Transposable element and host silencing activity in gigantic genomes
Transposable elements (TEs) and the silencing machinery of their hosts are engaged in a germline arms-race dynamic that shapes TE accumulation and, therefore, genome size. In animal species with extremely large genomes (>10 Gb), TE accumulation has been pushed to the extreme, prompting the qu...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-02-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2023.1124374/full |
| _version_ | 1797895444905328640 |
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| author | Jie Wang Liang Yuan Jiaxing Tang Jiaxing Tang Jiongyu Liu Cheng Sun Michael W. Itgen Guiying Chen Stanley K. Sessions Guangpu Zhang Guangpu Zhang Rachel Lockridge Mueller |
| author_facet | Jie Wang Liang Yuan Jiaxing Tang Jiaxing Tang Jiongyu Liu Cheng Sun Michael W. Itgen Guiying Chen Stanley K. Sessions Guangpu Zhang Guangpu Zhang Rachel Lockridge Mueller |
| author_sort | Jie Wang |
| collection | DOAJ |
| description | Transposable elements (TEs) and the silencing machinery of their hosts are engaged in a germline arms-race dynamic that shapes TE accumulation and, therefore, genome size. In animal species with extremely large genomes (>10 Gb), TE accumulation has been pushed to the extreme, prompting the question of whether TE silencing also deviates from typical conditions. To address this question, we characterize TE silencing via two pathways—the piRNA pathway and KRAB-ZFP transcriptional repression—in the male and female gonads of Ranodon sibiricus, a salamander species with a ∼21 Gb genome. We quantify 1) genomic TE diversity, 2) TE expression, and 3) small RNA expression and find a significant relationship between the expression of piRNAs and TEs they target for silencing in both ovaries and testes. We also quantified TE silencing pathway gene expression in R. sibiricus and 14 other vertebrates with genome sizes ranging from 1 to 130 Gb and find no association between pathway expression and genome size. Taken together, our results reveal that the gigantic R. sibiricus genome includes at least 19 putatively active TE superfamilies, all of which are targeted by the piRNA pathway in proportion to their expression levels, suggesting comprehensive piRNA-mediated silencing. Testes have higher TE expression than ovaries, suggesting that they may contribute more to the species’ high genomic TE load. We posit that apparently conflicting interpretations of TE silencing and genomic gigantism in the literature, as well as the absence of a correlation between TE silencing pathway gene expression and genome size, can be reconciled by considering whether the TE community or the host is currently “on the attack” in the arms race dynamic. |
| first_indexed | 2024-04-10T07:27:01Z |
| format | Article |
| id | doaj.art-ec9614dfcdc64a3d9bf6437384251d4c |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-04-10T07:27:01Z |
| publishDate | 2023-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-ec9614dfcdc64a3d9bf6437384251d4c2023-02-24T06:46:17ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2023-02-011110.3389/fcell.2023.11243741124374Transposable element and host silencing activity in gigantic genomesJie Wang0Liang Yuan1Jiaxing Tang2Jiaxing Tang3Jiongyu Liu4Cheng Sun5Michael W. Itgen6Guiying Chen7Stanley K. Sessions8Guangpu Zhang9Guangpu Zhang10Rachel Lockridge Mueller11CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan, ChinaSchool of Life Sciences, Xinjiang Normal University, Urumqi, ChinaCAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan, ChinaCollege of Life Sciences, Sichuan Normal University, Chengdu, ChinaCAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan, ChinaCollege of Life Sciences, Capital Normal University, Beijing, ChinaDepartment of Biology, Colorado State University, Fort Collins, CO, United StatesCollege of Life Sciences, Sichuan Normal University, Chengdu, ChinaBiology Department, Hartwick College, Oneonta, NY, United StatesCAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization & Ecological Restoration and Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu, Sichuan, ChinaCollege of Life Sciences, Sichuan Normal University, Chengdu, ChinaDepartment of Biology, Colorado State University, Fort Collins, CO, United StatesTransposable elements (TEs) and the silencing machinery of their hosts are engaged in a germline arms-race dynamic that shapes TE accumulation and, therefore, genome size. In animal species with extremely large genomes (>10 Gb), TE accumulation has been pushed to the extreme, prompting the question of whether TE silencing also deviates from typical conditions. To address this question, we characterize TE silencing via two pathways—the piRNA pathway and KRAB-ZFP transcriptional repression—in the male and female gonads of Ranodon sibiricus, a salamander species with a ∼21 Gb genome. We quantify 1) genomic TE diversity, 2) TE expression, and 3) small RNA expression and find a significant relationship between the expression of piRNAs and TEs they target for silencing in both ovaries and testes. We also quantified TE silencing pathway gene expression in R. sibiricus and 14 other vertebrates with genome sizes ranging from 1 to 130 Gb and find no association between pathway expression and genome size. Taken together, our results reveal that the gigantic R. sibiricus genome includes at least 19 putatively active TE superfamilies, all of which are targeted by the piRNA pathway in proportion to their expression levels, suggesting comprehensive piRNA-mediated silencing. Testes have higher TE expression than ovaries, suggesting that they may contribute more to the species’ high genomic TE load. We posit that apparently conflicting interpretations of TE silencing and genomic gigantism in the literature, as well as the absence of a correlation between TE silencing pathway gene expression and genome size, can be reconciled by considering whether the TE community or the host is currently “on the attack” in the arms race dynamic.https://www.frontiersin.org/articles/10.3389/fcell.2023.1124374/fullTE expressionTE diversityTE silencingpiRNA pathwaygenome size evolutionsalamander |
| spellingShingle | Jie Wang Liang Yuan Jiaxing Tang Jiaxing Tang Jiongyu Liu Cheng Sun Michael W. Itgen Guiying Chen Stanley K. Sessions Guangpu Zhang Guangpu Zhang Rachel Lockridge Mueller Transposable element and host silencing activity in gigantic genomes Frontiers in Cell and Developmental Biology TE expression TE diversity TE silencing piRNA pathway genome size evolution salamander |
| title | Transposable element and host silencing activity in gigantic genomes |
| title_full | Transposable element and host silencing activity in gigantic genomes |
| title_fullStr | Transposable element and host silencing activity in gigantic genomes |
| title_full_unstemmed | Transposable element and host silencing activity in gigantic genomes |
| title_short | Transposable element and host silencing activity in gigantic genomes |
| title_sort | transposable element and host silencing activity in gigantic genomes |
| topic | TE expression TE diversity TE silencing piRNA pathway genome size evolution salamander |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2023.1124374/full |
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