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Saltatory Evolution of the Ectodermal Neural Cortex Gene Family at the Vertebrate Origin

Feiner, Nathalie LU ; Murakami, Yasunori; Breithut, Lisa; Mazan, Sylvie; Meyer, Axel and Kuraku, Shigehiro (2013) In Genome Biology and Evolution 5(8). p.1485-1502
Abstract
The ectodermal neural cortex (ENC) gene family, whose members are implicated in neurogenesis, is part of the kelch repeat superfamily. To date, ENC genes have been identified only in osteichthyans, although other kelch repeat-containing genes are prevalent throughout bilaterians. The lack of elaborate molecular phylogenetic analysis with exhaustive taxon sampling has obscured the possible link of the establishment of this gene family with vertebrate novelties. In this study, we identified ENC homologs in diverse vertebrates by means of databasemining and polymerase chain reaction screens. Our analysis revealed that the ENC3 ortholog was lost in the basal eutherian lineage through single-gene deletion and that the triplication between ENC1,... (More)
The ectodermal neural cortex (ENC) gene family, whose members are implicated in neurogenesis, is part of the kelch repeat superfamily. To date, ENC genes have been identified only in osteichthyans, although other kelch repeat-containing genes are prevalent throughout bilaterians. The lack of elaborate molecular phylogenetic analysis with exhaustive taxon sampling has obscured the possible link of the establishment of this gene family with vertebrate novelties. In this study, we identified ENC homologs in diverse vertebrates by means of databasemining and polymerase chain reaction screens. Our analysis revealed that the ENC3 ortholog was lost in the basal eutherian lineage through single-gene deletion and that the triplication between ENC1, -2, and -3 occurred early in vertebrate evolution. Including our original data on the catshark and the zebrafish, our comparison revealed high conservation of the
pleiotropic expression pattern of ENC1 and shuffling of expression domains between ENC1, -2, and -3. Compared withmany other gene families including developmental key regulators, the ENC gene family is unique in that conventional molecular phylogenetic inference could identifynoobvious invertebrateortholog. This suggests a composite nature of the vertebrate-specificgene repertoire, consistingnot onlyofdenovogenes introducedat thevertebrateorigin but alsoof long-standinggenes withnoapparent invertebrate
orthologs. Some of the latter, including the ENC gene family, may be too rapidly evolving to provide sufficient phylogenetic signals marking orthology to their invertebrate counterparts. Such gene families that experienced saltatory evolution likely remain to be explored and might also have contributed to phenotypic evolution of vertebrates. (Less)
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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
vertebrate novelty, saltation, gene loss, conserved synteny, whole genome duplication
in
Genome Biology and Evolution
volume
5
issue
8
pages
1485 - 1502
publisher
Oxford University Press
external identifiers
  • scopus:84891641374
ISSN
1759-6653
DOI
10.1093/gbe/evt104
language
English
LU publication?
yes
id
c716c559-8439-4747-b6fc-26a7d82bf5fb
date added to LUP
2018-05-22 21:42:19
date last changed
2018-07-10 11:36:37
@article{c716c559-8439-4747-b6fc-26a7d82bf5fb,
  abstract     = {The ectodermal neural cortex (ENC) gene family, whose members are implicated in neurogenesis, is part of the kelch repeat superfamily. To date, ENC genes have been identified only in osteichthyans, although other kelch repeat-containing genes are prevalent throughout bilaterians. The lack of elaborate molecular phylogenetic analysis with exhaustive taxon sampling has obscured the possible link of the establishment of this gene family with vertebrate novelties. In this study, we identified ENC homologs in diverse vertebrates by means of databasemining and polymerase chain reaction screens. Our analysis revealed that the ENC3 ortholog was lost in the basal eutherian lineage through single-gene deletion and that the triplication between ENC1, -2, and -3 occurred early in vertebrate evolution. Including our original data on the catshark and the zebrafish, our comparison revealed high conservation of the<br/>pleiotropic expression pattern of ENC1 and shuffling of expression domains between ENC1, -2, and -3. Compared withmany other gene families including developmental key regulators, the ENC gene family is unique in that conventional molecular phylogenetic inference could identifynoobvious invertebrateortholog. This suggests a composite nature of the vertebrate-specificgene repertoire, consistingnot onlyofdenovogenes introducedat thevertebrateorigin but alsoof long-standinggenes withnoapparent invertebrate<br/>orthologs. Some of the latter, including the ENC gene family, may be too rapidly evolving to provide sufficient phylogenetic signals marking orthology to their invertebrate counterparts. Such gene families that experienced saltatory evolution likely remain to be explored and might also have contributed to phenotypic evolution of vertebrates.},
  author       = {Feiner, Nathalie and Murakami, Yasunori and Breithut, Lisa and Mazan, Sylvie and Meyer, Axel and Kuraku, Shigehiro},
  issn         = {1759-6653},
  keyword      = {vertebrate novelty,saltation,gene loss,conserved synteny,whole genome duplication},
  language     = {eng},
  month        = {07},
  number       = {8},
  pages        = {1485--1502},
  publisher    = {Oxford University Press},
  series       = {Genome Biology and Evolution},
  title        = {Saltatory Evolution of the Ectodermal Neural Cortex Gene Family at the Vertebrate Origin},
  url          = {http://dx.doi.org/10.1093/gbe/evt104},
  volume       = {5},
  year         = {2013},
}