Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genes

Background: ETCHbox genes are eutherian-specific homeobox genes expressed during preimplantation develop-ment at a time when the first cell lineage decisions are being made. The mouse has an unusual repertoire of ETCH-box genes with several gene families lost in evolution and the remaining two, Crxo...

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Authors: Royall, Amy H, Maeso, Ignacio, Dunwell, Thomas L, Holland, Peter WH
Format: article
Status:Published version
Publication Date:2018
Country:España
Institution:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
Repository:Recercat. Dipósit de la Recerca de Catalunya
OAI Identifier:oai:recercat.cat:2445/192240
Online Access:https://hdl.handle.net/2445/192240
Access Level:Open access
Keyword:Gens
Cromosomes
Ratolins transgènics
Genoma humà
Genes
Chromosomes
Transgenic mice
Human genome
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spelling Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genesRoyall, Amy HMaeso, IgnacioDunwell, Thomas LHolland, Peter WHGensCromosomesRatolins transgènicsGenoma humàGenesChromosomesTransgenic miceHuman genomeBackground: ETCHbox genes are eutherian-specific homeobox genes expressed during preimplantation develop-ment at a time when the first cell lineage decisions are being made. The mouse has an unusual repertoire of ETCH-box genes with several gene families lost in evolution and the remaining two, Crxos and Obox, greatly divergent in sequence and number. Each has undergone duplication to give a double homeodomain Crxos locus and a large cluster of over 60 Obox loci. The gene content differences between species raise important questions about how evolution can tolerate loss of genes implicated in key developmental events. Results: We find that Crxos internal duplication occurred in the mouse lineage, while Obox duplication was stepwise, generating subgroups with distinct sequence and expression. Ectopic expression of three Obox genes and a Crxos transcript in primary mouse embryonic cells followed by transcriptome sequencing allowed investigation into their functional roles. We find distinct transcriptomic influences for different Obox subgroups and Crxos, including modula-tion of genes related to zygotic genome activation and preparation for blastocyst formation. Comparison with similar experiments performed using human homeobox genes reveals striking overlap between genes downstream of mouse Crxos and genes downstream of human ARGFX. Conclusions: Mouse Crxos and human ARGFX homeobox genes are paralogous rather than orthologous, yet they have evolved to regulate a common set of genes. This suggests there was compensation of function alongside gene loss through co-option of a different locus. Functional compensation by non-orthologous genes with dissimilar sequences is unusual but may indicate underlying distributed robustness. Compensation may be driven by the strong evolutionary pressure for successful early embryo development.BioMed Central2023202320182023info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersion14 p.application/pdfhttps://hdl.handle.net/2445/192240Articles publicats en revistes (Genètica, Microbiologia i Estadística)reponame:Recercat. Dipósit de la Recerca de Catalunyainstname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)InglésReproducció del document publicat a: https://doi.org/10.1186/s13227-018-0091-4Evodevo, 2018, vol. 9, num. 2, p. 1-14https://doi.org/10.1186/s13227-018-0091-4cc-by (c) Royall, Amy H et al., 2018https://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:recercat.cat:2445/1922402026-05-29T05:05:01Z
dc.title.none.fl_str_mv Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genes
title Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genes
spellingShingle Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genes
Royall, Amy H
Gens
Cromosomes
Ratolins transgènics
Genoma humà
Genes
Chromosomes
Transgenic mice
Human genome
title_short Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genes
title_full Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genes
title_fullStr Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genes
title_full_unstemmed Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genes
title_sort Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genes
dc.creator.none.fl_str_mv Royall, Amy H
Maeso, Ignacio
Dunwell, Thomas L
Holland, Peter WH
author Royall, Amy H
author_facet Royall, Amy H
Maeso, Ignacio
Dunwell, Thomas L
Holland, Peter WH
author_role author
author2 Maeso, Ignacio
Dunwell, Thomas L
Holland, Peter WH
author2_role author
author
author
dc.subject.none.fl_str_mv Gens
Cromosomes
Ratolins transgènics
Genoma humà
Genes
Chromosomes
Transgenic mice
Human genome
topic Gens
Cromosomes
Ratolins transgènics
Genoma humà
Genes
Chromosomes
Transgenic mice
Human genome
description Background: ETCHbox genes are eutherian-specific homeobox genes expressed during preimplantation develop-ment at a time when the first cell lineage decisions are being made. The mouse has an unusual repertoire of ETCH-box genes with several gene families lost in evolution and the remaining two, Crxos and Obox, greatly divergent in sequence and number. Each has undergone duplication to give a double homeodomain Crxos locus and a large cluster of over 60 Obox loci. The gene content differences between species raise important questions about how evolution can tolerate loss of genes implicated in key developmental events. Results: We find that Crxos internal duplication occurred in the mouse lineage, while Obox duplication was stepwise, generating subgroups with distinct sequence and expression. Ectopic expression of three Obox genes and a Crxos transcript in primary mouse embryonic cells followed by transcriptome sequencing allowed investigation into their functional roles. We find distinct transcriptomic influences for different Obox subgroups and Crxos, including modula-tion of genes related to zygotic genome activation and preparation for blastocyst formation. Comparison with similar experiments performed using human homeobox genes reveals striking overlap between genes downstream of mouse Crxos and genes downstream of human ARGFX. Conclusions: Mouse Crxos and human ARGFX homeobox genes are paralogous rather than orthologous, yet they have evolved to regulate a common set of genes. This suggests there was compensation of function alongside gene loss through co-option of a different locus. Functional compensation by non-orthologous genes with dissimilar sequences is unusual but may indicate underlying distributed robustness. Compensation may be driven by the strong evolutionary pressure for successful early embryo development.
publishDate 2018
dc.date.none.fl_str_mv 2018
2023
2023
2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/2445/192240
url https://hdl.handle.net/2445/192240
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Reproducció del document publicat a: https://doi.org/10.1186/s13227-018-0091-4
Evodevo, 2018, vol. 9, num. 2, p. 1-14
https://doi.org/10.1186/s13227-018-0091-4
dc.rights.none.fl_str_mv cc-by (c) Royall, Amy H et al., 2018
https://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv cc-by (c) Royall, Amy H et al., 2018
https://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 14 p.
application/pdf
dc.publisher.none.fl_str_mv BioMed Central
publisher.none.fl_str_mv BioMed Central
dc.source.none.fl_str_mv Articles publicats en revistes (Genètica, Microbiologia i Estadística)
reponame:Recercat. Dipósit de la Recerca de Catalunya
instname:Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
instname_str Varias* (Consorci de Biblioteques Universitáries de Catalunya, Centre de Serveis Científics i Acadèmics de Catalunya)
reponame_str Recercat. Dipósit de la Recerca de Catalunya
collection Recercat. Dipósit de la Recerca de Catalunya
repository.name.fl_str_mv
repository.mail.fl_str_mv
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score 15,811543

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