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Open Access Research article

The genome of Romanomermis culicivorax: revealing fundamental changes in the core developmental genetic toolkit in Nematoda

Philipp H Schiffer1*, Michael Kroiher1, Christopher Kraus1, Georgios D Koutsovoulos2, Sujai Kumar2, Julia I R Camps1, Ndifon A Nsah1, Dominik Stappert3, Krystalynne Morris4, Peter Heger1, Janine Altmüller5, Peter Frommolt5, Peter Nürnberg5, W Kelley Thomas4, Mark L Blaxter2 and Einhard Schierenberg1

Author Affiliations

1 Zoologisches Institut, Universität zu Köln, Cologne, NRW, Germany

2 Institute of Evolutionary Biology, School of Biological Sciences, The University of Edinburgh, Edinburgh, Scotland, UK

3 Institute für Entwicklungsbiologie, Universität zu Köln, Cologne, NRW, Germany

4 Hubbard Center for Genome Studies, University of New Hampshire, Durham, NH, USA

5 Cologne Center for Genomics, Universität zu Köln, Cologne, NRW, Germany

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BMC Genomics 2013, 14:923  doi:10.1186/1471-2164-14-923

Published: 27 December 2013

Abstract

Background

The genetics of development in the nematode Caenorhabditis elegans has been described in exquisite detail. The phylum Nematoda has two classes: Chromadorea (which includes C. elegans) and the Enoplea. While the development of many chromadorean species resembles closely that of C. elegans, enoplean nematodes show markedly different patterns of early cell division and cell fate assignment. Embryogenesis of the enoplean Romanomermis culicivorax has been studied in detail, but the genetic circuitry underpinning development in this species has not been explored.

Results

We generated a draft genome for R. culicivorax and compared its gene content with that of C. elegans, a second enoplean, the vertebrate parasite Trichinella spiralis, and a representative arthropod, Tribolium castaneum. This comparison revealed that R. culicivorax has retained components of the conserved ecdysozoan developmental gene toolkit lost in C. elegans. T. spiralis has independently lost even more of this toolkit than has C. elegans. However, the C. elegans toolkit is not simply depauperate, as many novel genes essential for embryogenesis in C. elegans are not found in, or have only extremely divergent homologues in R. culicivorax and T. spiralis. Our data imply fundamental differences in the genetic programmes not only for early cell specification but also others such as vulva formation and sex determination.

Conclusions

Despite the apparent morphological conservatism, major differences in the molecular logic of development have evolved within the phylum Nematoda. R. culicivorax serves as a tractable system to contrast C. elegans and understand how divergent genomic and thus regulatory backgrounds nevertheless generate a conserved phenotype. The R. culicivorax draft genome will promote use of this species as a research model.

Keywords:
Nematode; Genome; Evolution; Development; Caenorhabditis; Mermithida; Romanomermis