Identification of microRNAs in the coral Stylophora pistillata.

Handle URI:
http://hdl.handle.net/10754/323560
Title:
Identification of microRNAs in the coral Stylophora pistillata.
Authors:
Liew, Yi Jin ( 0000-0003-2553-8870 ) ; Aranda, Manuel ( 0000-0001-6673-016X ) ; Carr, Adrian; Baumgarten, Sebastian ( 0000-0003-2646-7699 ) ; Zoccola, Didier; Tambutté, Sylvie; Allemand, Denis; Micklem, Gos; Voolstra, Christian R. ( 0000-0003-4555-3795 )
Abstract:
Coral reefs are major contributors to marine biodiversity. However, they are in rapid decline due to global environmental changes such as rising sea surface temperatures, ocean acidification, and pollution. Genomic and transcriptomic analyses have broadened our understanding of coral biology, but a study of the microRNA (miRNA) repertoire of corals is missing. miRNAs constitute a class of small non-coding RNAs of ∼22 nt in size that play crucial roles in development, metabolism, and stress response in plants and animals alike. In this study, we examined the coral Stylophora pistillata for the presence of miRNAs and the corresponding core protein machinery required for their processing and function. Based on small RNA sequencing, we present evidence for 31 bona fide microRNAs, 5 of which (miR-100, miR-2022, miR-2023, miR-2030, and miR-2036) are conserved in other metazoans. Homologues of Argonaute, Piwi, Dicer, Drosha, Pasha, and HEN1 were identified in the transcriptome of S. pistillata based on strong sequence conservation with known RNAi proteins, with additional support derived from phylogenetic trees. Examination of putative miRNA gene targets indicates potential roles in development, metabolism, immunity, and biomineralisation for several of the microRNAs. Here, we present first evidence of a functional RNAi machinery and five conserved miRNAs in S. pistillata, implying that miRNAs play a role in organismal biology of scleractinian corals. Analysis of predicted miRNA target genes in S. pistillata suggests potential roles of miRNAs in symbiosis and coral calcification. Given the importance of miRNAs in regulating gene expression in other metazoans, further expression analyses of small non-coding RNAs in transcriptional studies of corals should be informative about miRNA-affected processes and pathways.
KAUST Department:
Red Sea Research Center (RSRC)
Citation:
Liew YJ, Aranda M, Carr A, Baumgarten S, Zoccola D, et al. (2014) Identification of MicroRNAs in the Coral Stylophora pistillata. PLoS ONE 9: e91101. doi:10.1371/journal.pone.0091101.
Publisher:
Public Library of Science (PLoS)
Journal:
PLoS ONE
Issue Date:
21-Mar-2014
DOI:
10.1371/journal.pone.0091101
PubMed ID:
24658574
PubMed Central ID:
PMC3962355
Type:
Article
ISSN:
1932-6203
Sponsors:
This project was partially funded by bursaries from Cambridge Commonwealth Trust and Trinity Hall to YJL, and an Academic Excellence Alliance (AEA) Award (Award Number 1000000533) to CRV and GM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Additional Links:
http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0091101; http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3962355/
Appears in Collections:
Articles; Red Sea Research Center (RSRC)

Full metadata record

DC FieldValue Language
dc.contributor.authorLiew, Yi Jinen
dc.contributor.authorAranda, Manuelen
dc.contributor.authorCarr, Adrianen
dc.contributor.authorBaumgarten, Sebastianen
dc.contributor.authorZoccola, Didieren
dc.contributor.authorTambutté, Sylvieen
dc.contributor.authorAllemand, Denisen
dc.contributor.authorMicklem, Gosen
dc.contributor.authorVoolstra, Christian R.en
dc.date.accessioned2014-07-22T07:56:50Z-
dc.date.available2014-07-22T07:56:50Z-
dc.date.issued2014-03-21en
dc.identifier.citationLiew YJ, Aranda M, Carr A, Baumgarten S, Zoccola D, et al. (2014) Identification of MicroRNAs in the Coral Stylophora pistillata. PLoS ONE 9: e91101. doi:10.1371/journal.pone.0091101.en
dc.identifier.issn1932-6203en
dc.identifier.pmid24658574en
dc.identifier.doi10.1371/journal.pone.0091101en
dc.identifier.urihttp://hdl.handle.net/10754/323560en
dc.description.abstractCoral reefs are major contributors to marine biodiversity. However, they are in rapid decline due to global environmental changes such as rising sea surface temperatures, ocean acidification, and pollution. Genomic and transcriptomic analyses have broadened our understanding of coral biology, but a study of the microRNA (miRNA) repertoire of corals is missing. miRNAs constitute a class of small non-coding RNAs of ∼22 nt in size that play crucial roles in development, metabolism, and stress response in plants and animals alike. In this study, we examined the coral Stylophora pistillata for the presence of miRNAs and the corresponding core protein machinery required for their processing and function. Based on small RNA sequencing, we present evidence for 31 bona fide microRNAs, 5 of which (miR-100, miR-2022, miR-2023, miR-2030, and miR-2036) are conserved in other metazoans. Homologues of Argonaute, Piwi, Dicer, Drosha, Pasha, and HEN1 were identified in the transcriptome of S. pistillata based on strong sequence conservation with known RNAi proteins, with additional support derived from phylogenetic trees. Examination of putative miRNA gene targets indicates potential roles in development, metabolism, immunity, and biomineralisation for several of the microRNAs. Here, we present first evidence of a functional RNAi machinery and five conserved miRNAs in S. pistillata, implying that miRNAs play a role in organismal biology of scleractinian corals. Analysis of predicted miRNA target genes in S. pistillata suggests potential roles of miRNAs in symbiosis and coral calcification. Given the importance of miRNAs in regulating gene expression in other metazoans, further expression analyses of small non-coding RNAs in transcriptional studies of corals should be informative about miRNA-affected processes and pathways.en
dc.description.sponsorshipThis project was partially funded by bursaries from Cambridge Commonwealth Trust and Trinity Hall to YJL, and an Academic Excellence Alliance (AEA) Award (Award Number 1000000533) to CRV and GM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.en
dc.language.isoenen
dc.publisherPublic Library of Science (PLoS)en
dc.relation.urlhttp://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0091101en
dc.relation.urlhttp://www.ncbi.nlm.nih.gov/pmc/articles/PMC3962355/en
dc.rightsArchived with thanks to PloS oneen
dc.titleIdentification of microRNAs in the coral Stylophora pistillata.en
dc.typeArticleen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalPLoS ONEen
dc.identifier.pmcidPMC3962355en
dc.eprint.versionPublisher's Version/PDFen
dc.contributor.institutionCambridge Systems Biology Centre & Department of Genetics, University of Cambridge, Cambridge, United Kingdom.en
dc.contributor.institutionCentre Scientifique de Monaco, Monaco, Monaco.en
dc.contributor.affiliationKing Abdullah University of Science and Technology (KAUST)en
kaust.authorLiew, Yi Jinen
kaust.authorAranda, Manuelen
kaust.authorBaumgarten, Sebastianen
kaust.authorVoolstra, Christian R.en

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  • Files 13

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      Supporting Information S1 - Stylophora pistillata transcriptome (43,493 genes/loci ≥250 bp, DDBJ/EMBL/GenBank accession GARY00000000). doi:10.1371/journal.pone.0091101.s001
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      Supporting Information S2 - Stylophora pistillata transcriptome BLASTX and GO annotation (43,493 genes/loci ≥250 bp). doi:10.1371/journal.pone.0091101.s002
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      Supporting Information S3 - Candidate RNAi proteins in Stylophora pistillata. doi:10.1371/journal.pone.0091101.s003
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      Supporting Information S4 - Alignment of sequences used to construct maximum-likelihood phylogenetic trees (FASTA format). doi:10.1371/journal.pone.0091101.s004
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      Supporting Information S5 - Graphical alignment of the PAZ domains in Argonaute and Piwi proteins. Of note are the strong conservation of glutamate (E) at position 137 (mutants produce insoluble protein) and phenylalanine (F) at position 72 (required for RNA binding). However, the phenylalanine at position 48 in D. melanogaster AGO2 (also required for RNA binding) was not conserved at all. Key residue positions are marked with red asterisks. doi:10.1371/journal.pone.0091101.s005
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      Supporting Information S6 - Graphical alignment of the Piwi domains in Argonaute and Piwi proteins. The catalytic DDX triad, which contributes to the slicing activity of the ribonuclease (marked in red asterisks), is located at positions 46, 140 and 284 or positions 46, 140 and 155. This triad is present in one S. pistillata candidate, but not in two others, most likely due to the transcript sequences being incomplete. doi:10.1371/journal.pone.0091101.s006
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      Supporting Information S7 - Graphical alignment of the first RNase III domain in Dicer and Drosha proteins. Remarkably, all of the key acidic aspartate (D) and glutamate (E) residues, which are involved in the coordination of a divalent metal cation, are conserved across the candidate homologues and known sequences. doi:10.1371/journal.pone.0091101.s007
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      Supporting Information S8 - Graphical alignment of the second RNase III domain in Dicer and Drosha proteins. Similarly, most of the aspartate (D) and glutamate (E) residues involved in the coordination of a divalent metal cation are conserved - perfectly conserved for the Drosha candidate (“Locus_18820”), while the Dicer candidate (“Locus_10081”) only has the first two key residues. Both sequences however align well to known Dicer and Drosha proteins. doi:10.1371/journal.pone.0091101.s008
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      Supporting Information S9 - Graphical alignment of the dsRNA-binding domain in Pasha. The key alanine/alanine pair (AA, positions 21 and 22) and alanine/serine pair (AS, positions 139 and 140) involved in the binding of dsRNA are also present in the S. pistillata candidate Pasha. As Pasha is an essential cofactor of Drosha, it lends support to the positive discovery of Drosha in S. pistillata. doi:10.1371/journal.pone.0091101.s009
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      Supporting Information S10 - Graphical alignment of the methyltransferase domain in HEN1. The residues involved in Mg2+ coordination (positions 118, 121, 122 and 123) are well-conserved across the aligned sequences; residues associated with the cofactor AdoHcy and 3′ terminus (other positions marked by a red asterisk) are also well conserved. doi:10.1371/journal.pone.0091101.s010
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      Supporting Information S11 - List of additional criteria used to select bona fide miRNAs in S. pistillata from miRDeep2 results. doi:10.1371/journal.pone.0091101.s011
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      Supporting Information S12 - Enriched GO terms (P<0.01) associated with the set of 31 bona fide miRNAs identified in Stylophora pistillata. doi:10.1371/journal.pone.0091101.s012
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