Conserved and divergent arms of the antiviral response in the duplicated genomes of salmonid fishes

Thomas Clark; Shahmir Naseer; Manu Kumar Gundappa; Audrey Laurent; Aline Perquis; Bertrand Collet; Daniel J. Macqueen; Samuel A.M. Martin; Pierre Boudinot

doi:10.1016/j.ygeno.2023.110663

Conserved and divergent arms of the antiviral response in the duplicated genomes of salmonid fishes

Thomas Clark, Shahmir Naseer, Manu Kumar Gundappa, Audrey Laurent, Aline Perquis, Bertrand Collet, Daniel J. Macqueen, Samuel A.M. Martin^* (Corresponding Author), Pierre Boudinot^* (Corresponding Author)

^*Corresponding author for this work

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Abstract

Antiviral innate immunity is orchestrated by the interferon system, which appeared in ancestors of jawed vertebrates. Interferon upregulation induces hundreds of interferon-stimulated-genes (ISGs) with effector or regulatory functions. Here we investigated the evolutionary diversification of ISG responses through comparison of two salmonid fishes, accounting for the impact of sequential whole genome duplications ancestral to teleosts and salmonids. We analysed the transcriptomic response of the IFN pathway in the head kidney of rainbow trout and Atlantic salmon, which separated 25–30 Mya. We identified a large set of ISGs conserved in both species and cross-referenced them with zebrafish and human ISGs. In contrast, around one-third of salmonid ISG lacked orthologs in human, mouse, chicken or frog, and often between rainbow trout and Atlantic salmon, revealing a fast-evolving, lineage-specific arm of the antiviral response. This study also provides a key resource for in-depth functional analysis of ISGs in salmonids of commercial significance.

Original language	English
Article number	110663
Journal	Genomics
Volume	115
Issue number	4
Early online date	5 Jun 2023
DOIs	https://doi.org/10.1016/j.ygeno.2023.110663
Publication status	Published - 1 Jul 2023

Bibliographical note

Funding Information:
This work was funded by the European Union's Horizon 2020 research and innovation program under grant agreement No 817923 (AQUAFAANG), by ANR (ANR-21-CE35-0019, LipofishVac), by the Eranet ICRAD-Nucnanofish (ANR_13001498 and BBSRC_ICRAD BB/V019902/1), by the BBSRC Institutional strategic programme award (BBS/E/D/20002174) and by institutional grants from INRAE. We thank Drs Hugues Roest Crollius, Camille Berthelot, Alexandra Louis and Elise Parey for sharing synteny-based corrected data produced by SCORPiOs, and Louis du Pasquier for insightful discussions.

Data Availability Statement

I have shared the link to my data at the Attach file step.

Keywords

Animals
Antiviral Agents/pharmacology
Genome
Humans
Interferons/genetics
Mice
Oncorhynchus mykiss/genetics
Zebrafish/genetics

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0888-7543/© 2023 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
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Cite this

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title = "Conserved and divergent arms of the antiviral response in the duplicated genomes of salmonid fishes",

abstract = "Antiviral innate immunity is orchestrated by the interferon system, which appeared in ancestors of jawed vertebrates. Interferon upregulation induces hundreds of interferon-stimulated-genes (ISGs) with effector or regulatory functions. Here we investigated the evolutionary diversification of ISG responses through comparison of two salmonid fishes, accounting for the impact of sequential whole genome duplications ancestral to teleosts and salmonids. We analysed the transcriptomic response of the IFN pathway in the head kidney of rainbow trout and Atlantic salmon, which separated 25–30 Mya. We identified a large set of ISGs conserved in both species and cross-referenced them with zebrafish and human ISGs. In contrast, around one-third of salmonid ISG lacked orthologs in human, mouse, chicken or frog, and often between rainbow trout and Atlantic salmon, revealing a fast-evolving, lineage-specific arm of the antiviral response. This study also provides a key resource for in-depth functional analysis of ISGs in salmonids of commercial significance.",

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note = "Funding Information: This work was funded by the European Union's Horizon 2020 research and innovation program under grant agreement No 817923 (AQUAFAANG), by ANR (ANR-21-CE35-0019, LipofishVac), by the Eranet ICRAD-Nucnanofish (ANR_13001498 and BBSRC_ICRAD BB/V019902/1), by the BBSRC Institutional strategic programme award (BBS/E/D/20002174) and by institutional grants from INRAE. We thank Drs Hugues Roest Crollius, Camille Berthelot, Alexandra Louis and Elise Parey for sharing synteny-based corrected data produced by SCORPiOs, and Louis du Pasquier for insightful discussions. ",

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Conserved and divergent arms of the antiviral response in the duplicated genomes of salmonid fishes

Abstract

Bibliographical note

Data Availability Statement

Keywords

Access to Document

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