Dynamic and Widespread lncRNA Expression in a Sponge and the Origin of Animal Complexity

Gaiti, Federico, Fernandez-Valverde, Selene L., Nakanishi, Nagayasu, Calcino, Andrew D., Yanai, Itai, Tanurdzic, Milos and Degnan, Bernard M. (2015) Dynamic and Widespread lncRNA Expression in a Sponge and the Origin of Animal Complexity. Molecular Biology and Evolution, 32 9: 2367-2382. doi:10.1093/molbev/msv117


Author Gaiti, Federico
Fernandez-Valverde, Selene L.
Nakanishi, Nagayasu
Calcino, Andrew D.
Yanai, Itai
Tanurdzic, Milos
Degnan, Bernard M.
Title Dynamic and Widespread lncRNA Expression in a Sponge and the Origin of Animal Complexity
Journal name Molecular Biology and Evolution   Check publisher's open access policy
ISSN 0737-4038
1537-1719
Publication date 2015-09
Sub-type Article (original research)
DOI 10.1093/molbev/msv117
Open Access Status Not Open Access
Volume 32
Issue 9
Start page 2367
End page 2382
Total pages 16
Place of publication Cary, NC, United States
Publisher Oxford University Press
Collection year 2016
Language eng
Formatted abstract
Long noncoding RNAs (lncRNAs) are important developmental regulators in bilaterian animals. A correlation has been claimed between the lncRNA repertoire expansion and morphological complexity in vertebrate evolution. However, this claim has not been tested by examiningmorphologically simple animals. Here, we undertake a systematic investigation of lncRNAs in the demosponge Amphimedon queenslandica, a morphologically simple, early-branching metazoan. We combine RNA-Seq data across multiple developmental stages of Amphimedon with a filtering pipeline to conservatively predict 2,935 lncRNAs. These include intronic overlapping lncRNAs, exonic antisense overlapping lncRNAs, long inter-genic nonprotein coding RNAs, and precursors for small RNAs. Sponge lncRNAs are remarkably similar to their bilaterian counterparts in being relatively short with few exons and having low primary sequence conservation relative to protein-coding genes. As in bilaterians, a majority of sponge lncRNAs exhibit typical hallmarks of regulatory molecules, including high temporal specificity and dynamic developmental expression. Specific lncRNA expression profiles correlate tightly with conserved protein-coding genes likely involved in a range of developmental and physiological processes, such as the Wnt signaling pathway. Although the majority of Amphimedon lncRNAs appears to be taxonomically restricted with no identifiable orthologs, we find a few cases of conservation between demosponges in lncRNAs that are antisense to coding sequences. Based on the high similarity in the structure, organization, and dynamic expression of sponge lncRNAs to their bilaterian counterparts, we propose that these noncoding RNAs are an ancient feature of the metazoan genome. These results are consistent with lncRNAs regulating the development of animals, regardless of their level of morphological complexity.
Keyword Long noncoding RNAs
Evolution
Gene expression
Complexity
Basal metazoans
Long noncoding RNAs
Genome-wide identification
Open reading frames
Amphimedon-queenslandica
Human-cells
Evolutionary conservation
Transposable elements
Gene-expression
Reveals
Sequence
Q-Index Code C1
Q-Index Status Confirmed Code
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
Collections: Official 2016 Collection
School of Biological Sciences Publications
 
Versions
Version Filter Type
Citation counts: TR Web of Science Citation Count  Cited 8 times in Thomson Reuters Web of Science Article | Citations
Scopus Citation Count Cited 8 times in Scopus Article | Citations
Google Scholar Search Google Scholar
Created: Sun, 25 Oct 2015, 00:22:14 EST by System User on behalf of Scholarly Communication and Digitisation Service