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Ruminant-specific retrotransposons shape regulatory evolution of bovine immunity

Cattle are an important livestock species, and mapping the genomic architecture of agriculturally relevant traits such as disease susceptibility is a major challenge in the bovine research community. Lineage-specific transposable elements (TEs) are increasingly recognized to contribute to gene regul...

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Autores principales: Kelly, Conor J., Chitko-McKown, Carol G., Chuong, Edward B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9435751/
https://www.ncbi.nlm.nih.gov/pubmed/35948370
http://dx.doi.org/10.1101/gr.276241.121
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author Kelly, Conor J.
Chitko-McKown, Carol G.
Chuong, Edward B.
author_facet Kelly, Conor J.
Chitko-McKown, Carol G.
Chuong, Edward B.
author_sort Kelly, Conor J.
collection PubMed
description Cattle are an important livestock species, and mapping the genomic architecture of agriculturally relevant traits such as disease susceptibility is a major challenge in the bovine research community. Lineage-specific transposable elements (TEs) are increasingly recognized to contribute to gene regulatory evolution and variation, but this possibility has been largely unexplored in ruminant genomes. We conducted epigenomic profiling of the type II interferon (IFN) response in bovine cells and found thousands of ruminant-specific TEs including MER41_BT and Bov-A2 elements predicted to act as IFN-inducible enhancer elements. CRISPR knockout experiments in bovine cells established that critical immune factors including IFNAR2 and IL2RB are transcriptionally regulated by TE-derived enhancers. Finally, population genomic analysis of 38 individuals revealed that a subset of polymorphic TE insertions may function as enhancers in modern cattle. Our study reveals that lineage-specific TEs have shaped the evolution of ruminant IFN responses and potentially continue to contribute to immune gene regulatory differences across modern breeds and individuals. Together with previous work in human cells, our findings demonstrate that lineage-specific TEs have been independently co-opted to regulate IFN-inducible gene expression in multiple species, supporting TE co-option as a recurrent mechanism driving the evolution of IFN-inducible transcriptional networks.
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spelling pubmed-94357512023-02-01 Ruminant-specific retrotransposons shape regulatory evolution of bovine immunity Kelly, Conor J. Chitko-McKown, Carol G. Chuong, Edward B. Genome Res Research Cattle are an important livestock species, and mapping the genomic architecture of agriculturally relevant traits such as disease susceptibility is a major challenge in the bovine research community. Lineage-specific transposable elements (TEs) are increasingly recognized to contribute to gene regulatory evolution and variation, but this possibility has been largely unexplored in ruminant genomes. We conducted epigenomic profiling of the type II interferon (IFN) response in bovine cells and found thousands of ruminant-specific TEs including MER41_BT and Bov-A2 elements predicted to act as IFN-inducible enhancer elements. CRISPR knockout experiments in bovine cells established that critical immune factors including IFNAR2 and IL2RB are transcriptionally regulated by TE-derived enhancers. Finally, population genomic analysis of 38 individuals revealed that a subset of polymorphic TE insertions may function as enhancers in modern cattle. Our study reveals that lineage-specific TEs have shaped the evolution of ruminant IFN responses and potentially continue to contribute to immune gene regulatory differences across modern breeds and individuals. Together with previous work in human cells, our findings demonstrate that lineage-specific TEs have been independently co-opted to regulate IFN-inducible gene expression in multiple species, supporting TE co-option as a recurrent mechanism driving the evolution of IFN-inducible transcriptional networks. Cold Spring Harbor Laboratory Press 2022-08 /pmc/articles/PMC9435751/ /pubmed/35948370 http://dx.doi.org/10.1101/gr.276241.121 Text en © 2022 Kelly et al.; Published by Cold Spring Harbor Laboratory Press https://creativecommons.org/licenses/by-nc/4.0/This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see https://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/ (https://creativecommons.org/licenses/by-nc/4.0/) .
spellingShingle Research
Kelly, Conor J.
Chitko-McKown, Carol G.
Chuong, Edward B.
Ruminant-specific retrotransposons shape regulatory evolution of bovine immunity
title Ruminant-specific retrotransposons shape regulatory evolution of bovine immunity
title_full Ruminant-specific retrotransposons shape regulatory evolution of bovine immunity
title_fullStr Ruminant-specific retrotransposons shape regulatory evolution of bovine immunity
title_full_unstemmed Ruminant-specific retrotransposons shape regulatory evolution of bovine immunity
title_short Ruminant-specific retrotransposons shape regulatory evolution of bovine immunity
title_sort ruminant-specific retrotransposons shape regulatory evolution of bovine immunity
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9435751/
https://www.ncbi.nlm.nih.gov/pubmed/35948370
http://dx.doi.org/10.1101/gr.276241.121
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