Ancient expansion of the Hox cluster in Lepidoptera generated four homeobox genes implicated in extra-embryonic tissue formation

Ferguson, Laura; Marletaz, Ferdinand; Carter, Jean-Michel; Taylor, William R.; Gibbs, Melanie ORCID: https://orcid.org/0000-0002-4091-9789; Breuker, Casper J.; Holland, Peter W.H.. 2014 Ancient expansion of the Hox cluster in Lepidoptera generated four homeobox genes implicated in extra-embryonic tissue formation. PLoS Genetics, 10 (10), e1004698. 12, pp. https://doi.org/10.1371/journal.pgen.1004698

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Abstract/Summary

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.

Item Type:	Publication - Article
Digital Object Identifier (DOI):	https://doi.org/10.1371/journal.pgen.1004698
UKCEH and CEH Sections/Science Areas:	Pywell
ISSN:	1553-7390
Additional Information. Not used in RCUK Gateway to Research.:	Open Access paper - Official URL link provides full text
NORA Subject Terms:	Ecology and Environment Zoology
Date made live:	27 Oct 2014 14:22 +0 (UTC)
URI:	https://nora.nerc.ac.uk/id/eprint/508421

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