Homeobox Gene Duplication and Divergence in Arachnids

Homeobox genes are key toolkit genes that regulate the development of metazoans and changes in their regulation and copy number have contributed to the evolution of phenotypic diversity. We recently identified a whole genome duplication (WGD) event that occurred in an ancestor of spiders and scorpions (Arachnopulmonata), and that many homeobox genes, including two Hox clusters, appear to have been retained in arachnopulmonates. To better understand the consequences of this ancient WGD and the evolution of arachnid homeobox genes, we have characterized and compared the homeobox repertoires in a range of arachnids. We found that many families and clusters of these genes are duplicated in all studied arachnopulmonates (Parasteatoda tepidariorum, Pholcus phalangioides, Centruroides sculpturatus, and Mesobuthus martensii) compared with nonarachnopulmonate arachnids (Phalangium opilio, Neobisium carcinoides, Hesperochernes sp., and Ixodes scapularis). To assess divergence in the roles of homeobox ohnologs, we analyzed the expression of P. tepidariorum homeobox genes during embryogenesis and found pervasive changes in the level and timing of their expression. Furthermore, we compared the spatial expression of a subset of P. tepidariorum ohnologs with their single copy orthologs in P. opilio embryos. We found evidence for likely subfunctionlization and neofunctionalization of these genes in the spider. Overall our results show a high level of retention of homeobox genes in spiders and scorpions post-WGD, which is likely to have made a major contribution to their developmental evolution and diversification through pervasive subfunctionlization and neofunctionalization, and paralleling the outcomes of WGD in vertebrates.

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Main Authors: Leite, Daniel J., Baudouin-Gonzalez, Luís, Iwasaki-Yokozawa, Sawa, Lozano Fernández, Jesús, Turetzek, Natascha, Akiyama-Oda, Yasuko, Prpic, Nikola-Michael, Pisani, Davide, Oda, Hiroki, Sharma, Prashant P., McGregor, Alistair P.
Other Authors: Leverhulme Trust
Format: artículo biblioteca
Language:English
Published: Oxford University Press 2018-09
Subjects:Homeobox genes, Development, Gene duplication,
Online Access:http://hdl.handle.net/10261/217095
http://dx.doi.org/10.13039/100000001
http://dx.doi.org/10.13039/501100001659
http://dx.doi.org/10.13039/501100001691
http://dx.doi.org/10.13039/501100000275
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spelling dig-ibe-es-10261-2170952021-12-27T16:18:38Z Homeobox Gene Duplication and Divergence in Arachnids Leite, Daniel J. Baudouin-Gonzalez, Luís Iwasaki-Yokozawa, Sawa Lozano Fernández, Jesús Turetzek, Natascha Akiyama-Oda, Yasuko Prpic, Nikola-Michael Pisani, Davide Oda, Hiroki Sharma, Prashant P. McGregor, Alistair P. Leverhulme Trust Japan Society for the Promotion of Science National Science Foundation (US) German Research Foundation Homeobox genes Development Gene duplication Homeobox genes are key toolkit genes that regulate the development of metazoans and changes in their regulation and copy number have contributed to the evolution of phenotypic diversity. We recently identified a whole genome duplication (WGD) event that occurred in an ancestor of spiders and scorpions (Arachnopulmonata), and that many homeobox genes, including two Hox clusters, appear to have been retained in arachnopulmonates. To better understand the consequences of this ancient WGD and the evolution of arachnid homeobox genes, we have characterized and compared the homeobox repertoires in a range of arachnids. We found that many families and clusters of these genes are duplicated in all studied arachnopulmonates (Parasteatoda tepidariorum, Pholcus phalangioides, Centruroides sculpturatus, and Mesobuthus martensii) compared with nonarachnopulmonate arachnids (Phalangium opilio, Neobisium carcinoides, Hesperochernes sp., and Ixodes scapularis). To assess divergence in the roles of homeobox ohnologs, we analyzed the expression of P. tepidariorum homeobox genes during embryogenesis and found pervasive changes in the level and timing of their expression. Furthermore, we compared the spatial expression of a subset of P. tepidariorum ohnologs with their single copy orthologs in P. opilio embryos. We found evidence for likely subfunctionlization and neofunctionalization of these genes in the spider. Overall our results show a high level of retention of homeobox genes in spiders and scorpions post-WGD, which is likely to have made a major contribution to their developmental evolution and diversification through pervasive subfunctionlization and neofunctionalization, and paralleling the outcomes of WGD in vertebrates. This work was supported by a Leverhulme Trust grant (RPG2016-234) to A.P.M., Nigel Groome studentships to D.J.L. and L.B.G., a Marie Skłodowska-Curie Fellowship for J.L.-F. (655814), and the Japan Society for the Promotion of Science (JSPS) Grants-in-Aid for Scientific Research (KAKENHI) awards to H.O. (15K07139) and Y.A.-O. (26440130). P.P.S. was supported by National Science Foundation grant IOS-1552610. N.T. and N.M.P. were supported by grants from the Deutsche Forschungsgemeinschaft grant numbers PR 1109/4-1 and PR 1109/6-1. No 2020-07-27T12:33:19Z 2020-07-27T12:33:19Z 2018-09 artículo http://purl.org/coar/resource_type/c_6501 Mol. Biol. Evol. 35(9): 2240–2253 (2018) 0737-4038 http://hdl.handle.net/10261/217095 10.1093/molbev/msy125 1537-1719 http://dx.doi.org/10.13039/100000001 http://dx.doi.org/10.13039/501100001659 http://dx.doi.org/10.13039/501100001691 http://dx.doi.org/10.13039/501100000275 29924328 en Preprint http://dx.doi.org/10.1093/molbev/msy125 No open Oxford University Press
institution IBE ES
collection DSpace
country España
countrycode ES
component Bibliográfico
access En linea
databasecode dig-ibe-es
tag biblioteca
region Europa del Sur
libraryname Biblioteca del IBE España
language English
topic Homeobox genes
Development
Gene duplication
Homeobox genes
Development
Gene duplication
spellingShingle Homeobox genes
Development
Gene duplication
Homeobox genes
Development
Gene duplication
Leite, Daniel J.
Baudouin-Gonzalez, Luís
Iwasaki-Yokozawa, Sawa
Lozano Fernández, Jesús
Turetzek, Natascha
Akiyama-Oda, Yasuko
Prpic, Nikola-Michael
Pisani, Davide
Oda, Hiroki
Sharma, Prashant P.
McGregor, Alistair P.
Homeobox Gene Duplication and Divergence in Arachnids
description Homeobox genes are key toolkit genes that regulate the development of metazoans and changes in their regulation and copy number have contributed to the evolution of phenotypic diversity. We recently identified a whole genome duplication (WGD) event that occurred in an ancestor of spiders and scorpions (Arachnopulmonata), and that many homeobox genes, including two Hox clusters, appear to have been retained in arachnopulmonates. To better understand the consequences of this ancient WGD and the evolution of arachnid homeobox genes, we have characterized and compared the homeobox repertoires in a range of arachnids. We found that many families and clusters of these genes are duplicated in all studied arachnopulmonates (Parasteatoda tepidariorum, Pholcus phalangioides, Centruroides sculpturatus, and Mesobuthus martensii) compared with nonarachnopulmonate arachnids (Phalangium opilio, Neobisium carcinoides, Hesperochernes sp., and Ixodes scapularis). To assess divergence in the roles of homeobox ohnologs, we analyzed the expression of P. tepidariorum homeobox genes during embryogenesis and found pervasive changes in the level and timing of their expression. Furthermore, we compared the spatial expression of a subset of P. tepidariorum ohnologs with their single copy orthologs in P. opilio embryos. We found evidence for likely subfunctionlization and neofunctionalization of these genes in the spider. Overall our results show a high level of retention of homeobox genes in spiders and scorpions post-WGD, which is likely to have made a major contribution to their developmental evolution and diversification through pervasive subfunctionlization and neofunctionalization, and paralleling the outcomes of WGD in vertebrates.
author2 Leverhulme Trust
author_facet Leverhulme Trust
Leite, Daniel J.
Baudouin-Gonzalez, Luís
Iwasaki-Yokozawa, Sawa
Lozano Fernández, Jesús
Turetzek, Natascha
Akiyama-Oda, Yasuko
Prpic, Nikola-Michael
Pisani, Davide
Oda, Hiroki
Sharma, Prashant P.
McGregor, Alistair P.
format artículo
topic_facet Homeobox genes
Development
Gene duplication
author Leite, Daniel J.
Baudouin-Gonzalez, Luís
Iwasaki-Yokozawa, Sawa
Lozano Fernández, Jesús
Turetzek, Natascha
Akiyama-Oda, Yasuko
Prpic, Nikola-Michael
Pisani, Davide
Oda, Hiroki
Sharma, Prashant P.
McGregor, Alistair P.
author_sort Leite, Daniel J.
title Homeobox Gene Duplication and Divergence in Arachnids
title_short Homeobox Gene Duplication and Divergence in Arachnids
title_full Homeobox Gene Duplication and Divergence in Arachnids
title_fullStr Homeobox Gene Duplication and Divergence in Arachnids
title_full_unstemmed Homeobox Gene Duplication and Divergence in Arachnids
title_sort homeobox gene duplication and divergence in arachnids
publisher Oxford University Press
publishDate 2018-09
url http://hdl.handle.net/10261/217095
http://dx.doi.org/10.13039/100000001
http://dx.doi.org/10.13039/501100001659
http://dx.doi.org/10.13039/501100001691
http://dx.doi.org/10.13039/501100000275
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