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MBE Advance Access first published online on November 3, 2004
This version published online on November 8, 2004
Molecular Biology and Evolution, doi:10.1093/molbev/msi037
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved
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Accepted October 26, 2004

Research Article

Positive Selection in the Carbohydrate Recognition Domains of Sea Urchin Sperm Receptor for Egg Jelly (suREJ) Proteins

Silvia A. Mah 1, Willie J. Swanson 2, and Victor D. Vacquier 1*

1 Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, California 92093-0202
2 Department of Genome Sciences, University of Washington, Seattle, Washington 98195-7730

* To whom correspondence should be addressed.
Victor D. Vacquier, E-mail: vvacquier{at}ucsd.edu


  Abstract

A wealth of evidence shows that protein-carbohydrate recognition mediates the steps of gamete interaction during fertilization. Carbohydrate recognition domains (CRD) comprise a large family of ancient protein modules of approximately 120 amino acids, having the same protein fold, that bind terminal sugar residues on glycoproteins and polysaccharides. Sea urchin sperm express three suREJ (sea urchin receptor for egg jelly) proteins on their plasma membranes. suREJ1 has two CRDs, whereas suREJ2 and suREJ3 both have one CRD. suREJ1 binds the fucose sulfate polymer (FSP) of egg jelly to induce the sperm acrosome reaction. The structure of FSP is species-specific, therefore the suREJ1 CRDs could encode molecular recognition between sperm and egg underlying the species-specific induction of the acrosome reaction. The functions of suREJ2 and suREJ3 have not been explored, but suREJ3 is exclusively localized on the plasma membrane over the sperm acrosomal vesicle and is physically associated with sea urchin polycystin-2, a known cation channel. An evolutionary analysis of these four CRDs was performed for six sea urchin species. Phylogenetic analysis shows that these CRDs were already differentiated in the common ancestor of these six sea urchins. The CRD phylogeny agrees with previous work on these species based on one nuclear gene and several mitochondrial genes. Maximum likelihood shows that positive selection acts on these four CRDs. Threading the suREJ CRDs onto the prototypic CRD crystal structure shows that many of the sites under positive selection are on extended loops, which are involved in saccharide binding. This is the first demonstration of positive selection in CRDs and is another example of positive selection acting on the evolution of gamete recognition proteins.

Keywords: positive selection; fertilization; acrosome reaction; sperm lectins; sperm receptors; C-type lectins; maximum likelihood; sexual antagonism.
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