et al. 2009; Wang et al. 2017).…”

Section: Discussionsupporting

confidence: 62%

Evidence of Extensive Intraspecific Noncoding Reshuffling in a 169-kb Mitochondrial Genome of a Basidiomycetous Fungus

Lee

Lin

et al. 2019

Genome Biology and Evolution

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Comparative genomics of fungal mitochondrial genomes (mitogenomes) have revealed a remarkable pattern of rearrangement between and within major phyla owing to horizontal gene transfer and recombination. The role of recombination was exemplified at a finer evolutionary time scale in basidiomycetes group of fungi as they display a diversity of mitochondrial DNA inheritance patterns. Here, we assembled mitogenomes of six species from the Hymenochaetales order of basidiomycetes and examined 59 mitogenomes from 2 genetic lineages of Phellinus noxius. Gene order is largely collinear, while intergene regions are major determinants of mitogenome size variation. Substantial sequence divergence was found in shared introns consistent with high horizontal gene transfer frequency observed in yeasts, but we also identified a rare case where an intron was retained in five species since speciation. In contrast to the hyperdiversity observed in nuclear genomes of Phellinus noxius, mitogenomes’ intraspecific polymorphisms at protein-coding sequences are extremely low. Phylogeny network based on introns revealed turnover as well as exchange of introns between two lineages. Strikingly, some strains harbor a mosaic origin of introns from both lineages. Analysis of intergenic sequence indicated substantial differences between and within lineages, and an expansion may be ongoing as a result of exchange between distal intergenes. These findings suggest that the evolution in mitochondrial DNAs is usually lineage specific but chimeric mitotypes are frequently observed, thus capturing the possible evolutionary processes shaping mitogenomes in a basidiomycete. The large mitogenome sizes reported in various basidiomycetes appear to be a result of interspecific reshuffling of intergenes.

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“…Our results add up to the expanding list of basidiomycete mitogenomes that have displayed evidences of hybridization and recombination (Xu et al. 2009; Wang et al. 2017).…”

Section: Discussionsupporting

confidence: 62%

Evidence of Extensive Intraspecific Noncoding Reshuffling in a 169-kb Mitochondrial Genome of a Basidiomycetous Fungus

Lee

Lin

et al. 2019

Genome Biology and Evolution

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“…Thelephora ganbajun is a rare wild edible fungus that is distributed in pine forests in high-altitude areas of Yunnan Province, southwestern China [11][12][13][14][15]. In the present study, we found that T. ganbajun could accumulate zinc in the form of zinc-enriched polysaccharides.…”

Section: Introductionsupporting

confidence: 47%

Distribution of Zinc in Mycelial Cells and Antioxidant and Anti-Inflammatory Activities of Mycelia Zinc Polysaccharides from Thelephora ganbajun TG-01

Zheng

Zhang

et al. 2020

Oxidative Medicine and Cellular Longevity

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This study demonstrates that Thelephora ganbajun had a strong ability to absorb zinc, and zinc can be compartmentally stored in the small vesicles and mainly accumulated in the form of zinc-enriched polysaccharides (zinc content was 25.0±1.27 mg/g). Mycelia zinc polysaccharides (MZPS) and its fractions were isolated. The main fraction (MZPS-2) with the highest antioxidant activity in vitro was composed of mannose : galacturonic acid : glucose : galactose in a molar ratio of 61.19 : 1 : 39.67 : 48.67, with a weight-averaged molecular weight of 5.118×105 Da. MZPS-2 had both α-pyranose and β-pyranose configuration and had a triple helical conformation. By establishing zebrafish models, we found that MZPS-2 can significantly scavenge free radicals, reduce the generation of reactive oxygen species caused by inflammation, and inhibit the recruitment of neutrophils toward the injury site. Therefore, MZPS-2 exhibited antioxidant and anti-inflammatory effects and can be used as a zinc supplement with specific biological activities to alleviate zinc deficiency complications, such as chronic oxidative stress or inflammation.

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“…The mating type genes regulate mating (hyphal fusion) and meiosis. Recent research has shown increasing evidence for mitochondrial DNA recombination under both laboratory and field conditions, though it is widely believed that the inheritance of mitochondrial DNA in fungi is uniparental and non-recombining (Wilson and Xu, 2012;Breton and Stewart, 2015;Xu and Wang, 2015;Wang et al, 2017). Indeed, mutation of a specific gene involved in sex-determination caused the rapid spread of multiple introns in the human pathogenic yeast Cryptococcus neoformans (Yan et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

Comparative Analyses of Mitochondrial Genomes Provide Evolutionary Insights Into Nematode-Trapping Fungi

et al. 2020

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Predatory fungi in Orbiliaceae (Ascomycota) have evolved a diversity of trapping devices that enable them to trap and kill nematodes, other small animals, and protozoans. These trapping devices include adhesive hyphae, adhesive knobs, adhesive networks, constricting rings, and non-constricting rings. Their diversity and practical importance have attracted significant attention from biologists, making them excellent model organisms for studying adaptative evolution and as biological control agents against parasitic nematodes. The putative origins and evolutionary relationships among these carnivorous fungi have been investigated using nuclear protein-encoding genes, but their patterns of mitogenome relationships and divergences remain unknown. Here we analyze and compare the mitogenomes of 12 fungal strains belonging to eight species, including six species representing all four types of nematode trapping devices and two from related but non-predatory fungi. All 12 analyzed mitogenomes were of circular DNA molecules, with lengths ranging from 146,101 bp to 280,699 bp. Gene synteny analysis revealed several gene rearrangements and intron transfers among the mitogenomes. In addition, the number of protein coding genes (PCGs), GC content, AT skew, and GC skew varied among these mitogenomes. The increased number and total size of introns were the main contributors to the length differences among the mitogenomes. Phylogenetic analyses of the protein-coding genes indicated that mitochondrial and nuclear genomes evolved at different rates, and signals of positive selection were found in several genes involved in energy metabolism. Our study provides novel insights into the evolution of nematode-trapping fungi and shall facilitate further investigations of this ecologically and agriculturally important group of fungi.

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

Cited by 18 publications

References 28 publications

Evidence of Extensive Intraspecific Noncoding Reshuffling in a 169-kb Mitochondrial Genome of a Basidiomycetous Fungus

Evidence of Extensive Intraspecific Noncoding Reshuffling in a 169-kb Mitochondrial Genome of a Basidiomycetous Fungus

Distribution of Zinc in Mycelial Cells and Antioxidant and Anti-Inflammatory Activities of Mycelia Zinc Polysaccharides from Thelephora ganbajun TG-01

Comparative Analyses of Mitochondrial Genomes Provide Evolutionary Insights Into Nematode-Trapping Fungi

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