Gene family expansion and functional diversification of chitinase and chitin synthase genes in Atlantic salmon (Salmo salar)

Chitin is one of the most abundant polysaccharides in nature, forming important structures in insects, crustaceans, and fungal cell walls. Vertebrates on the other hand are generally considered “nonchitinous” organisms, despite having highly conserved chitin metabolism-associated genes. Recent work...

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Published in:G3 Genes|Genomes|Genetics
Main Authors: Holen, Matilde Mengkrog, Vaaje-Kolstad, Gustav, Kent, Matthew Peter, Sandve, Simen Rød
Format: Text
Language:English
Published: Oxford University Press 2023
Subjects:
Online Access:http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10234404/
http://www.ncbi.nlm.nih.gov/pubmed/36972305
https://doi.org/10.1093/g3journal/jkad069
id ftpubmed:oai:pubmedcentral.nih.gov:10234404
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spelling ftpubmed:oai:pubmedcentral.nih.gov:10234404 2023-06-18T03:39:52+02:00 Gene family expansion and functional diversification of chitinase and chitin synthase genes in Atlantic salmon (Salmo salar) Holen, Matilde Mengkrog Vaaje-Kolstad, Gustav Kent, Matthew Peter Sandve, Simen Rød 2023-03-27 http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10234404/ http://www.ncbi.nlm.nih.gov/pubmed/36972305 https://doi.org/10.1093/g3journal/jkad069 en eng Oxford University Press http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10234404/ http://www.ncbi.nlm.nih.gov/pubmed/36972305 http://dx.doi.org/10.1093/g3journal/jkad069 © The Author(s) 2023. Published by Oxford University Press on behalf of The Genetics Society of America. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. G3 (Bethesda) Investigation Text 2023 ftpubmed https://doi.org/10.1093/g3journal/jkad069 2023-06-04T01:37:24Z Chitin is one of the most abundant polysaccharides in nature, forming important structures in insects, crustaceans, and fungal cell walls. Vertebrates on the other hand are generally considered “nonchitinous” organisms, despite having highly conserved chitin metabolism-associated genes. Recent work has revealed that the largest group of vertebrates, the teleosts, have the potential to both synthesize and degrade endogenous chitin. Yet, little is known about the genes and proteins responsible for these dynamic processes. Here, we used comparative genomics, transcriptomics, and chromatin accessibility data to characterize the repertoire, evolution, and regulation of genes involved in chitin metabolism in teleosts, with a particular focus on Atlantic salmon. Reconstruction of gene family phylogenies provides evidence for an expansion of teleost and salmonid chitinase and chitin synthase genes after multiple whole-genome duplications. Analyses of multi-tissue gene expression data demonstrated a strong bias of gastrointestinal tract expression for chitin metabolism genes, but with different spatial and temporal tissue specificities. Finally, we integrated transcriptomes from a developmental time series of the gastrointestinal tract with chromatin accessibility data to identify putative transcription factors responsible for regulating chitin metabolism gene expression (CDX1 and CDX2) as well as tissue-specific divergence in the regulation of gene duplicates (FOXJ2). The findings presented here support the hypothesis that chitin metabolism genes in teleosts play a role in developing and maintaining a chitin-based barrier in the teleost gut and provide a basis for further investigations into the molecular basis of this barrier. Text Atlantic salmon Salmo salar PubMed Central (PMC) G3 Genes|Genomes|Genetics
institution Open Polar
collection PubMed Central (PMC)
op_collection_id ftpubmed
language English
topic Investigation
spellingShingle Investigation
Holen, Matilde Mengkrog
Vaaje-Kolstad, Gustav
Kent, Matthew Peter
Sandve, Simen Rød
Gene family expansion and functional diversification of chitinase and chitin synthase genes in Atlantic salmon (Salmo salar)
topic_facet Investigation
description Chitin is one of the most abundant polysaccharides in nature, forming important structures in insects, crustaceans, and fungal cell walls. Vertebrates on the other hand are generally considered “nonchitinous” organisms, despite having highly conserved chitin metabolism-associated genes. Recent work has revealed that the largest group of vertebrates, the teleosts, have the potential to both synthesize and degrade endogenous chitin. Yet, little is known about the genes and proteins responsible for these dynamic processes. Here, we used comparative genomics, transcriptomics, and chromatin accessibility data to characterize the repertoire, evolution, and regulation of genes involved in chitin metabolism in teleosts, with a particular focus on Atlantic salmon. Reconstruction of gene family phylogenies provides evidence for an expansion of teleost and salmonid chitinase and chitin synthase genes after multiple whole-genome duplications. Analyses of multi-tissue gene expression data demonstrated a strong bias of gastrointestinal tract expression for chitin metabolism genes, but with different spatial and temporal tissue specificities. Finally, we integrated transcriptomes from a developmental time series of the gastrointestinal tract with chromatin accessibility data to identify putative transcription factors responsible for regulating chitin metabolism gene expression (CDX1 and CDX2) as well as tissue-specific divergence in the regulation of gene duplicates (FOXJ2). The findings presented here support the hypothesis that chitin metabolism genes in teleosts play a role in developing and maintaining a chitin-based barrier in the teleost gut and provide a basis for further investigations into the molecular basis of this barrier.
format Text
author Holen, Matilde Mengkrog
Vaaje-Kolstad, Gustav
Kent, Matthew Peter
Sandve, Simen Rød
author_facet Holen, Matilde Mengkrog
Vaaje-Kolstad, Gustav
Kent, Matthew Peter
Sandve, Simen Rød
author_sort Holen, Matilde Mengkrog
title Gene family expansion and functional diversification of chitinase and chitin synthase genes in Atlantic salmon (Salmo salar)
title_short Gene family expansion and functional diversification of chitinase and chitin synthase genes in Atlantic salmon (Salmo salar)
title_full Gene family expansion and functional diversification of chitinase and chitin synthase genes in Atlantic salmon (Salmo salar)
title_fullStr Gene family expansion and functional diversification of chitinase and chitin synthase genes in Atlantic salmon (Salmo salar)
title_full_unstemmed Gene family expansion and functional diversification of chitinase and chitin synthase genes in Atlantic salmon (Salmo salar)
title_sort gene family expansion and functional diversification of chitinase and chitin synthase genes in atlantic salmon (salmo salar)
publisher Oxford University Press
publishDate 2023
url http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10234404/
http://www.ncbi.nlm.nih.gov/pubmed/36972305
https://doi.org/10.1093/g3journal/jkad069
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source G3 (Bethesda)
op_relation http://www.ncbi.nlm.nih.gov/pmc/articles/PMC10234404/
http://www.ncbi.nlm.nih.gov/pubmed/36972305
http://dx.doi.org/10.1093/g3journal/jkad069
op_rights © The Author(s) 2023. Published by Oxford University Press on behalf of The Genetics Society of America.
https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
op_doi https://doi.org/10.1093/g3journal/jkad069
container_title G3 Genes|Genomes|Genetics
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