Analysis of Polycerate Mutants Reveals the Evolutionary Co-option of HOXD1 for Horn Patterning in Bovidae
Abstract In the course of evolution, pecorans (i.e., higher ruminants) developed a remarkable diversity of osseous cranial appendages, collectively referred to as “headgear,” which likely share the same origin and genetic basis. However, the nature and function of the genetic determinants underlying...
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| Veröffentlicht in: | Molecular biology and evolution 2021-05, Vol.38 (6), p.2260-2272 |
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| creator | Allais-Bonnet, Aurélie Hintermann, Aurélie Deloche, Marie-Christine Cornette, Raphaël Bardou, Philippe Naval-Sanchez, Marina Pinton, Alain Haruda, Ashleigh Grohs, Cécile Zakany, Jozsef Bigi, Daniele Medugorac, Ivica Putelat, Olivier Greyvenstein, Ockert Hadfield, Tracy Jemaa, Slim Ben Bunevski, Gjoko Menzi, Fiona Hirter, Nathalie Paris, Julia M Hedges, John Palhiere, Isabelle Rupp, Rachel Lenstra, Johannes A Gidney, Louisa Lesur, Joséphine Schafberg, Renate Stache, Michael Wandhammer, Marie-Dominique Arbogast, Rose-Marie Guintard, Claude Blin, Amandine Boukadiri, Abdelhak Rivière, Julie Esquerré, Diane Donnadieu, Cécile Danchin-Burge, Coralie Reich, Coralie M Riley, David G Marle-Koster, Este van Cockett, Noelle Hayes, Benjamin J Drögemüller, Cord Kijas, James Pailhoux, Eric Tosser-Klopp, Gwenola Duboule, Denis Capitan, Aurélien |
| description | Abstract
In the course of evolution, pecorans (i.e., higher ruminants) developed a remarkable diversity of osseous cranial appendages, collectively referred to as “headgear,” which likely share the same origin and genetic basis. However, the nature and function of the genetic determinants underlying their number and position remain elusive. Jacob and other rare populations of sheep and goats are characterized by polyceraty, the presence of more than two horns. Here, we characterize distinct POLYCERATE alleles in each species, both associated with defective HOXD1 function. We show that haploinsufficiency at this locus results in the splitting of horn bud primordia, likely following the abnormal extension of an initial morphogenetic field. These results highlight the key role played by this gene in headgear patterning and illustrate the evolutionary co-option of a gene involved in the early development of bilateria to properly fix the position and number of these distinctive organs of Bovidae. |
| doi_str_mv | 10.1093/molbev/msab021 |
| format | Article |
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In the course of evolution, pecorans (i.e., higher ruminants) developed a remarkable diversity of osseous cranial appendages, collectively referred to as “headgear,” which likely share the same origin and genetic basis. However, the nature and function of the genetic determinants underlying their number and position remain elusive. Jacob and other rare populations of sheep and goats are characterized by polyceraty, the presence of more than two horns. Here, we characterize distinct POLYCERATE alleles in each species, both associated with defective HOXD1 function. We show that haploinsufficiency at this locus results in the splitting of horn bud primordia, likely following the abnormal extension of an initial morphogenetic field. These results highlight the key role played by this gene in headgear patterning and illustrate the evolutionary co-option of a gene involved in the early development of bilateria to properly fix the position and number of these distinctive organs of Bovidae.</description><identifier>ISSN: 1537-1719</identifier><identifier>ISSN: 0737-4038</identifier><identifier>EISSN: 1537-1719</identifier><identifier>DOI: 10.1093/molbev/msab021</identifier><identifier>PMID: 33528505</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Animal genetics ; Development Biology ; Discoveries ; Embryology and Organogenesis ; Genetics ; Life Sciences ; Morphogenesis</subject><ispartof>Molecular biology and evolution, 2021-05, Vol.38 (6), p.2260-2272</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. 2021</rights><rights>The Author(s) 2021. 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In the course of evolution, pecorans (i.e., higher ruminants) developed a remarkable diversity of osseous cranial appendages, collectively referred to as “headgear,” which likely share the same origin and genetic basis. However, the nature and function of the genetic determinants underlying their number and position remain elusive. Jacob and other rare populations of sheep and goats are characterized by polyceraty, the presence of more than two horns. Here, we characterize distinct POLYCERATE alleles in each species, both associated with defective HOXD1 function. We show that haploinsufficiency at this locus results in the splitting of horn bud primordia, likely following the abnormal extension of an initial morphogenetic field. 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Gwenola</creatorcontrib><creatorcontrib>Duboule, Denis</creatorcontrib><creatorcontrib>Capitan, Aurélien</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Molecular biology and evolution</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Allais-Bonnet, Aurélie</au><au>Hintermann, Aurélie</au><au>Deloche, Marie-Christine</au><au>Cornette, Raphaël</au><au>Bardou, Philippe</au><au>Naval-Sanchez, Marina</au><au>Pinton, Alain</au><au>Haruda, Ashleigh</au><au>Grohs, Cécile</au><au>Zakany, Jozsef</au><au>Bigi, Daniele</au><au>Medugorac, Ivica</au><au>Putelat, Olivier</au><au>Greyvenstein, Ockert</au><au>Hadfield, Tracy</au><au>Jemaa, Slim Ben</au><au>Bunevski, Gjoko</au><au>Menzi, Fiona</au><au>Hirter, Nathalie</au><au>Paris, Julia M</au><au>Hedges, John</au><au>Palhiere, Isabelle</au><au>Rupp, Rachel</au><au>Lenstra, Johannes A</au><au>Gidney, Louisa</au><au>Lesur, Joséphine</au><au>Schafberg, Renate</au><au>Stache, Michael</au><au>Wandhammer, Marie-Dominique</au><au>Arbogast, Rose-Marie</au><au>Guintard, Claude</au><au>Blin, Amandine</au><au>Boukadiri, Abdelhak</au><au>Rivière, Julie</au><au>Esquerré, Diane</au><au>Donnadieu, Cécile</au><au>Danchin-Burge, Coralie</au><au>Reich, Coralie M</au><au>Riley, David G</au><au>Marle-Koster, Este van</au><au>Cockett, Noelle</au><au>Hayes, Benjamin J</au><au>Drögemüller, Cord</au><au>Kijas, James</au><au>Pailhoux, Eric</au><au>Tosser-Klopp, Gwenola</au><au>Duboule, Denis</au><au>Capitan, Aurélien</au><au>Wittkopp, Patricia</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Analysis of Polycerate Mutants Reveals the Evolutionary Co-option of HOXD1 for Horn Patterning in Bovidae</atitle><jtitle>Molecular biology and evolution</jtitle><addtitle>Mol Biol Evol</addtitle><date>2021-05-19</date><risdate>2021</risdate><volume>38</volume><issue>6</issue><spage>2260</spage><epage>2272</epage><pages>2260-2272</pages><issn>1537-1719</issn><issn>0737-4038</issn><eissn>1537-1719</eissn><abstract>Abstract
In the course of evolution, pecorans (i.e., higher ruminants) developed a remarkable diversity of osseous cranial appendages, collectively referred to as “headgear,” which likely share the same origin and genetic basis. However, the nature and function of the genetic determinants underlying their number and position remain elusive. Jacob and other rare populations of sheep and goats are characterized by polyceraty, the presence of more than two horns. Here, we characterize distinct POLYCERATE alleles in each species, both associated with defective HOXD1 function. We show that haploinsufficiency at this locus results in the splitting of horn bud primordia, likely following the abnormal extension of an initial morphogenetic field. These results highlight the key role played by this gene in headgear patterning and illustrate the evolutionary co-option of a gene involved in the early development of bilateria to properly fix the position and number of these distinctive organs of Bovidae.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>33528505</pmid><doi>10.1093/molbev/msab021</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0003-3185-0932</orcidid><orcidid>https://orcid.org/0000-0003-0550-4673</orcidid><orcidid>https://orcid.org/0000-0001-5379-7314</orcidid><orcidid>https://orcid.org/0000-0002-5484-0270</orcidid><orcidid>https://orcid.org/0000-0003-3375-5816</orcidid><orcidid>https://orcid.org/0000-0002-0809-7180</orcidid><orcidid>https://orcid.org/0000-0003-0195-8766</orcidid><orcidid>https://orcid.org/0000-0002-0004-0251</orcidid><orcidid>https://orcid.org/0009-0009-6128-9569</orcidid><orcidid>https://orcid.org/0000-0003-4245-7140</orcidid><orcidid>https://orcid.org/0000-0002-9411-9605</orcidid><orcidid>https://orcid.org/0000-0002-5164-3095</orcidid><orcidid>https://orcid.org/0000-0001-6646-1932</orcidid><orcidid>https://orcid.org/0000-0001-9773-522X</orcidid><orcidid>https://orcid.org/0000-0001-8012-9143</orcidid><orcidid>https://orcid.org/0009-0009-3557-8551</orcidid><orcidid>https://orcid.org/0000-0002-3563-8966</orcidid><orcidid>https://orcid.org/0000-0003-4182-4201</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1537-1719 |
| ispartof | Molecular biology and evolution, 2021-05, Vol.38 (6), p.2260-2272 |
| issn | 1537-1719 0737-4038 1537-1719 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_8136503 |
| source | DOAJ Directory of Open Access Journals; Oxford Journals Open Access Collection; EZB-FREE-00999 freely available EZB journals; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry |
| subjects | Animal genetics Development Biology Discoveries Embryology and Organogenesis Genetics Life Sciences Morphogenesis |
| title | Analysis of Polycerate Mutants Reveals the Evolutionary Co-option of HOXD1 for Horn Patterning in Bovidae |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-23T09%3A47%3A49IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Analysis%20of%20Polycerate%20Mutants%20Reveals%20the%20Evolutionary%20Co-option%20of%20HOXD1%20for%20Horn%20Patterning%20in%20Bovidae&rft.jtitle=Molecular%20biology%20and%20evolution&rft.au=Allais-Bonnet,%20Aur%C3%A9lie&rft.date=2021-05-19&rft.volume=38&rft.issue=6&rft.spage=2260&rft.epage=2272&rft.pages=2260-2272&rft.issn=1537-1719&rft.eissn=1537-1719&rft_id=info:doi/10.1093/molbev/msab021&rft_dat=%3Cproquest_pubme%3E2485517107%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2485517107&rft_id=info:pmid/33528505&rft_oup_id=10.1093/molbev/msab021&rfr_iscdi=true |