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

Abstract 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. Rec...

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Published in:G3 Genes|Genomes|Genetics
Main Authors: Holen, Matilde Mengkrog, Vaaje-Kolstad, Gustav, Kent, Matthew Peter, Sandve, Simen Rød
Other Authors: Yáñez, J
Format: Article in Journal/Newspaper
Language:English
Published: Oxford University Press (OUP) 2023
Subjects:
Online Access:http://dx.doi.org/10.1093/g3journal/jkad069
https://academic.oup.com/g3journal/advance-article-pdf/doi/10.1093/g3journal/jkad069/49651789/jkad069.pdf
https://academic.oup.com/g3journal/article-pdf/13/6/jkad069/56716340/jkad069.pdf
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spelling croxfordunivpr:10.1093/g3journal/jkad069 2024-05-19T07:37:41+00:00 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 Yáñez, J 2023 http://dx.doi.org/10.1093/g3journal/jkad069 https://academic.oup.com/g3journal/advance-article-pdf/doi/10.1093/g3journal/jkad069/49651789/jkad069.pdf https://academic.oup.com/g3journal/article-pdf/13/6/jkad069/56716340/jkad069.pdf en eng Oxford University Press (OUP) https://creativecommons.org/licenses/by/4.0/ G3: Genes, Genomes, Genetics volume 13, issue 6 ISSN 2160-1836 journal-article 2023 croxfordunivpr https://doi.org/10.1093/g3journal/jkad069 2024-05-02T09:29:41Z Abstract 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. Article in Journal/Newspaper Atlantic salmon Salmo salar Oxford University Press G3 Genes|Genomes|Genetics
institution Open Polar
collection Oxford University Press
op_collection_id croxfordunivpr
language English
description Abstract 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.
author2 Yáñez, J
format Article in Journal/Newspaper
author Holen, Matilde Mengkrog
Vaaje-Kolstad, Gustav
Kent, Matthew Peter
Sandve, Simen Rød
spellingShingle 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)
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 (OUP)
publishDate 2023
url http://dx.doi.org/10.1093/g3journal/jkad069
https://academic.oup.com/g3journal/advance-article-pdf/doi/10.1093/g3journal/jkad069/49651789/jkad069.pdf
https://academic.oup.com/g3journal/article-pdf/13/6/jkad069/56716340/jkad069.pdf
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source G3: Genes, Genomes, Genetics
volume 13, issue 6
ISSN 2160-1836
op_rights https://creativecommons.org/licenses/by/4.0/
op_doi https://doi.org/10.1093/g3journal/jkad069
container_title G3 Genes|Genomes|Genetics
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