Genomic analyses reveal low mitochondrial and high nuclear diversity in the cyclosporin-producing fungus Tolypocladium inflatum
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Mitochondrial DNA is generally regarded to evolve faster than nuclear DNA in animals, whereas if this is also true in fungi remains unclear. Herein, we annotate the first complete mitochondrial genome (mitogenome) of the cyclosporin-producing fungus Tolypocladium inflatum and report the genome-wide sequence variations among five isolates originating from distantly separated localities. We found that T. inflatum has among the most compact of fungal mitogenomes; its 25 kb DNA molecule encodes all standard fungal mitochondrial genes and harbors only one intron. Transcriptional analyses validated the expression of most conserved genes. We found several uncommon repetitive elements and evidence of gene transfer from the mitochondrion to the nucleus. Phylogenetic analyses confirmed the placement of T. inflatum in the fungal order Hypocreales although there was uncertainty on its family-level affiliation. Comparative genomic analyses among the five isolates identified an overall lower level of intraspecific variation in mitogenomes than in nuclear genomes; however, both the nuclear and mitochondrial genomes revealed similar isolate relationships, not correlating with geographic sources of these isolates. Our study shed new insights into the evolution of the medicinally important ascomycete T. inflatum.
KeywordsTolypocladium inflatum Mitochondrial genome Transcriptome Comparative genomics Phylogeny Evolution
The authors thank USDA-ARS Collection of Entomopathogenic Fungal Cultures for providing T. inflatum isolates.
This study was funded by the National Natural Science Foundation of China (81102759), the Natural Science Foundation of Shanxi Province (2014021030-2, 201601D011065), the Fund Program for the Scientific Activities of Selected Returned Overseas Professionals in Shanxi Province, and the Research Project Supported by Shanxi Scholarship Council of China (2017-015).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no competing interests.
This article does not contain any studies with human participants or animals performed by any of the authors.
- Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D, Luo S, McCurdy S, Foy M, Ewan M, Roth R, George D, Eletr S, Albrecht G, Vermaas E, Williams SR, Moon K, Burcham T, Pallas M, DuBridge RB, Kirchner J, Fearon K, Mao J, Corcoran K (2000) Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat Biotech 18:630–634CrossRefGoogle Scholar
- Bushley KE, Raja R, Jaiswal P, Cumbie JS, Nonogaki M, Boyd AE, Owensby CA, Knaus BJ, Elser J, Miller D, Di Y, McPhail KL, Spatafora JW (2013) The genome of Tolypocladium inflatum: evolution, organization, and expression of the cyclosporin biosynthetic gene cluster. PLoS Genet 9:e1003496CrossRefPubMedPubMedCentralGoogle Scholar
- Chen K, Wallis JW, McLellan MD, Larson DE, Kalicki JM, Pohl CS, McGrath SD, Wendl MC, Zhang Q, Locke DP, Shi X, Fulton RS, Ley TJ, Wilson RK, Ding L, Mardis ER (2009) BreakDancer: an algorithm for high-resolution mapping of genomic structural variation. Nat Methods 6:677–681CrossRefPubMedPubMedCentralGoogle Scholar
- Gams W (1971) Tolypocladium, eine Hyphomycetengattung mit geschwollenen Phialiden. Persoonia 6:185–191Google Scholar
- Ghikas D, Kouvelis V, Typas M (2006) The complete mitochondrial genome of the entomopathogenic fungus Metarhizium anisopliae var. anisopliae: gene order and trn gene clusters reveal a common evolutionary course for all Sordariomycetes, while intergenic regions show variation. Arch Microbiol 185:393–401CrossRefPubMedGoogle Scholar
- Jung PP, Friedrich A, Reisser C, Hou J, Schacherer J (2012) Mitochondrial genome evolution in a single protoploid yeast species. G3-Genes Genom. G E N 2:1103–1111Google Scholar
- Kouvelis VN, Ghikas DV, Typas MA (2004) The analysis of the complete mitochondrial genome of Lecanicillium muscarium (synonym Verticillium lecanii) suggests a minimum common gene organization in mtDNAs of Sordariomycetes: phylogenetic implications. Fungal Genet Biol 41:930–940CrossRefPubMedGoogle Scholar
- Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2016) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 34:772–773Google Scholar
- Oh J, Kong WS, Sung GH (2014) Complete mitochondrial genome of the entomopathogenic fungus Beauveria pseudobassiana (Ascomycota, Cordycipitaceae). Mitochondr DNA 26:777–778Google Scholar
- Quandt CA, Kepler RM, Gams W, Araujo JP, Ban S, Evans HC, Hughes D, Humber R, Hywel-Jones N, Li Z, Luangsa-Ard JJ, Rehner SA, Sanjuan T, Sato H, Shrestha B, Sung GH, Yao YJ, Zare R, Spatafora JW (2014) Phylogenetic-based nomenclatural proposals for Ophiocordycipitaceae (Hypocreales) with new combinations in Tolypocladium. IMA Fungus 5:121–134CrossRefPubMedPubMedCentralGoogle Scholar