Bindin from a sea star

Abstract

The genetic basis for the evolution of development includes genes that encode proteins expressed on the surfaces of sperm and eggs. Previous studies of the sperm acrosomal protein bindin have helped to characterize the adaptive evolution of gamete compatibility and speciation in sea urchins. The absence of evidence for bindin expression in taxa other than the Echinoidea has limited such studies to sea urchins, and led to the suggestion that bindin might be a sea urchin-specific molecule. Here we characterize the gene that encodes bindin in a broadcast-spawning asterinid sea star (Patiria miniata). We describe the sequence and domain structure of a full-length bindin cDNA and its single intron. In comparison to sea urchins, P. miniata bindin is larger but the two molecules share several general features of their domain structure and some sequence features of two domains. Our results extend the known evolutionary history of bindin from the Mesozoic (among the crown group sea urchins) into the early Paleozoic (and the common ancestor of eleutherozoans), and present new opportunities for understanding the role of bindin molecular evolution in sexual selection, life history evolution, and speciation among sea stars.

Structure and evolution of the sea star egg receptor for sperm bindin

“…New studies of P. miniata bindin show that positive selection leads to the evolution of divergent alleles in northern and southern populations, highly significant bindin population differentiation and quantitative differences in sperm–egg compatibility related to bindin genotypic differences (Patiño et al . ; Sunday & Hart ; J. Sunday, unpublished data). In contrast, my preliminary survey of a small number of complete EBR1 coding sequences did not uncover evidence of significant differentiation between these populations at most EBR1 domains, and the two populations share some divergent alleles for at least two positively selected parts of the EBR1 coding sequence, including a plausible protein‐recognition domain (EGF) and one copy of the repetitive domain structure that is associated with the evolution of species specificity of sperm binding in sea urchins (EBR repeats; Kamei & Glabe ).…”

“…First, this similarity of protein domains is unlike the near‐complete protein domain divergence between sea urchin and sea star bindin (Patiño et al . ), which differ in coding sequence length and predicted protein size and in repetitive domain organization; the two taxonomic classes share just one conserved domain (a core region of about 50 codons), but even the location of that core in the complete coding sequence is not conserved (in the middle of the coding sequence between two highly variable domains in sea urchins; at the 3′ end of the coding sequence in sea stars). One interpretation of the difference between receptor and ligand protein domain conservation is that the specificity of their interaction (and of sperm–egg compatibility) is not determined by the protein domain organization of EBR1 (because the two taxonomic classes share similar structural features but are reproductively incompatible), but might depend on the protein domain organization of bindin and on specific amino acid substitutions within and among individual protein domains for both bindin and EBR1 (the latter possibly dependent on its glycosylation pattern).…”

Selection in the Rapid Evolution of Gamete Recognition Proteins in Marine Invertebrates

“…The sf-bindin sequence is known for one starfish species (Patiño et al 2009). The conserved features between su-and sf-bindins include: placement of cysteine residues in a long prepro region, a furin cleavage site between the prepro and mature sequences, repeating sequence elements, and the B18 fusagenic peptide that differs from sea urchin by one residue.…”

Rates of sea urchin bindin evolution

“…Among the sea urchin species that have been studied to date, the length of mature bindin ranges from 193-418 amino acids (Zigler and Lessios 2003a). The single sea star in which bindin has been characterized was found to contain 793 amino acids (Patino et al 2009). In both sea urchins and sea stars, there is a single intron separating two exons.…”

“…Eighteen amino acids in this conserved region, thought to be involved in membrane fusion (Rocha et al 2008), have not changed since the extant orders of Echinoidea split from each other, 250 million years ago (mya). Only one amino acid in this region has changed between sea stars and sea urchins in the 500 million years (my) that the two echinoderm classes have been evolving independently (Patino et al 2009;Vacquier and Swanson 2011). The reputation of bindin as a fastevolving protein is owed to two regions flanking the conserved core, which in some genera have accumulated many point mutations and insertionsdeletions.…”