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Open Access Research article

The Caenorhabditis globin gene family reveals extensive nematode-specific radiation and diversification

David Hoogewijs1, Sasha De Henau1, Sylvia Dewilde2, Luc Moens2, Marjolein Couvreur3, Gaetan Borgonie3, Serge N Vinogradov4, Scott W Roy5 and Jacques R Vanfleteren1*

Author Affiliations

1 Department of Biology and Center for Molecular Phylogeny and Evolution, Ghent University, B-9000 Ghent, Belgium

2 Department of Biomedical Sciences, University of Antwerp, B-2610 Antwerp, Belgium

3 Department of Biology, Nematology section, Ghent University, 9000 Ghent, Belgium

4 Department of Biochemistry and Molecular Biology, Wayne State University School of Medicine, Detroit, Michigan 48201, USA

5 National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20814, USA

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BMC Evolutionary Biology 2008, 8:279  doi:10.1186/1471-2148-8-279

Published: 9 October 2008

Abstract

Background

Globin isoforms with variant properties and functions have been found in the pseudocoel, body wall and cuticle of various nematode species and even in the eyespots of the insect-parasite Mermis nigrescens. In fact, much higher levels of complexity exist, as shown by recent whole genome analysis studies. In silico analysis of the genome of Caenorhabditis elegans revealed an unexpectedly high number of globin genes featuring a remarkable diversity in gene structure, amino acid sequence and expression profiles.

Results

In the present study we have analyzed whole genomic data from C. briggsae, C. remanei, Pristionchus pacificus and Brugia malayi and EST data from several other nematode species to study the evolutionary history of the nematode globin gene family. We find a high level of conservation of the C. elegans globin complement, with even distantly related nematodes harboring orthologs to many Caenorhabditis globins. Bayesian phylogenetic analysis resolves all nematode globins into two distinct globin classes. Analysis of the globin intron-exon structures suggests extensive loss of ancestral introns and gain of new positions in deep nematode ancestors, and mainly loss in the Caenorhabditis lineage. We also show that the Caenorhabditis globin genes are expressed in distinct, mostly non-overlapping, sets of cells and that they are all under strong purifying selection.

Conclusion

Our results enable reconstruction of the evolutionary history of the globin gene family in the nematode phylum. A duplication of an ancestral globin gene occurred before the divergence of the Platyhelminthes and the Nematoda and one of the duplicated genes radiated further in the nematode phylum before the split of the Spirurina and Rhabditina and was followed by further radiation in the lineage leading to Caenorhabditis. The resulting globin genes were subject to processes of subfunctionalization and diversification leading to cell-specific expression patterns. Strong purifying selection subsequently dampened further evolution and facilitated fixation of the duplicated genes in the genome.