Cargando…

Transposable elements drive the evolution of metazoan zinc finger genes

Cys2-His2 zinc finger genes (ZNFs) form the largest family of transcription factors in metazoans. ZNF evolution is highly dynamic and characterized by the rapid expansion and contraction of numerous subfamilies across the animal phylogeny. The forces and mechanisms underlying rapid ZNF evolution rem...

Descripción completa

Detalles Bibliográficos
Autores principales: Wells, Jonathan N., Chang, Ni-Chen, McCormick, John, Coleman, Caitlyn, Ramos, Nathalie, Jin, Bozhou, Feschotte, Cédric
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10547256/
https://www.ncbi.nlm.nih.gov/pubmed/37714714
http://dx.doi.org/10.1101/gr.277966.123
_version_ 1785115022065664000
author Wells, Jonathan N.
Chang, Ni-Chen
McCormick, John
Coleman, Caitlyn
Ramos, Nathalie
Jin, Bozhou
Feschotte, Cédric
author_facet Wells, Jonathan N.
Chang, Ni-Chen
McCormick, John
Coleman, Caitlyn
Ramos, Nathalie
Jin, Bozhou
Feschotte, Cédric
author_sort Wells, Jonathan N.
collection PubMed
description Cys2-His2 zinc finger genes (ZNFs) form the largest family of transcription factors in metazoans. ZNF evolution is highly dynamic and characterized by the rapid expansion and contraction of numerous subfamilies across the animal phylogeny. The forces and mechanisms underlying rapid ZNF evolution remain poorly understood, but there is growing evidence that, in tetrapods, the targeting and repression of lineage-specific transposable elements (TEs) plays a critical role in the evolution of the Krüppel-associated box ZNF (KZNF) subfamily. Currently, it is unknown whether this function and coevolutionary relationship is unique to KZNFs or is a broader feature of metazoan ZNFs. Here, we present evidence that genomic conflict with TEs has been a central driver of the diversification of ZNFs in animals. Sampling from 3221 genome assemblies, we show that the copy number of retroelements correlates with that of ZNFs across at least 750 million years of metazoan evolution. Using computational predictions, we show that ZNFs preferentially bind TEs in diverse animal species. We further investigate the largest ZNF subfamily found in cyprinid fish, which is characterized by a conserved sequence we dubbed the fish N-terminal zinc finger–associated (FiNZ) domain. Zebrafish possess approximately 700 FiNZ-ZNFs, many of which are evolving adaptively under positive selection. Like mammalian KZNFs, most zebrafish FiNZ-ZNFs are expressed at the onset of zygotic genome activation, and blocking their translation using morpholinos during early embryogenesis results in derepression of transcriptionally active TEs. Together, these data suggest that ZNF diversification has been intimately connected to TE expansion throughout animal evolution.
format Online
Article
Text
id pubmed-10547256
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Cold Spring Harbor Laboratory Press
record_format MEDLINE/PubMed
spelling pubmed-105472562023-10-04 Transposable elements drive the evolution of metazoan zinc finger genes Wells, Jonathan N. Chang, Ni-Chen McCormick, John Coleman, Caitlyn Ramos, Nathalie Jin, Bozhou Feschotte, Cédric Genome Res Research Cys2-His2 zinc finger genes (ZNFs) form the largest family of transcription factors in metazoans. ZNF evolution is highly dynamic and characterized by the rapid expansion and contraction of numerous subfamilies across the animal phylogeny. The forces and mechanisms underlying rapid ZNF evolution remain poorly understood, but there is growing evidence that, in tetrapods, the targeting and repression of lineage-specific transposable elements (TEs) plays a critical role in the evolution of the Krüppel-associated box ZNF (KZNF) subfamily. Currently, it is unknown whether this function and coevolutionary relationship is unique to KZNFs or is a broader feature of metazoan ZNFs. Here, we present evidence that genomic conflict with TEs has been a central driver of the diversification of ZNFs in animals. Sampling from 3221 genome assemblies, we show that the copy number of retroelements correlates with that of ZNFs across at least 750 million years of metazoan evolution. Using computational predictions, we show that ZNFs preferentially bind TEs in diverse animal species. We further investigate the largest ZNF subfamily found in cyprinid fish, which is characterized by a conserved sequence we dubbed the fish N-terminal zinc finger–associated (FiNZ) domain. Zebrafish possess approximately 700 FiNZ-ZNFs, many of which are evolving adaptively under positive selection. Like mammalian KZNFs, most zebrafish FiNZ-ZNFs are expressed at the onset of zygotic genome activation, and blocking their translation using morpholinos during early embryogenesis results in derepression of transcriptionally active TEs. Together, these data suggest that ZNF diversification has been intimately connected to TE expansion throughout animal evolution. Cold Spring Harbor Laboratory Press 2023-08 /pmc/articles/PMC10547256/ /pubmed/37714714 http://dx.doi.org/10.1101/gr.277966.123 Text en © 2023 Wells et al.; Published by Cold Spring Harbor Laboratory Press https://creativecommons.org/licenses/by/4.0/This article, published in Genome Research, is available under a Creative Commons License (Attribution 4.0 International), as described at http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research
Wells, Jonathan N.
Chang, Ni-Chen
McCormick, John
Coleman, Caitlyn
Ramos, Nathalie
Jin, Bozhou
Feschotte, Cédric
Transposable elements drive the evolution of metazoan zinc finger genes
title Transposable elements drive the evolution of metazoan zinc finger genes
title_full Transposable elements drive the evolution of metazoan zinc finger genes
title_fullStr Transposable elements drive the evolution of metazoan zinc finger genes
title_full_unstemmed Transposable elements drive the evolution of metazoan zinc finger genes
title_short Transposable elements drive the evolution of metazoan zinc finger genes
title_sort transposable elements drive the evolution of metazoan zinc finger genes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10547256/
https://www.ncbi.nlm.nih.gov/pubmed/37714714
http://dx.doi.org/10.1101/gr.277966.123
work_keys_str_mv AT wellsjonathann transposableelementsdrivetheevolutionofmetazoanzincfingergenes
AT changnichen transposableelementsdrivetheevolutionofmetazoanzincfingergenes
AT mccormickjohn transposableelementsdrivetheevolutionofmetazoanzincfingergenes
AT colemancaitlyn transposableelementsdrivetheevolutionofmetazoanzincfingergenes
AT ramosnathalie transposableelementsdrivetheevolutionofmetazoanzincfingergenes
AT jinbozhou transposableelementsdrivetheevolutionofmetazoanzincfingergenes
AT feschottecedric transposableelementsdrivetheevolutionofmetazoanzincfingergenes