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The evolution of lncRNA repertoires and expression patterns in tetrapods
Open accessAbstract
Only a very small fraction of long noncoding RNAs (lncRNAs) are well characterized. The evolutionary history of lncRNAs can provide insights into their functionality, but the absence of lncRNA annotations in non-model organisms has precluded comparative analyses. Here we present a large-scale evolutionary study of lncRNA repertoires and expression patterns, in 11 tetrapod species. We identify approximately 11,000 primate-specific lncRNAs and 2,500 highly conserved lncRNAs, including approximately 400 genes that are likely to have originated more than 300 million years ago. We find that lncRNAs, in particular ancient ones, are in general actively regulated and may function predominantly in embryonic development. Most lncRNAs evolve rapidly in terms of sequence and expression levels, but tissue specificities are often conserved. We compared expression patterns of homologous lncRNA and protein-coding families across tetrapods to reconstruct an evolutionarily conserved co-expression network. This network suggests potential functions for lncRNAs in fundamental processes such as spermatogenesis and synaptic transmission, but also in more specific mechanisms such as placenta development through microRNA production.
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“As a group, these lncRNAs are enriched in the brain relative to other tissues (Extended Data Fig. 2l, m) and most that have been evaluated across species exhibit primate-specific expression patterns in the brain11, which we confirm for several transcripts (Supplementary Information, Extended Data Fig. 3a–h).”
From Genome-wide changes in lncRNA, splicing, and regional gene expression patterns in autism (2016) · cites this paper as [11]
In the citing paper
“Our analyses also reveal primate-specific lncRNAs that are probably relevant to understanding human higher cognition11,30.”
From Genome-wide changes in lncRNA, splicing, and regional gene expression patterns in autism (2016) · cites this paper as [11]
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“As a subset of lncRNAs are thought to function by repressing mRNA targets (72)”
From Transcriptome-wide isoform-level dysregulation in ASD, schizophrenia, and bipolar disorder (2018) · cites this paper as [72]
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Metadata
- Authors
- Necsulea, A., Soumillon, M., Warnefors, M., Liechti, A., Daish, T., Zeller, U., Baker, J. C., Grützner, F., & Kaessmann, H.
- Affiliations
- Broad Institute (US)
- SIB Swiss Institute of Bioinformatics (CH)
- The University of Adelaide (AU)
- Humboldt-Universität zu Berlin (DE)
- Stanford Medicine (US)
- Corresponding author
- Kaessmann, Henrik
- Venue
- Nature
- Published
- 2014-01-19
- Volume
- 505
- Issue
- 7485
- Pages
- 635-640
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2088069070
- Cited by
- 984
- References
- 58
- Citations by year
- 2026: 30 · 2025: 26 · 2024: 62 · 2023: 55 · 2022: 70 · 2021: 85 · 2020: 116 · 2019: 107 · 2018: 87 · 2017: 106 · 2016: 104 · 2015: 91 · 2014: 44
- FWCI
- 36.87
- Type
- journal article
- Language
- en
- Open access
- green
- cnrs.hal.science
- Licence
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- RePEc: Research Papers in Economics (submittedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- IRIS (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- Funders
- Wellcome Trust (099175/Z/12/Z)
- Medical Research Council (MC_PC_15004)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Chromosomal and Genetic Variations
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- long non-coding RNA, lncRNA evolution, tetrapods, embryonic development, tissue-specific gene expression, co-expression network, spermatogenesis, synaptic transmission, placental development, non-model organisms
- MeSH terms
- Animals, Anura, Chickens, Multigene Family, Humans, Primates, Proteins, RNA Precursors, Conserved Sequence, Gene Expression Regulation, Developmental, Evolution, Molecular, Genomics, MicroRNAs, Mice, Transcriptome, RNA, Long Noncoding
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