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Core genes of biomineralization and cis-regulatory long non-coding RNA regulate shell growth in bivalves

2024-10Journal article Open access
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dc.contributor.authorPeng, Maoxiao
dc.contributor.authorCardoso, João
dc.contributor.authorPearson, Gareth Anthony
dc.contributor.authorCanario, Adelino
dc.contributor.authorPower, Deborah Mary
dc.date.accessioned2024-11-12T13:30:56Z
dc.date.available2024-11-12T13:30:56Z
dc.date.issued2024-10
dc.description.abstractBivalve molluscs are abundant in marine and freshwater systems and contribute essential ecosystem services. They are characterized by an exuberant diversity of biomineralized shells and typically have two symmetric valves (a.k.a shells), but oysters (Ostreidae), some clams (Anomiidae and Chamidae) and scallops (Pectinida) have two asymmetrical valves. Predicting and modelling the likely consequences of ocean acidification on bivalve survival, biodiversity and aquaculture makes understanding shell biomineralization and its regulation a priority. Objectives: This study aimed to a) exploit the atypical asymmetric shell growth of some bivalves and through comparative analysis of the genome and transcriptome pinpoint candidate biomineralization-related genes and regulatory long non-coding RNAs (LncRNAs) and b) demonstrate their roles in regulating shell biomineralization/growth. Methods: Meta-analysis of genomes, de novo generated mantle transcriptomes or transcriptomes and proteomes from public databases for six asymmetric to symmetric bivalve species was used to identify biomineralization-related genes. Bioinformatics filtering uncovered genes and regulatory modules characteristic of bivalves with asymmetric shells and identified candidate biomineralization-related genes and lncRNAs with a biased expression in asymmetric valves. A shell regrowth model in oyster and gene silencing experiments, were used to characterize candidate gene function. Results: Shell matrix genes with asymmetric expression in the mantle of the two valves were identified and unique cis-regulatory lncRNA modules characterized in Ostreidae. LncRNAs that regulate the expression of the tissue inhibitor of metalloproteinases gene family (TIMPDR) and of the shell matrix protein domain family (SMPDR) were identified. In vitro and in vivo silencing experiments revealed the candidate genes and lncRNA were associated with divergent shell growth rates and modified the microstructure of calcium carbonate (CaCO3) crystals. Conclusion: LncRNAs are putative regulatory factors of the bivalve biomineralization toolbox. In the Ostreidae family of bivalves biomineralization-related genes are cis-regulated by lncRNA and modify the planar growth rate and spatial orientation of crystals in the shell.eng
dc.description.sponsorship2022.08563.PTDC; EMBRC.PT ALG-01-0145-FEDER-022121 BIODATA.PT ALG-01-0145-FEDER-022231
dc.identifier.doi10.1016/j.jare.2023.11.024
dc.identifier.issn2090-1232
dc.identifier.urihttp://hdl.handle.net/10400.1/26253
dc.language.isoeng
dc.peerreviewedyes
dc.publisherElsevier
dc.relationAlgarve Centre for Marine Sciences
dc.relationAlgarve Centre for Marine Sciences
dc.relationCentre for Marine and Environmental Research
dc.relationEMBRC.PT ALG-01-0145-FEDER-022121 BIODATA.PT ALG-01-0145-FEDER-022231
dc.relation.ispartofJournal of Advanced Research
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/
dc.subjectBivalve
dc.subjectMantle transcriptomes
dc.subjectLncRNA cis-regulation
dc.subjectShell asymmetry
dc.subjectShell biomineralization toolbox
dc.titleCore genes of biomineralization and cis-regulatory long non-coding RNA regulate shell growth in bivalveseng
dc.typejournal article
dspace.entity.typePublication
oaire.awardTitleAlgarve Centre for Marine Sciences
oaire.awardTitleAlgarve Centre for Marine Sciences
oaire.awardTitleCentre for Marine and Environmental Research
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/6817 - DCRRNI ID/UIDB%2F04326%2F2020/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/6817 - DCRRNI ID/UIDP%2F04326%2F2020/PT
oaire.awardURIinfo:eu-repo/grantAgreement/FCT/6817 - DCRRNI ID/LA%2FP%2F0101%2F2020/PT
oaire.citation.endPage129
oaire.citation.startPage117
oaire.citation.titleJournal of Advanced Research
oaire.citation.volume64
oaire.fundingStream6817 - DCRRNI ID
oaire.fundingStream6817 - DCRRNI ID
oaire.fundingStream6817 - DCRRNI ID
oaire.versionhttp://purl.org/coar/version/c_970fb48d4fbd8a85
person.familyNamePeng
person.familyNameCardoso
person.familyNamePearson
person.familyNameCanario
person.familyNamePower
person.givenNameMaoxiao
person.givenNameJoão
person.givenNameGareth Anthony
person.givenNameAdelino
person.givenNameDeborah Mary
person.identifierR-000-75E
person.identifier113536
person.identifier143624
person.identifier.ciencia-id0A1D-96B9-27EB
person.identifier.ciencia-id5C1C-8247-D614
person.identifier.ciencia-id3315-9919-1A52
person.identifier.ciencia-id1F1E-D3B3-F804
person.identifier.ciencia-id891A-8A44-3CAE
person.identifier.orcid0000-0002-4855-1202
person.identifier.orcid0000-0002-7353-1799
person.identifier.orcid0000-0002-0768-464X
person.identifier.orcid0000-0002-6244-6468
person.identifier.orcid0000-0003-1366-0246
person.identifier.ridC-5552-2008
person.identifier.ridJ-3911-2013
person.identifier.ridC-7942-2009
person.identifier.scopus-author-id9639597300
person.identifier.scopus-author-id55916875600
person.identifier.scopus-author-id56568523700
person.identifier.scopus-author-id7101806760
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.identifierhttp://doi.org/10.13039/501100001871
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
project.funder.nameFundação para a Ciência e a Tecnologia
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