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

AbstractChitin 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. Rece...

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Published in:G3 Genes|Genomes|Genetics
Main Authors: Matilde Mengkrog Holen, Gustav Vaaje-Kolstad, Matthew Peter Kent, Simen Rød Sandve
Format: Article in Journal/Newspaper
Language:English
Published: Oxford University Press 2023
Subjects:
Online Access:https://doi.org/10.1093/g3journal/jkad069
https://doaj.org/article/255dd6e0cb794c26a3e04682f4f6dfc1
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spelling ftdoajarticles:oai:doaj.org/article:255dd6e0cb794c26a3e04682f4f6dfc1 2023-07-30T04:02:25+02:00 Gene family expansion and functional diversification of chitinase and chitin synthase genes in Atlantic salmon ( Salmo salar ) Matilde Mengkrog Holen Gustav Vaaje-Kolstad Matthew Peter Kent Simen Rød Sandve 2023-03-01T00:00:00Z https://doi.org/10.1093/g3journal/jkad069 https://doaj.org/article/255dd6e0cb794c26a3e04682f4f6dfc1 EN eng Oxford University Press https://academic.oup.com/g3journal/article-lookup/doi/10.1093/g3journal/jkad069 https://doaj.org/toc/2160-1836 2160-1836 doi:10.1093/g3journal/jkad069 https://doaj.org/article/255dd6e0cb794c26a3e04682f4f6dfc1 G3: Genes, Genomes, Genetics, Vol 13, Iss 6 (2023) Genetics QH426-470 article 2023 ftdoajarticles https://doi.org/10.1093/g3journal/jkad069 2023-07-09T00:37:10Z AbstractChitin 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 Directory of Open Access Journals: DOAJ Articles G3 Genes|Genomes|Genetics
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Genetics
QH426-470
spellingShingle Genetics
QH426-470
Matilde Mengkrog Holen
Gustav Vaaje-Kolstad
Matthew Peter Kent
Simen Rød Sandve
Gene family expansion and functional diversification of chitinase and chitin synthase genes in Atlantic salmon ( Salmo salar )
topic_facet Genetics
QH426-470
description AbstractChitin 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 Article in Journal/Newspaper
author Matilde Mengkrog Holen
Gustav Vaaje-Kolstad
Matthew Peter Kent
Simen Rød Sandve
author_facet Matilde Mengkrog Holen
Gustav Vaaje-Kolstad
Matthew Peter Kent
Simen Rød Sandve
author_sort Matilde Mengkrog Holen
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 https://doi.org/10.1093/g3journal/jkad069
https://doaj.org/article/255dd6e0cb794c26a3e04682f4f6dfc1
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source G3: Genes, Genomes, Genetics, Vol 13, Iss 6 (2023)
op_relation https://academic.oup.com/g3journal/article-lookup/doi/10.1093/g3journal/jkad069
https://doaj.org/toc/2160-1836
2160-1836
doi:10.1093/g3journal/jkad069
https://doaj.org/article/255dd6e0cb794c26a3e04682f4f6dfc1
op_doi https://doi.org/10.1093/g3journal/jkad069
container_title G3 Genes|Genomes|Genetics
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