Telomere-to-Telomere Genome Sequences across a Single Genus Reveal Highly Variable Chromosome Rearrangement Rates but Absolute Stasis of Chromosome Number
Genome rearrangements in filamentous fungi are prevalent but little is known about the modalities of their evolution, in part because few complete genomes are available within a single genus. To address this, we have generated and compared 15 complete telomere-to-telomere genomes across the phylogen...
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| Format: | Article |
| Language: | English |
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MDPI AG
2022-06-01
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| Series: | Journal of Fungi |
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| Online Access: | https://www.mdpi.com/2309-608X/8/7/670 |
| _version_ | 1797446000835559424 |
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| author | Mathieu Quenu Artemis D. Treindl Kate Lee Daigo Takemoto Torsten Thünen Samad Ashrafi David Winter Austen R. D. Ganley Adrian Leuchtmann Carolyn A. Young Murray P. Cox |
| author_facet | Mathieu Quenu Artemis D. Treindl Kate Lee Daigo Takemoto Torsten Thünen Samad Ashrafi David Winter Austen R. D. Ganley Adrian Leuchtmann Carolyn A. Young Murray P. Cox |
| author_sort | Mathieu Quenu |
| collection | DOAJ |
| description | Genome rearrangements in filamentous fungi are prevalent but little is known about the modalities of their evolution, in part because few complete genomes are available within a single genus. To address this, we have generated and compared 15 complete telomere-to-telomere genomes across the phylogeny of a single genus of filamentous fungi, <i>Epichloë</i>. We find that the striking distinction between gene-rich and repeat-rich regions previously reported for isolated species is ubiquitous across the <i>Epichloë</i> genus. We built a species phylogeny from single-copy gene orthologs to provide a comparative framing to study chromosome composition and structural change through evolutionary time. All <i>Epichloë</i> genomes have exactly seven nuclear chromosomes, but despite this conserved ploidy, analyses reveal low synteny and substantial rearrangement of gene content across the genus. These rearrangements are highly lineage-dependent, with most occurring over short evolutionary distances, with long periods of structural stasis. Quantification of chromosomal rearrangements shows they are uncorrelated with numbers of substitutions and evolutionary distances, suggesting that different modes of evolution are acting to create nucleotide and chromosome-scale changes. |
| first_indexed | 2024-03-09T13:34:07Z |
| format | Article |
| id | doaj.art-3f7f0c6dc4be456795e1e094703619d4 |
| institution | Directory Open Access Journal |
| issn | 2309-608X |
| language | English |
| last_indexed | 2024-03-09T13:34:07Z |
| publishDate | 2022-06-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Journal of Fungi |
| spelling | doaj.art-3f7f0c6dc4be456795e1e094703619d42023-11-30T21:14:01ZengMDPI AGJournal of Fungi2309-608X2022-06-018767010.3390/jof8070670Telomere-to-Telomere Genome Sequences across a Single Genus Reveal Highly Variable Chromosome Rearrangement Rates but Absolute Stasis of Chromosome NumberMathieu Quenu0Artemis D. Treindl1Kate Lee2Daigo Takemoto3Torsten Thünen4Samad Ashrafi5David Winter6Austen R. D. Ganley7Adrian Leuchtmann8Carolyn A. Young9Murray P. Cox10School of Natural Sciences, Massey University, Palmerston North 4442, New ZealandPlant Ecological Genetics, Institute of Integrative Biology, ETH Zürich, 8092 Zürich, SwitzerlandSchool of Natural Sciences, Massey University, Palmerston North 4442, New ZealandGraduate School of Bioagricultural Sciences, Nagoya University, Nagoya 464-8601, JapanJulius Kühn Institute–Federal Research Centre for Cultivated Plants, Institute for Crop and Soil Science, 38116 Braunschweig, GermanyJulius Kühn Institute–Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, 38116 Braunschweig, GermanySchool of Natural Sciences, Massey University, Palmerston North 4442, New ZealandSchool of Biological Sciences, University of Auckland, Auckland 1010, New ZealandPlant Ecological Genetics, Institute of Integrative Biology, ETH Zürich, 8092 Zürich, SwitzerlandNoble Research Institute, Ardmore, OK 73401, USASchool of Natural Sciences, Massey University, Palmerston North 4442, New ZealandGenome rearrangements in filamentous fungi are prevalent but little is known about the modalities of their evolution, in part because few complete genomes are available within a single genus. To address this, we have generated and compared 15 complete telomere-to-telomere genomes across the phylogeny of a single genus of filamentous fungi, <i>Epichloë</i>. We find that the striking distinction between gene-rich and repeat-rich regions previously reported for isolated species is ubiquitous across the <i>Epichloë</i> genus. We built a species phylogeny from single-copy gene orthologs to provide a comparative framing to study chromosome composition and structural change through evolutionary time. All <i>Epichloë</i> genomes have exactly seven nuclear chromosomes, but despite this conserved ploidy, analyses reveal low synteny and substantial rearrangement of gene content across the genus. These rearrangements are highly lineage-dependent, with most occurring over short evolutionary distances, with long periods of structural stasis. Quantification of chromosomal rearrangements shows they are uncorrelated with numbers of substitutions and evolutionary distances, suggesting that different modes of evolution are acting to create nucleotide and chromosome-scale changes.https://www.mdpi.com/2309-608X/8/7/670<i>Epichloë</i>genome structurechromosome evolutionstructural variation |
| spellingShingle | Mathieu Quenu Artemis D. Treindl Kate Lee Daigo Takemoto Torsten Thünen Samad Ashrafi David Winter Austen R. D. Ganley Adrian Leuchtmann Carolyn A. Young Murray P. Cox Telomere-to-Telomere Genome Sequences across a Single Genus Reveal Highly Variable Chromosome Rearrangement Rates but Absolute Stasis of Chromosome Number Journal of Fungi <i>Epichloë</i> genome structure chromosome evolution structural variation |
| title | Telomere-to-Telomere Genome Sequences across a Single Genus Reveal Highly Variable Chromosome Rearrangement Rates but Absolute Stasis of Chromosome Number |
| title_full | Telomere-to-Telomere Genome Sequences across a Single Genus Reveal Highly Variable Chromosome Rearrangement Rates but Absolute Stasis of Chromosome Number |
| title_fullStr | Telomere-to-Telomere Genome Sequences across a Single Genus Reveal Highly Variable Chromosome Rearrangement Rates but Absolute Stasis of Chromosome Number |
| title_full_unstemmed | Telomere-to-Telomere Genome Sequences across a Single Genus Reveal Highly Variable Chromosome Rearrangement Rates but Absolute Stasis of Chromosome Number |
| title_short | Telomere-to-Telomere Genome Sequences across a Single Genus Reveal Highly Variable Chromosome Rearrangement Rates but Absolute Stasis of Chromosome Number |
| title_sort | telomere to telomere genome sequences across a single genus reveal highly variable chromosome rearrangement rates but absolute stasis of chromosome number |
| topic | <i>Epichloë</i> genome structure chromosome evolution structural variation |
| url | https://www.mdpi.com/2309-608X/8/7/670 |
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