Transposable Elements versus the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles
Transposable elements (TEs) are exceptional contributors to eukaryotic genome diversity. Their ubiquitous presence impacts the genomes of nearly all species and mediates genome evolution by causing mutations and chromosomal rearrangements and by modulating gene expression. We performed an exhaustive...
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| Published in | PLoS genetics Vol. 12; no. 6; p. e1006108 |
|---|---|
| Main Authors | , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
13.06.2016
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1553-7404 1553-7390 1553-7404 |
| DOI | 10.1371/journal.pgen.1006108 |
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| Abstract | Transposable elements (TEs) are exceptional contributors to eukaryotic genome diversity. Their ubiquitous presence impacts the genomes of nearly all species and mediates genome evolution by causing mutations and chromosomal rearrangements and by modulating gene expression. We performed an exhaustive analysis of the TE content in 18 fungal genomes, including strains of the same species and species of the same genera. Our results depicted a scenario of exceptional variability, with species having 0.02 to 29.8% of their genome consisting of transposable elements. A detailed analysis performed on two strains of Pleurotus ostreatus uncovered a genome that is populated mainly by Class I elements, especially LTR-retrotransposons amplified in recent bursts from 0 to 2 million years (My) ago. The preferential accumulation of TEs in clusters led to the presence of genomic regions that lacked intra- and inter-specific conservation. In addition, we investigated the effect of TE insertions on the expression of their nearby upstream and downstream genes. Our results showed that an important number of genes under TE influence are significantly repressed, with stronger repression when genes are localized within transposon clusters. Our transcriptional analysis performed in four additional fungal models revealed that this TE-mediated silencing was present only in species with active cytosine methylation machinery. We hypothesize that this phenomenon is related to epigenetic defense mechanisms that are aimed to suppress TE expression and control their proliferation. |
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| AbstractList | Transposable elements (TEs) are exceptional contributors to eukaryotic genome diversity. Their ubiquitous presence impacts the genomes of nearly all species and mediates genome evolution by causing mutations and chromosomal rearrangements and by modulating gene expression. We performed an exhaustive analysis of the TE content in 18 fungal genomes, including strains of the same species and species of the same genera. Our results depicted a scenario of exceptional variability, with species having 0.02 to 29.8% of their genome consisting of transposable elements. A detailed analysis performed on two strains of Pleurotus ostreatus uncovered a genome that is populated mainly by Class I elements, especially LTR-retrotransposons amplified in recent bursts from 0 to 2 million years (My) ago. The preferential accumulation of TEs in clusters led to the presence of genomic regions that lacked intra- and inter-specific conservation. In addition, we investigated the effect of TE insertions on the expression of their nearby upstream and downstream genes. Our results showed that an important number of genes under TE influence are significantly repressed, with stronger repression when genes are localized within transposon clusters. Our transcriptional analysis performed in four additional fungal models revealed that this TE-mediated silencing was present only in species with active cytosine methylation machinery. We hypothesize that this phenomenon is related to epigenetic defense mechanisms that are aimed to suppress TE expression and control their proliferation. Transposable elements (TEs) are exceptional contributors to eukaryotic genome diversity. Their ubiquitous presence impacts the genomes of nearly all species and mediates genome evolution by causing mutations and chromosomal rearrangements and by modulating gene expression. We performed an exhaustive analysis of the TE content in 18 fungal genomes, including strains of the same species and species of the same genera. Our results depicted a scenario of exceptional variability, with species having 0.02 to 29.8% of their genome consisting of transposable elements. A detailed analysis performed on two strains of Pleurotus ostreatus uncovered a genome that is populated mainly by Class I elements, especially LTR-retrotransposons amplified in recent bursts from 0 to 2 million years (My) ago. The preferential accumulation of TEs in clusters led to the presence of genomic regions that lacked intra- and inter-specific conservation. In addition, we investigated the effect of TE insertions on the expression of their nearby upstream and downstream genes. Our results showed that an important number of genes under TE influence are significantly repressed, with stronger repression when genes are localized within transposon clusters. Our transcriptional analysis performed in four additional fungal models revealed that this TE-mediated silencing was present only in species with active cytosine methylation machinery. We hypothesize that this phenomenon is related to epigenetic defense mechanisms that are aimed to suppress TE expression and control their proliferation.Transposable elements (TEs) are exceptional contributors to eukaryotic genome diversity. Their ubiquitous presence impacts the genomes of nearly all species and mediates genome evolution by causing mutations and chromosomal rearrangements and by modulating gene expression. We performed an exhaustive analysis of the TE content in 18 fungal genomes, including strains of the same species and species of the same genera. Our results depicted a scenario of exceptional variability, with species having 0.02 to 29.8% of their genome consisting of transposable elements. A detailed analysis performed on two strains of Pleurotus ostreatus uncovered a genome that is populated mainly by Class I elements, especially LTR-retrotransposons amplified in recent bursts from 0 to 2 million years (My) ago. The preferential accumulation of TEs in clusters led to the presence of genomic regions that lacked intra- and inter-specific conservation. In addition, we investigated the effect of TE insertions on the expression of their nearby upstream and downstream genes. Our results showed that an important number of genes under TE influence are significantly repressed, with stronger repression when genes are localized within transposon clusters. Our transcriptional analysis performed in four additional fungal models revealed that this TE-mediated silencing was present only in species with active cytosine methylation machinery. We hypothesize that this phenomenon is related to epigenetic defense mechanisms that are aimed to suppress TE expression and control their proliferation. Transposable elements (TEs) are exceptional contributors to eukaryotic genome diversity. Their ubiquitous presence impacts the genomes of nearly all species and mediates genome evolution by causing mutations and chromosomal rearrangements and by modulating gene expression. We performed an exhaustive analysis of the TE content in 18 fungal genomes, including strains of the same species and species of the same genera. Our results depicted a scenario of exceptional variability, with species having 0.02 to 29.8% of their genome consisting of transposable elements. A detailed analysis performed on two strains of Pleurotus ostreatus uncovered a genome that is populated mainly by Class I elements, especially LTR-retrotransposons amplified in recent bursts from 0 to 2 million years (My) ago. The preferential accumulation of TEs in clusters led to the presence of genomic regions that lacked intra- and inter-specific conservation. In addition, we investigated the effect of TE insertions on the expression of their nearby upstream and downstream genes. Our results showed that an important number of genes under TE influence are significantly repressed, with stronger repression when genes are localized within transposon clusters. Our transcriptional analysis performed in four additional fungal models revealed that this TE-mediated silencing was present only in species with active cytosine methylation machinery. We hypothesize that this phenomenon is related to epigenetic defense mechanisms that are aimed to suppress TE expression and control their proliferation. Transposable elements (TEs) are enigmatic genetic units that have played important roles in the evolution of eukaryotic genomes. Since their discovery in the 1950s, they have gained increasing attention and are known today as active genome modelers in multiple species. Although these elements have been widely studied in plants, much less is known about their occurrence and impact on the fungal kingdom. Using a diverse set of basidiomycete and ascomycete fungi, we quantified and characterized a huge diversity of DNA and RNA transposable elements, and we identified species that had 0.02 to 29.8% of their genomes occupied by transposable elements. In addition, using our basidiomycete model Pleurotus ostreatus , we demonstrated how TE insertions produced detrimental effects on the expression of upstream and downstream genes, which were downregulated compared with the control groups. This silencing mechanism was present in the basidiomycetes tested but exhibited a patchy distribution in ascomycetes, and might be related to specific genome defense mechanisms that control transposon proliferation. This finding reveals the broader impact of transposable elements in fungi. In addition to their importance as long-term evolutionary forces, they play major roles in the more dynamic transcriptome regulation of certain species. Transposable elements (TEs) are exceptional contributors to eukaryotic genome diversity. Their ubiquitous presence impacts the genomes of nearly all species and mediates genome evolution by causing mutations and chromosomal rearrangements and by modulating gene expression. We performed an exhaustive analysis of the TE content in 18 fungal genomes, including strains of the same species and species of the same genera. Our results depicted a scenario of exceptional variability, with species having 0.02 to 29.8% of their genome consisting of transposable elements. A detailed analysis performed on two strains of Pleurotus ostreatus uncovered a genome that is populated mainly by Class I elements, especially LTR-retrotransposons amplified in recent bursts from 0 to 2 million years (My) ago. The preferential accumulation of TEs in clusters led to the presence of genomic regions that lacked intra- and inter-specific conservation. In addition, we investigated the effect of TE insertions on the expression of their nearby upstream and downstream genes. Our results showed that an important number of genes under TE influence are significantly repressed, with stronger repression when genes are localized within transposon clusters. Our transcriptional analysis performed in four additional fungal models revealed that this TE-mediated silencing was present only in species with active cytosine methylation machinery. We hypothesize that this phenomenon is related to epigenetic defense mechanisms that are aimed to suppress TE expression and control their proliferation. |
| Audience | Academic |
| Author | LaButti, Kurt Ramírez, Lucía Schmutz, Jeremy Borgognone, Alessandra Pérez, Gúmer Pisabarro, Antonio G. López-Varas, Leticia Lapidus, Alla Castanera, Raúl Grimwood, Jane Grigoriev, Igor V. Stajich, Jason E. |
| AuthorAffiliation | 2 U.S. Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America 3 Center for Algorithmic Biotechnology, St. Petersburg State University, St. Petersburg, Russia 4 Hudson Alpha Institute for Biotechnology, Huntsville, Alabama, United States of America University of Utah School of Medicine, UNITED STATES 1 Genetics and Microbiology Research Group, Department of Agrarian Production, Public University of Navarre, Pamplona, Navarre, Spain 5 Department of Plant Pathology and Microbiology, Institute for Integrative Genome Biology, University of California-Riverside, Riverside, California, United States of America |
| AuthorAffiliation_xml | – name: 1 Genetics and Microbiology Research Group, Department of Agrarian Production, Public University of Navarre, Pamplona, Navarre, Spain – name: University of Utah School of Medicine, UNITED STATES – name: 4 Hudson Alpha Institute for Biotechnology, Huntsville, Alabama, United States of America – name: 5 Department of Plant Pathology and Microbiology, Institute for Integrative Genome Biology, University of California-Riverside, Riverside, California, United States of America – name: 3 Center for Algorithmic Biotechnology, St. Petersburg State University, St. Petersburg, Russia – name: 2 U.S. Department of Energy Joint Genome Institute, Walnut Creek, California, United States of America |
| Author_xml | – sequence: 1 givenname: Raúl surname: Castanera fullname: Castanera, Raúl – sequence: 2 givenname: Leticia surname: López-Varas fullname: López-Varas, Leticia – sequence: 3 givenname: Alessandra surname: Borgognone fullname: Borgognone, Alessandra – sequence: 4 givenname: Kurt surname: LaButti fullname: LaButti, Kurt – sequence: 5 givenname: Alla surname: Lapidus fullname: Lapidus, Alla – sequence: 6 givenname: Jeremy surname: Schmutz fullname: Schmutz, Jeremy – sequence: 7 givenname: Jane surname: Grimwood fullname: Grimwood, Jane – sequence: 8 givenname: Gúmer orcidid: 0000-0003-2153-1962 surname: Pérez fullname: Pérez, Gúmer – sequence: 9 givenname: Antonio G. surname: Pisabarro fullname: Pisabarro, Antonio G. – sequence: 10 givenname: Igor V. surname: Grigoriev fullname: Grigoriev, Igor V. – sequence: 11 givenname: Jason E. orcidid: 0000-0002-7591-0020 surname: Stajich fullname: Stajich, Jason E. – sequence: 12 givenname: Lucía surname: Ramírez fullname: Ramírez, Lucía |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27294409$$D View this record in MEDLINE/PubMed https://www.osti.gov/servlets/purl/1378343$$D View this record in Osti.gov |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2016 Public Library of Science 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles. PLoS Genet 12(6): e1006108. doi:10.1371/journal.pgen.1006108 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles. PLoS Genet 12(6): e1006108. doi:10.1371/journal.pgen.1006108 |
| Copyright_xml | – notice: COPYRIGHT 2016 Public Library of Science – notice: 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles. PLoS Genet 12(6): e1006108. doi:10.1371/journal.pgen.1006108 – notice: 2016 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles. PLoS Genet 12(6): e1006108. doi:10.1371/journal.pgen.1006108 |
| CorporateAuthor | Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States) |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 USDOE Office of Science (SC) AGL2014-55971-R; AC02-05CH11231 Conceived and designed the experiments: RC JES LR. Performed the experiments: RC LLV AB. Analyzed the data: RC JES LR. Contributed reagents/materials/analysis tools: KL AL JES JG GP JS. Wrote the paper: RC AGP IVG JES LR. The authors have declared that no competing interests exist. |
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| Snippet | Transposable elements (TEs) are exceptional contributors to eukaryotic genome diversity. Their ubiquitous presence impacts the genomes of nearly all species... Transposable elements (TEs) are exceptional contributors to eukaryotic genome diversity. Their ubiquitous presence impacts the genomes of nearly all species... |
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| SubjectTerms | 60 APPLIED LIFE SCIENCES Ascomycota - genetics Base Sequence BASIC BIOLOGICAL SCIENCES Biology and Life Sciences Datasets Defense mechanisms Deoxyribonucleic acid DNA DNA methylation DNA sequencing DNA Transposable Elements - genetics DNA, Fungal - genetics Epigenetics Eukaryotes Fungi Gene expression Genome, Fungal - genetics Genomes Methods Mutation Observations Phylogenetics Physiological aspects Pleurotus - genetics Pleurotus ostreatus Proteins Research and Analysis Methods Retroelements - genetics Sequence Alignment Sequence Analysis, DNA Studies Transcription (Genetics) Transcription, Genetic - genetics Transposons |
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| Title | Transposable Elements versus the Fungal Genome: Impact on Whole-Genome Architecture and Transcriptional Profiles |
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