Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genes
Abstract Background ETCHbox genes are eutherian-specific homeobox genes expressed during preimplantation development at a time when the first cell lineage decisions are being made. The mouse has an unusual repertoire of ETCHbox genes with several gene families lost in evolution and the remaining two...
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| Format: | Article |
| Language: | English |
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BMC
2018-01-01
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| Series: | EvoDevo |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s13227-018-0091-4 |
| _version_ | 1818246616560173056 |
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| author | Amy H. Royall Ignacio Maeso Thomas L. Dunwell Peter W. H. Holland |
| author_facet | Amy H. Royall Ignacio Maeso Thomas L. Dunwell Peter W. H. Holland |
| author_sort | Amy H. Royall |
| collection | DOAJ |
| description | Abstract Background ETCHbox genes are eutherian-specific homeobox genes expressed during preimplantation development at a time when the first cell lineage decisions are being made. The mouse has an unusual repertoire of ETCHbox 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 modulation 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. |
| first_indexed | 2024-12-12T14:51:39Z |
| format | Article |
| id | doaj.art-27f1577861454bafa3f627c33de354f0 |
| institution | Directory Open Access Journal |
| issn | 2041-9139 |
| language | English |
| last_indexed | 2024-12-12T14:51:39Z |
| publishDate | 2018-01-01 |
| publisher | BMC |
| record_format | Article |
| series | EvoDevo |
| spelling | doaj.art-27f1577861454bafa3f627c33de354f02022-12-22T00:20:59ZengBMCEvoDevo2041-91392018-01-019111410.1186/s13227-018-0091-4Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genesAmy H. Royall0Ignacio Maeso1Thomas L. Dunwell2Peter W. H. Holland3Department of Zoology, University of OxfordCentro Andaluz de Biología del Desarrollo, Consejo Superior de Investigaciones Científicas/Universidad Pablo de OlavideDepartment of Zoology, University of OxfordDepartment of Zoology, University of OxfordAbstract Background ETCHbox genes are eutherian-specific homeobox genes expressed during preimplantation development at a time when the first cell lineage decisions are being made. The mouse has an unusual repertoire of ETCHbox 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 modulation 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.http://link.springer.com/article/10.1186/s13227-018-0091-4Gene duplicationGene lossHomeodomainPRD classARGFXTranscription factor |
| spellingShingle | Amy H. Royall Ignacio Maeso Thomas L. Dunwell Peter W. H. Holland Mouse Obox and Crxos modulate preimplantation transcriptional profiles revealing similarity between paralogous mouse and human homeobox genes EvoDevo Gene duplication Gene loss Homeodomain PRD class ARGFX Transcription factor |
| title | 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_short | 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 |
| topic | Gene duplication Gene loss Homeodomain PRD class ARGFX Transcription factor |
| url | http://link.springer.com/article/10.1186/s13227-018-0091-4 |
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