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Transcriptomic analysis of shell repair and biomineralization in the blue mussel, Mytilus edulis

BACKGROUND: Biomineralization by molluscs involves regulated deposition of calcium carbonate crystals within a protein framework to produce complex biocomposite structures. Effective biomineralization is a key trait for aquaculture, and animal resilience under future climate change. While many enzym...

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Autores principales: Yarra, Tejaswi, Ramesh, Kirti, Blaxter, Mark, Hüning, Anne, Melzner, Frank, Clark, Melody S.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
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Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8194122/
https://www.ncbi.nlm.nih.gov/pubmed/34112105
http://dx.doi.org/10.1186/s12864-021-07751-7
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author Yarra, Tejaswi
Ramesh, Kirti
Blaxter, Mark
Hüning, Anne
Melzner, Frank
Clark, Melody S.
author_facet Yarra, Tejaswi
Ramesh, Kirti
Blaxter, Mark
Hüning, Anne
Melzner, Frank
Clark, Melody S.
author_sort Yarra, Tejaswi
collection PubMed
description BACKGROUND: Biomineralization by molluscs involves regulated deposition of calcium carbonate crystals within a protein framework to produce complex biocomposite structures. Effective biomineralization is a key trait for aquaculture, and animal resilience under future climate change. While many enzymes and structural proteins have been identified from the shell and in mantle tissue, understanding biomieralization is impeded by a lack of fundamental knowledge of the genes and pathways involved. In adult bivalves, shells are secreted by the mantle tissue during growth, maintenance and repair, with the repair process, in particular, amenable to experimental dissection at the transcriptomic level in individual animals. RESULTS: Gene expression dynamics were explored in the adult blue mussel, Mytilus edulis, during experimentally induced shell repair, using the two valves of each animal as a matched treatment-control pair. Gene expression was assessed using high-resolution RNA-Seq against a de novo assembled database of functionally annotated transcripts. A large number of differentially expressed transcripts were identified in the repair process. Analysis focused on genes encoding proteins and domains identified in shell biology, using a new database of proteins and domains previously implicated in biomineralization in mussels and other molluscs. The genes implicated in repair included many otherwise novel transcripts that encoded proteins with domains found in other shell matrix proteins, as well as genes previously associated with primary shell formation in larvae. Genes with roles in intracellular signalling and maintenance of membrane resting potential were among the loci implicated in the repair process. While haemocytes have been proposed to be actively involved in repair, no evidence was found for this in the M. edulis data. CONCLUSIONS: The shell repair experimental model and a newly developed shell protein domain database efficiently identified transcripts involved in M. edulis shell production. In particular, the matched pair analysis allowed factoring out of much of the inherent high level of variability between individual mussels. This snapshot of the damage repair process identified a large number of genes putatively involved in biomineralization from initial signalling, through calcium mobilization to shell construction, providing many novel transcripts for future in-depth functional analyses.
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spelling pubmed-81941222021-06-15 Transcriptomic analysis of shell repair and biomineralization in the blue mussel, Mytilus edulis Yarra, Tejaswi Ramesh, Kirti Blaxter, Mark Hüning, Anne Melzner, Frank Clark, Melody S. BMC Genomics Research Article BACKGROUND: Biomineralization by molluscs involves regulated deposition of calcium carbonate crystals within a protein framework to produce complex biocomposite structures. Effective biomineralization is a key trait for aquaculture, and animal resilience under future climate change. While many enzymes and structural proteins have been identified from the shell and in mantle tissue, understanding biomieralization is impeded by a lack of fundamental knowledge of the genes and pathways involved. In adult bivalves, shells are secreted by the mantle tissue during growth, maintenance and repair, with the repair process, in particular, amenable to experimental dissection at the transcriptomic level in individual animals. RESULTS: Gene expression dynamics were explored in the adult blue mussel, Mytilus edulis, during experimentally induced shell repair, using the two valves of each animal as a matched treatment-control pair. Gene expression was assessed using high-resolution RNA-Seq against a de novo assembled database of functionally annotated transcripts. A large number of differentially expressed transcripts were identified in the repair process. Analysis focused on genes encoding proteins and domains identified in shell biology, using a new database of proteins and domains previously implicated in biomineralization in mussels and other molluscs. The genes implicated in repair included many otherwise novel transcripts that encoded proteins with domains found in other shell matrix proteins, as well as genes previously associated with primary shell formation in larvae. Genes with roles in intracellular signalling and maintenance of membrane resting potential were among the loci implicated in the repair process. While haemocytes have been proposed to be actively involved in repair, no evidence was found for this in the M. edulis data. CONCLUSIONS: The shell repair experimental model and a newly developed shell protein domain database efficiently identified transcripts involved in M. edulis shell production. In particular, the matched pair analysis allowed factoring out of much of the inherent high level of variability between individual mussels. This snapshot of the damage repair process identified a large number of genes putatively involved in biomineralization from initial signalling, through calcium mobilization to shell construction, providing many novel transcripts for future in-depth functional analyses. BioMed Central 2021-06-10 /pmc/articles/PMC8194122/ /pubmed/34112105 http://dx.doi.org/10.1186/s12864-021-07751-7 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Yarra, Tejaswi
Ramesh, Kirti
Blaxter, Mark
Hüning, Anne
Melzner, Frank
Clark, Melody S.
Transcriptomic analysis of shell repair and biomineralization in the blue mussel, Mytilus edulis
title Transcriptomic analysis of shell repair and biomineralization in the blue mussel, Mytilus edulis
title_full Transcriptomic analysis of shell repair and biomineralization in the blue mussel, Mytilus edulis
title_fullStr Transcriptomic analysis of shell repair and biomineralization in the blue mussel, Mytilus edulis
title_full_unstemmed Transcriptomic analysis of shell repair and biomineralization in the blue mussel, Mytilus edulis
title_short Transcriptomic analysis of shell repair and biomineralization in the blue mussel, Mytilus edulis
title_sort transcriptomic analysis of shell repair and biomineralization in the blue mussel, mytilus edulis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8194122/
https://www.ncbi.nlm.nih.gov/pubmed/34112105
http://dx.doi.org/10.1186/s12864-021-07751-7
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