Cited by 713Chromosomal and Genetic VariationsCancer-related molecular mechanisms researchGenomics and Chromatin Dynamics

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Transposable Elements Are Major Contributors to the Origin, Diversification, and Regulation of Vertebrate Long Noncoding RNAs

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Kapusta, Aurélie, Kronenberg, Zev, Lynch, Vincent J., Zhuo, Xiaoyu, Ramsay, LeeAnn, Bourque, Guillaume, Yandell, Mark, Feschotte, Cédric·2013·PLoS Genetics

DOI 10.1371/journal.pgen.1003470PMC PMC3636048

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Abstract

Advances in vertebrate genomics have uncovered thousands of loci encoding long noncoding RNAs (lncRNAs). While progress has been made in elucidating the regulatory functions of lncRNAs, little is known about their origins and evolution. Here we explore the contribution of transposable elements (TEs) to the makeup and regulation of lncRNAs in human, mouse, and zebrafish. Surprisingly, TEs occur in more than two thirds of mature lncRNA transcripts and account for a substantial portion of total lncRNA sequence (~30% in human), whereas they seldom occur in protein-coding transcripts. While TEs contribute less to lncRNA exons than expected, several TE families are strongly enriched in lncRNAs. There is also substantial interspecific variation in the coverage and types of TEs embedded in lncRNAs, partially reflecting differences in the TE landscapes of the genomes surveyed. In human, TE sequences in lncRNAs evolve under greater evolutionary constraint than their non-TE sequences, than their intronic TEs, or than random DNA. Consistent with functional constraint, we found that TEs contribute signals essential for the biogenesis of many lncRNAs, including ~30,000 unique sites for transcription initiation, splicing, or polyadenylation in human. In addition, we identified ~35,000 TEs marked as open chromatin located within 10 kb upstream of lncRNA genes. The density of these marks in one cell type correlate with elevated expression of the downstream lncRNA in the same cell type, suggesting that these TEs contribute to cis-regulation. These global trends are recapitulated in several lncRNAs with established functions. Finally a subset of TEs embedded in lncRNAs are subject to RNA editing and predicted to form secondary structures likely important for function. In conclusion, TEs are nearly ubiquitous in lncRNAs and have played an important role in the lineage-specific diversification of vertebrate lncRNA repertoires.

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Additional file 6 of Tissue-specific usage of transposable element-derived promoters in mouse development
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Additional file 7 of Tissue-specific usage of transposable element-derived promoters in mouse development
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Additional file 2 of Tissue-specific usage of transposable element-derived promoters in mouse development
Miao, B., Fu, S., Lyu, C., Gontarz, P. M., Wang, T., & Zhang, B. (2020) · Figshare · doi:10.6084/m9.figshare.13018134
Additional file 3 of Tissue-specific usage of transposable element-derived promoters in mouse development
Miao, B., Fu, S., Lyu, C., Gontarz, P. M., Wang, T., & Zhang, B. (2020) · Figshare · doi:10.6084/m9.figshare.13018137
Additional file 8 of Tissue-specific usage of transposable element-derived promoters in mouse development
Miao, B., Fu, S., Lyu, C., Gontarz, P. M., Wang, T., & Zhang, B. (2020) · Figshare · doi:10.6084/m9.figshare.13018152
Additional file 4 of Tissue-specific usage of transposable element-derived promoters in mouse development
Miao, B., Fu, S., Lyu, C., Gontarz, P. M., Wang, T., & Zhang, B. (2020) · Figshare · doi:10.6084/m9.figshare.13018140
Additional file 11 of Tissue-specific usage of transposable element-derived promoters in mouse development
Miao, B., Fu, S., Lyu, C., Gontarz, P. M., Wang, T., & Zhang, B. (2020) · Figshare · doi:10.6084/m9.figshare.13018125
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Additional file 1 of Characterization of an eutherian gene cluster generated after transposon domestication identifies Bex3 as relevant for advanced neurological functions
Navas-Pérez, E., Vicente-García, C., Mirra, S., Burguera, D., Fernàndez‐Castillo, N., Ferrán, J. L., López-Mayorga, M., Alaiz-Noya, M., Suárez‐Pereira, I., Antón-Galindo, E., et al. (2020) · Figshare · doi:10.6084/m9.figshare.13142468
Additional file 13 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704137
Additional file 6 of Long noncoding RNAs emerge from transposon-derived antisense sequences and may contribute to infection stage-specific transposon regulation in a fungal phytopathogen
Qian, J., Ibrahim, H. M. M., Erz, M., Kümmel, F., Panstruga, R., & Kusch, S. (2024) · Figshare · doi:10.6084/m9.figshare.26640178
Additional file 16 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704146
Additional file 7 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704119
Additional file 2 of De novo emergence, existence, and demise of a protein-coding gene in murids
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Additional file 5 of Tissue-specific usage of transposable element-derived promoters in mouse development
Miao, B., Fu, S., Lyu, C., Gontarz, P. M., Wang, T., & Zhang, B. (2020) · Figshare · doi:10.6084/m9.figshare.13018143
Additional file 1 of De novo emergence, existence, and demise of a protein-coding gene in murids
Petržílek, J., Pasulka, J., Malı́k, R., Horvat, F., Kataruka, S., Fulka, H., & Svoboda, P. (2023) · Figshare · doi:10.6084/m9.figshare.22613096
Additional file 5 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704113
Additional file 4 of Long noncoding RNAs emerge from transposon-derived antisense sequences and may contribute to infection stage-specific transposon regulation in a fungal phytopathogen
Qian, J., Ibrahim, H. M. M., Erz, M., Kümmel, F., Panstruga, R., & Kusch, S. (2024) · Figshare · doi:10.6084/m9.figshare.26640172
Additional file 3 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704107
Additional file 9 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704125
Additional file 8 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704122
Additional file 8 of Long noncoding RNAs emerge from transposon-derived antisense sequences and may contribute to infection stage-specific transposon regulation in a fungal phytopathogen
Qian, J., Ibrahim, H. M. M., Erz, M., Kümmel, F., Panstruga, R., & Kusch, S. (2024) · Figshare · doi:10.6084/m9.figshare.26640184
Additional file 1 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.25572518
Additional file 7 of Long noncoding RNAs emerge from transposon-derived antisense sequences and may contribute to infection stage-specific transposon regulation in a fungal phytopathogen
Qian, J., Ibrahim, H. M. M., Erz, M., Kümmel, F., Panstruga, R., & Kusch, S. (2024) · Figshare · doi:10.6084/m9.figshare.26640181
Additional file 4 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704110
Additional file 1 of Revealing the novel complexity of plant long non-coding RNA by strand-specific and whole transcriptome sequencing for evolutionarily representative plant species
Zhu, Y., Chen, L., Hong, X., Shi, H., & Li, X. (2022) · Figshare · doi:10.6084/m9.figshare.19799861
Additional file 3 of Long noncoding RNAs emerge from transposon-derived antisense sequences and may contribute to infection stage-specific transposon regulation in a fungal phytopathogen
Qian, J., Ibrahim, H. M. M., Erz, M., Kümmel, F., Panstruga, R., & Kusch, S. (2024) · Figshare · doi:10.6084/m9.figshare.26640169
Additional file 12 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704134
Additional file 21 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704161
Additional file 15 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704143
Additional file 17 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704149
Additional file 10 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704128
Additional file 1 of Long noncoding RNAs emerge from transposon-derived antisense sequences and may contribute to infection stage-specific transposon regulation in a fungal phytopathogen
Qian, J., Ibrahim, H. M. M., Erz, M., Kümmel, F., Panstruga, R., & Kusch, S. (2023) · Figshare · doi:10.6084/m9.figshare.24564179
Additional file 20 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704158
Additional file 2 of Characterization of an eutherian gene cluster generated after transposon domestication identifies Bex3 as relevant for advanced neurological functions
Navas-Pérez, E., Vicente-García, C., Mirra, S., Burguera, D., Fernàndez‐Castillo, N., Ferrán, J. L., López-Mayorga, M., Alaiz-Noya, M., Suárez‐Pereira, I., Antón-Galindo, E., et al. (2020) · Figshare · doi:10.6084/m9.figshare.13142471
Additional file 12 of Tissue-specific usage of transposable element-derived promoters in mouse development
Miao, B., Fu, S., Lyu, C., Gontarz, P. M., Wang, T., & Zhang, B. (2020) · Figshare · doi:10.6084/m9.figshare.13018128
Additional file 2 of Long noncoding RNAs emerge from transposon-derived antisense sequences and may contribute to infection stage-specific transposon regulation in a fungal phytopathogen
Qian, J., Ibrahim, H. M. M., Erz, M., Kümmel, F., Panstruga, R., & Kusch, S. (2024) · Figshare · doi:10.6084/m9.figshare.24564282
Additional file 2 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.25572650
Additional file 6 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704116
Additional file 5 of Long noncoding RNAs emerge from transposon-derived antisense sequences and may contribute to infection stage-specific transposon regulation in a fungal phytopathogen
Qian, J., Ibrahim, H. M. M., Erz, M., Kümmel, F., Panstruga, R., & Kusch, S. (2024) · Figshare · doi:10.6084/m9.figshare.26640175
Additional file 14 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704140
Additional file 18 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704152
Additional file 19 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704155
Additional file 1 of Identification of LINE retrotransposons and long non-coding RNAs expressed in the octopus brain
Petrosino, G., Ponte, G., Volpe, M., Zarrella, I., Ansaloni, F., Langella, C., Cristina, G. D., Finaurini, S., Russo, M. T., Basu, S., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19785781
Additional file 4 of Revealing the novel complexity of plant long non-coding RNA by strand-specific and whole transcriptome sequencing for evolutionarily representative plant species
Zhu, Y., Chen, L., Hong, X., Shi, H., & Li, X. (2022) · Figshare · doi:10.6084/m9.figshare.19799870
Additional file 1 of Evolution of mouse circadian enhancers from transposable elements
Judd, J., Sanderson, H., & Feschotte, C. (2021) · Figshare · doi:10.6084/m9.figshare.14881014
Self-citation
Additional file 11 of Constructing eRNA-mediated gene regulatory networks to explore the genetic basis of muscle and fat-relevant traits in pigs
Wang, C., Chen, C., Lei, B., Qin, S., Zhang, Y., Li, K., Zhang, S., & Liu, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26704131
Additional file 2 of Evolution of mouse circadian enhancers from transposable elements
Judd, J., Sanderson, H., & Feschotte, C. (2021) · Figshare · doi:10.6084/m9.figshare.14881017
Self-citation
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Authors: Kapusta, A., Kronenberg, Z., Lynch, V. J., Zhuo, X., Ramsay, L., Bourque, G., Yandell, M., & Feschotte, C.
Affiliations: University of Utah (US)
University of Chicago (US)
McGill University and Génome Québec Innovation Centre (CA)
Corresponding author: Feschotte, Cédric
ORCID: Kapusta, Aurélie
Kronenberg, Zev
Lynch, Vincent J.
Zhuo, Xiaoyu
Bourque, Guillaume
Yandell, Mark
Feschotte, Cédric
Venue: PLoS Genetics
Publisher: Public Library of Science (PLoS)
Published: 2013-04-25
Volume: 9
Issue: 4
Pages: e1003470
ISSN: 1553-7390 (ISSN-L)
1553-7404
DOI: 10.1371/journal.pgen.1003470
PMC: PMC3636048
OpenAlex: W2029868997
Cited by: 687
References: 115
Citations by year: 2026: 21 · 2025: 27 · 2024: 60 · 2023: 52 · 2022: 57 · 2021: 70 · 2020: 53 · 2019: 52 · 2018: 68 · 2017: 58 · 2016: 50 · 2015: 62 · 2014: 42 · 2013: 13
FWCI: 67.23
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS Genetics (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Knowledge@UChicago (University of Chicago) (submittedVersion, cc-by-nc-nd)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
University of Chicago (cc-by)
Funders: National Science Foundation (1126998)
National Institutes of Health
Canadian Institutes of Health Research (115090_1)
National Human Genome Research Institute (R01HG004694)
National Institute of General Medical Sciences (T32GM007464, R01GM077582)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords: transposable elements, long non-coding RNA, lncRNA evolution, lncRNA biogenesis, cis-regulation, open chromatin, RNA editing, secondary structure, transcription initiation, splicing, polyadenylation, human, mice, zebrafish
MeSH terms: Animals, DNA Transposable Elements, Exons, Humans, Introns, Vertebrates, RNA, Long Noncoding

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Transposable Elements Are Major Contributors to the Origin, Diversification, and Regulation of Vertebrate Long Noncoding RNAs

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