The evolution of lncRNA repertoires and expression patterns in tetrapods.
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.
1] Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland [2] Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland [3] Laboratory of Developmental Genomics, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland (A.N.); Harvard Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, Massachusetts 02138, USA, and Broad Institute, Cambridge, Massachusetts 02142, USA (M.S.).
Anamaria
A
Necsulea
1] Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland [2] Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland [3] Laboratory of Developmental Genomics, Ecole Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland (A.N.); Harvard Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, Massachusetts 02138, USA, and Broad Institute, Cambridge, Massachusetts 02142, USA (M.S.).
Magali
M
Soumillon
1] Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland [2] Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland.
Maria
M
Warnefors
1] Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland [2] Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland.
Angélica
A
Liechti
The Robinson Institute, School of Molecular and Biomedical Science, University of Adelaide, Adelaide, South Australia 5005, Australia.
Tasman
T
Daish
Department of Systematic Zoology, Faculty of Agriculture and Horticulture, Humboldt University Berlin, 10099 Berlin, Germany.
Ulrich
U
Zeller
Department of Genetics, Stanford University School of Medicine, Stanford University, Stanford, California 94305, USA.
Julie C
JC
Baker
The Robinson Institute, School of Molecular and Biomedical Science, University of Adelaide, Adelaide, South Australia 5005, Australia.
Frank
F
Grützner
1] Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland [2] Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland.
Henrik
H
Kaessmann
D000818:Animals; D001001:Anura / Q000235:genetics; D002645:Chickens / Q000235:genetics; D017124:Conserved Sequence / Q000235:genetics; D019143:Evolution, Molecular; D018507:Gene Expression Regulation, Developmental / Q000235:genetics; D023281:Genomics; D006801:Humans; D051379:Mice; D035683:MicroRNAs / Q000235:genetics; D005810:Multigene Family; D011323:Primates / Q000235:genetics; D011506:Proteins / Q000235:genetics; D012322:RNA Precursors / Q000235:genetics; D062085:RNA, Long Noncoding / Q000235:genetics*; D059467:Transcriptome
C094335:H19 long non-coding RNA; D035683:MicroRNAs; D011506:Proteins; D012322:RNA Precursors; D062085:RNA, Long Noncoding