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Small, but surprisingly repetitive genomes: transposon expansion and not polyploidy has driven a doubling in genome size in a metazoan species complex
BACKGROUND: The causes and consequences of genome size variation across Eukaryotes, which spans five orders of magnitude, have been hotly debated since before the advent of genome sequencing. Previous studies have mostly examined variation among larger taxonomic units (e.g., orders, or genera), whil...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2019
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6555955/ https://www.ncbi.nlm.nih.gov/pubmed/31174483 http://dx.doi.org/10.1186/s12864-019-5859-y |
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author | Blommaert, J. Riss, S. Hecox-Lea, B. Mark Welch, D. B. Stelzer, C. P. |
author_facet | Blommaert, J. Riss, S. Hecox-Lea, B. Mark Welch, D. B. Stelzer, C. P. |
author_sort | Blommaert, J. |
collection | PubMed |
description | BACKGROUND: The causes and consequences of genome size variation across Eukaryotes, which spans five orders of magnitude, have been hotly debated since before the advent of genome sequencing. Previous studies have mostly examined variation among larger taxonomic units (e.g., orders, or genera), while comparisons among closely related species are rare. Rotifers of the Brachionus plicatilis species complex exhibit a seven-fold variation in genome size and thus represent a unique opportunity to study such changes on a relatively short evolutionary timescale. Here, we sequenced and analysed the genomes of four species of this complex with nuclear DNA contents spanning 110–422 Mbp. To establish the likely mechanisms of genome size change, we analysed both sequencing read libraries and assemblies for signatures of polyploidy and repetitive element content. We also compared these genomes to that of B. calyciflorus, the closest relative with a sequenced genome (293 Mbp nuclear DNA content). RESULTS: Despite the very large differences in genome size, we saw no evidence of ploidy level changes across the B. plicatilis complex. However, repetitive element content explained a large portion of genome size variation (at least 54%). The species with the largest genome, B. asplanchnoidis, has a strikingly high 44% repetitive element content, while the smaller B. plicatilis genomes contain between 14 and 25% repetitive elements. According to our analyses, the B. calyciflorus genome contains 39% repetitive elements, which is substantially higher than previously reported (21%), and suggests that high repetitive element load could be widespread in monogonont rotifers. CONCLUSIONS: Even though the genome sizes of these species are at the low end of the metazoan spectrum, their genomes contain substantial amounts of repetitive elements. Polyploidy does not appear to play a role in genome size variations in these species, and these variations can be mostly explained by changes in repetitive element content. This contradicts the naïve expectation that small genomes are streamlined, or less complex, and that large variations in nuclear DNA content between closely related species are due to polyploidy. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5859-y) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-6555955 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-65559552019-06-10 Small, but surprisingly repetitive genomes: transposon expansion and not polyploidy has driven a doubling in genome size in a metazoan species complex Blommaert, J. Riss, S. Hecox-Lea, B. Mark Welch, D. B. Stelzer, C. P. BMC Genomics Research Article BACKGROUND: The causes and consequences of genome size variation across Eukaryotes, which spans five orders of magnitude, have been hotly debated since before the advent of genome sequencing. Previous studies have mostly examined variation among larger taxonomic units (e.g., orders, or genera), while comparisons among closely related species are rare. Rotifers of the Brachionus plicatilis species complex exhibit a seven-fold variation in genome size and thus represent a unique opportunity to study such changes on a relatively short evolutionary timescale. Here, we sequenced and analysed the genomes of four species of this complex with nuclear DNA contents spanning 110–422 Mbp. To establish the likely mechanisms of genome size change, we analysed both sequencing read libraries and assemblies for signatures of polyploidy and repetitive element content. We also compared these genomes to that of B. calyciflorus, the closest relative with a sequenced genome (293 Mbp nuclear DNA content). RESULTS: Despite the very large differences in genome size, we saw no evidence of ploidy level changes across the B. plicatilis complex. However, repetitive element content explained a large portion of genome size variation (at least 54%). The species with the largest genome, B. asplanchnoidis, has a strikingly high 44% repetitive element content, while the smaller B. plicatilis genomes contain between 14 and 25% repetitive elements. According to our analyses, the B. calyciflorus genome contains 39% repetitive elements, which is substantially higher than previously reported (21%), and suggests that high repetitive element load could be widespread in monogonont rotifers. CONCLUSIONS: Even though the genome sizes of these species are at the low end of the metazoan spectrum, their genomes contain substantial amounts of repetitive elements. Polyploidy does not appear to play a role in genome size variations in these species, and these variations can be mostly explained by changes in repetitive element content. This contradicts the naïve expectation that small genomes are streamlined, or less complex, and that large variations in nuclear DNA content between closely related species are due to polyploidy. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-5859-y) contains supplementary material, which is available to authorized users. BioMed Central 2019-06-07 /pmc/articles/PMC6555955/ /pubmed/31174483 http://dx.doi.org/10.1186/s12864-019-5859-y Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Blommaert, J. Riss, S. Hecox-Lea, B. Mark Welch, D. B. Stelzer, C. P. Small, but surprisingly repetitive genomes: transposon expansion and not polyploidy has driven a doubling in genome size in a metazoan species complex |
title | Small, but surprisingly repetitive genomes: transposon expansion and not polyploidy has driven a doubling in genome size in a metazoan species complex |
title_full | Small, but surprisingly repetitive genomes: transposon expansion and not polyploidy has driven a doubling in genome size in a metazoan species complex |
title_fullStr | Small, but surprisingly repetitive genomes: transposon expansion and not polyploidy has driven a doubling in genome size in a metazoan species complex |
title_full_unstemmed | Small, but surprisingly repetitive genomes: transposon expansion and not polyploidy has driven a doubling in genome size in a metazoan species complex |
title_short | Small, but surprisingly repetitive genomes: transposon expansion and not polyploidy has driven a doubling in genome size in a metazoan species complex |
title_sort | small, but surprisingly repetitive genomes: transposon expansion and not polyploidy has driven a doubling in genome size in a metazoan species complex |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6555955/ https://www.ncbi.nlm.nih.gov/pubmed/31174483 http://dx.doi.org/10.1186/s12864-019-5859-y |
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