Analysis of Polycerate Mutants Reveals the Evolutionary Co-option of HOXD1 for Horn Patterning in Bovidae

Aurélie Allais-Bonnet; Aurélie Hintermann; Marie-Christine Deloche; Raphaël Cornette; Philippe Bardou; Marina Naval-Sanchez; Alain Pinton; Ashleigh Haruda; Cécile Grohs; Jozsef Zakany; Daniele Bigi; Ivica Medugorac; Olivier Putelat; Ockert Greyvenstein; Tracy Hadfield; Slim Ben Jemaa; Gjoko Bunevski; Fiona Menzi; Nathalie Hirter; Julia M Paris; John Hedges; Isabelle Palhiere; Rachel Rupp; Johannes A Lenstra; Louisa Gidney; Joséphine Lesur; Renate Schafberg; Michael Stache; Marie-Dominique Wandhammer; Rose-Marie Arbogast; Claude Guintard; Amandine Blin; Abdelhak Boukadiri; Julie Rivière; Diane Esquerré; Cécile Donnadieu; Coralie Danchin-Burge; Coralie M Reich; David G Riley; Este van Marle-Koster; Noelle Cockett; Benjamin J Hayes; Cord Drögemüller; James Kijas; Eric Pailhoux; Gwenola Tosser-Klopp; Denis Duboule; Aurélien Capitan

doi:10.1093/molbev/msab021

Analysis of Polycerate Mutants Reveals the Evolutionary Co-option of HOXD1 for Horn Patterning in Bovidae

Aurélie Allais-Bonnet, Aurélie Hintermann, Marie-Christine Deloche, Raphaël Cornette, Philippe Bardou, Marina Naval-Sanchez, Alain Pinton, Ashleigh Haruda, Cécile Grohs, Jozsef Zakany, Daniele Bigi, Ivica Medugorac, Olivier Putelat, Ockert Greyvenstein, Tracy Hadfield, Slim Ben Jemaa, Gjoko Bunevski, Fiona Menzi, Nathalie Hirter, Julia M ParisJohn Hedges, Isabelle Palhiere, Rachel Rupp, Johannes A Lenstra, Louisa Gidney, Joséphine Lesur, Renate Schafberg, Michael Stache, Marie-Dominique Wandhammer, Rose-Marie Arbogast, Claude Guintard, Amandine Blin, Abdelhak Boukadiri, Julie Rivière, Diane Esquerré, Cécile Donnadieu, Coralie Danchin-Burge, Coralie M Reich, David G Riley, Este van Marle-Koster, Noelle Cockett, Benjamin J Hayes, Cord Drögemüller, James Kijas, Eric Pailhoux, Gwenola Tosser-Klopp, Denis Duboule, Aurélien Capitan

Research output: Contribution to journal › Article › Academic › peer-review

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.

Original language	English
Pages (from-to)	2260-2272
Number of pages	13
Journal	Molecular Biology and Evolution
Volume	38
Issue number	6
Early online date	2 Feb 2021
DOIs	https://doi.org/10.1093/molbev/msab021
Publication status	Published - 1 Jun 2021
Externally published	Yes

Bibliographical note

Publisher Copyright:
© 2021 The Author(s). Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

Keywords

Hox genes
co-option
goat and sheep genomics
regulatory mutation

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10.1093/molbev/msab021Licence: CC BY-NC

msab021Final published version, 1.23 MBLicence: CC BY-NC

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Allais-Bonnet, A., Hintermann, A., Deloche, M.-C., Cornette, R., Bardou, P., Naval-Sanchez, M., Pinton, A., Haruda, A., Grohs, C., Zakany, J., Bigi, D., Medugorac, I., Putelat, O., Greyvenstein, O., Hadfield, T., Jemaa, S. B., Bunevski, G., Menzi, F., Hirter, N., ... Capitan, A. (2021). Analysis of Polycerate Mutants Reveals the Evolutionary Co-option of HOXD1 for Horn Patterning in Bovidae. Molecular Biology and Evolution, 38(6), 2260-2272. https://doi.org/10.1093/molbev/msab021

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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.",

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note = "Publisher Copyright: {\textcopyright} 2021 The Author(s). Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.",

year = "2021",

month = jun,

day = "1",

doi = "10.1093/molbev/msab021",

language = "English",

volume = "38",

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Allais-Bonnet, A, Hintermann, A, Deloche, M-C, Cornette, R, Bardou, P, Naval-Sanchez, M, Pinton, A, Haruda, A, Grohs, C, Zakany, J, Bigi, D, Medugorac, I, Putelat, O, Greyvenstein, O, Hadfield, T, Jemaa, SB, Bunevski, G, Menzi, F, Hirter, N, Paris, JM, Hedges, J, Palhiere, I, Rupp, R, Lenstra, JA, Gidney, L, Lesur, J, Schafberg, R, Stache, M, Wandhammer, M-D, Arbogast, R-M, Guintard, C, Blin, A, Boukadiri, A, Rivière, J, Esquerré, D, Donnadieu, C, Danchin-Burge, C, Reich, CM, Riley, DG, van Marle-Koster, E, Cockett, N, Hayes, BJ, Drögemüller, C, Kijas, J, Pailhoux, E, Tosser-Klopp, G, Duboule, D & Capitan, A 2021, 'Analysis of Polycerate Mutants Reveals the Evolutionary Co-option of HOXD1 for Horn Patterning in Bovidae', Molecular Biology and Evolution, vol. 38, no. 6, pp. 2260-2272. https://doi.org/10.1093/molbev/msab021

TY - JOUR

T1 - Analysis of Polycerate Mutants Reveals the Evolutionary Co-option of HOXD1 for Horn Patterning in Bovidae

AU - Allais-Bonnet, Aurélie

AU - Hintermann, Aurélie

AU - Deloche, Marie-Christine

AU - Cornette, Raphaël

AU - Bardou, Philippe

AU - Naval-Sanchez, Marina

AU - Pinton, Alain

AU - Haruda, Ashleigh

AU - Grohs, Cécile

AU - Zakany, Jozsef

AU - Bigi, Daniele

AU - Medugorac, Ivica

AU - Putelat, Olivier

AU - Greyvenstein, Ockert

AU - Hadfield, Tracy

AU - Jemaa, Slim Ben

AU - Bunevski, Gjoko

AU - Menzi, Fiona

AU - Hirter, Nathalie

AU - Paris, Julia M

AU - Hedges, John

AU - Palhiere, Isabelle

AU - Rupp, Rachel

AU - Lenstra, Johannes A

AU - Gidney, Louisa

AU - Lesur, Joséphine

AU - Schafberg, Renate

AU - Stache, Michael

AU - Wandhammer, Marie-Dominique

AU - Arbogast, Rose-Marie

AU - Guintard, Claude

AU - Blin, Amandine

AU - Boukadiri, Abdelhak

AU - Rivière, Julie

AU - Esquerré, Diane

AU - Donnadieu, Cécile

AU - Danchin-Burge, Coralie

AU - Reich, Coralie M

AU - Riley, David G

AU - van Marle-Koster, Este

AU - Cockett, Noelle

AU - Hayes, Benjamin J

AU - Drögemüller, Cord

AU - Kijas, James

AU - Pailhoux, Eric

AU - Tosser-Klopp, Gwenola

AU - Duboule, Denis

AU - Capitan, Aurélien

PY - 2021/6/1

Y1 - 2021/6/1

N2 - 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.

AB - 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.

KW - Hox genes

KW - co-option

KW - goat and sheep genomics

KW - regulatory mutation

UR - http://www.scopus.com/inward/record.url?scp=85107087208&partnerID=8YFLogxK

U2 - 10.1093/molbev/msab021

DO - 10.1093/molbev/msab021

M3 - Article

C2 - 33528505

SN - 0737-4038

VL - 38

SP - 2260

EP - 2272

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

IS - 6

ER -

Analysis of Polycerate Mutants Reveals the Evolutionary Co-option of HOXD1 for Horn Patterning in Bovidae

Abstract

Bibliographical note

Keywords

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