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PLoS Genet. 2014 Oct 23;10(10):e1004698. doi: 10.1371/journal.pgen.1004698. eCollection 2014 Oct.

Ancient expansion of the hox cluster in lepidoptera generated four homeobox genes implicated in extra-embryonic tissue formation.

Author information

1
Department of Zoology, University of Oxford, Oxford, United Kingdom.
2
Evolutionary Developmental Biology Research Group, Faculty of Health and Life Sciences, Department of Biological and Medical Sciences, Oxford Brookes University, Headington, Oxford, United Kingdom.
3
MRC National Institute for Medical Research, Mill Hill, London, United Kingdom.
4
NERC Centre for Ecology and Hydrology, Wallingford, Oxfordshire, United Kingdom.

Abstract

Gene duplications within the conserved Hox cluster are rare in animal evolution, but in Lepidoptera an array of divergent Hox-related genes (Shx genes) has been reported between pb and zen. Here, we use genome sequencing of five lepidopteran species (Polygonia c-album, Pararge aegeria, Callimorpha dominula, Cameraria ohridella, Hepialus sylvina) plus a caddisfly outgroup (Glyphotaelius pellucidus) to trace the evolution of the lepidopteran Shx genes. We demonstrate that Shx genes originated by tandem duplication of zen early in the evolution of large clade Ditrysia; Shx are not found in a caddisfly and a member of the basally diverging Hepialidae (swift moths). Four distinct Shx genes were generated early in ditrysian evolution, and were stably retained in all descendent Lepidoptera except the silkmoth which has additional duplications. Despite extensive sequence divergence, molecular modelling indicates that all four Shx genes have the potential to encode stable homeodomains. The four Shx genes have distinct spatiotemporal expression patterns in early development of the Speckled Wood butterfly (Pararge aegeria), with ShxC demarcating the future sites of extraembryonic tissue formation via strikingly localised maternal RNA in the oocyte. All four genes are also expressed in presumptive serosal cells, prior to the onset of zen expression. Lepidopteran Shx genes represent an unusual example of Hox cluster expansion and integration of novel genes into ancient developmental regulatory networks.

PMID:
25340822
PMCID:
PMC4207634
DOI:
10.1371/journal.pgen.1004698
[Indexed for MEDLINE]
Free PMC Article

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