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MBE Advance Access published online on August 10, 2005
Molecular Biology and Evolution, doi:10.1093/molbev/msi236
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Published by Oxford University Press 2005.
Accepted August 3, 2005

Research Article

Subfunctionalization of Expression and Peptide Domains Following the Ancient Duplication of the Proopiomelanocortin Gene in Teleost Fishes

Flávio S. J. de Souza 1 *, Viviana F. Bumaschny 1 *, Malcolm J. Low 2, and Marcelo Rubinstein 3*

1 Instituto de Investigaciones en Ingeniería Genética y Biología Molecular, CONICET and Dept. Fisiología, Biología Molecular y Celular, FCEyN, Universidad de Buenos Aires, Argentina
2 Vollum Institute, Oregon Health & Science University, Portland, OR 97239, USA; Dept. Behavioral Neuroscience, Oregon Health & Science University, Portland, OR 97239, USA; Center for the Study of Weight Regulation and Associated Disorders, Oregon Health & Science University, Portland, OR 97239, USA
3 Instituto de Investigaciones en Ingeniería Genética y Biología Molecular, CONICET and Dept. Fisiología, Biología Molecular y Celular, FCEyN, Universidad de Buenos Aires, Argentina; Center for the Study of Weight Regulation and Associated Disorders, Oregon Health & Science University, Portland, OR 97239, USA; Centro de Estudios Científicos, Valdivia, Chile

* To whom correspondence should be addressed.
Marcelo Rubinstein, E-mail: mrubins{at}dna.uba.ar


  Abstract

The proopiomelanocortin gene (POMC) encodes several bioactive peptides including adrenocorticotropin hormone (ACTH), {alpha}-, {beta}- and {gamma}-MSH and the opioid peptide {beta}-endorphin, which play key roles in vertebrate physiology. In the human, mouse and chicken genomes there is only one POMC gene. By searching public genome projects, we have found that Tetraodon (Tetraodon nigroviridis), Fugu (Takifugu rubripes) and zebrafish (Danio rerio) possess two POMC genes, which we called POMC{alpha} and POMC{beta}, and we present phylogenetic and mapping evidence that these paralogue genes originated in the whole-genome duplication specific to the teleost lineage over 300 million years ago. In addition, we present evidence for two types of subfunction partitioning between the paralogues: First, in situ hybridization experiments indicate that the expression domains of the ancestral POMC gene have been subfunctionalized in Tetraodon, with POMC{alpha} expressed in the nucleus lateralis tuberis of the hypothalamus, as well as in the rostral pars distalis and pars intermedia of the pituitary, whereas POMC{beta} is expressed in the preoptic area of the brain and weakly in the pituitary pars intermedia. Second, POMC{beta} genes have a {beta}-endorphin segment that lacks the consensus opioid signal and seems to be under neutral evolution in tetraodontids, whereas POMC{alpha} genes possess well-conserved peptide regions. Thus, POMC paralogues have experienced subfunctionalization of both expression and peptide domains during teleost evolution. The study of regulatory regions of fish POMC genes might shed light on the mechanisms of enhancer partitioning between duplicate genes as well as the roles of POMC-derived peptides in fish physiology.

Keywords: POMC; teleosts; evolution; Tetraodon; beta-endorphin; subfunctionalization.

*These authors contributed equally to this work


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