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Explosive Lineage-Specific Expansion of the Orphan Nuclear Receptor HNF4 in Nematodes

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Abstract

The nuclear receptor superfamily expanded in at least two episodes: one early in metazoan evolution, the second within the vertebrate lineage. An exception to this pattern is the genome of the nematode Caenorhabditis elegans, which encodes more than 270 nuclear receptors, most of them highly divergent. We generated 128 cDNA sequences for 76 C. elegans nuclear receptors, confirming that these are active genes. Among these numerous receptors are 13 orthologues of nuclear receptors found in arthropods and/or vertebrates. We show that the supplementary nuclear receptors (supnrs) originated from an explosive burst of duplications of a unique orphan receptor, HNF4. This origin has specific implications for the role of ligand binding in the function and evolution of the nematode supplementary nuclear receptors. Moreover, the supplementary nuclear receptors include a group of very rapidly evolving genes found primarily on chromosome V. We propose a model of lineage-specific duplications from a chromosome on which duplication and substitution rates are highly increased. Our results provide a framework to study nuclear receptors in nematodes, as well as to consider the functional and evolutionary consequences of lineage-specific duplications.

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Acknowledgments

We thank Nicolas Galtier for the use of the program Maseclean2 and Satoshi Oota for the use of the program NJML+ (version 0.8.3.2). We thank Stéphane Guindon for help with the use of PhyML. We thank Barton Slatko, Laurie Mazzola, and Jennifer Ware for DNA sequencing. C.V.M. and C.R.G. gratefully acknowledge Don Comb for support of their contributions to this work. Work by M.R.R. and V.L. was supported by the CNRS “Bioinformatique” program. We thank François Bonneton, Laurent Duret, Fédéric Flamant, Hector Escriva Garcia, Laurent Ségalat, and Michael Schubert for critical reading of the manuscript. We also gratefully acknowledge the Nematode Genome Sequencing Consortium for providing public access to a preliminary assembly of the Caenorhabditis briggsae genome sequence.

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Correspondence to Vincent Laudet.

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Robinson-Rechavi, M., Maina, C.V., Gissendanner, C.R. et al. Explosive Lineage-Specific Expansion of the Orphan Nuclear Receptor HNF4 in Nematodes. J Mol Evol 60, 577–586 (2005). https://doi.org/10.1007/s00239-004-0175-8

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