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Open Access Research article

Expansion and functional diversification of a leucyl aminopeptidase family that encodes the major protein constituents of Drosophila sperm

Steve Dorus1, Elaine C Wilkin1 and Timothy L Karr2*

Author Affiliations

1 Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UK

2 Centers for Evolutionary Medicine and Informatics and Infectious Diseases and Vaccinology, Biodesign Institute, Arizona State University, Tempe, AZ 85287-5001, USA

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BMC Genomics 2011, 12:177  doi:10.1186/1471-2164-12-177

Published: 5 April 2011

Abstract

Background

The evolutionary diversification of gene families through gene creation (and loss) is a dynamic process believed to be critical to the evolution of functional novelty. Previous identification of a closely related family of eight annotated metalloprotease genes of the M17 Merops family in the Drosophila sperm proteome (termed,

    S
perm-
    L
eucyl
    A
mino
    P
eptidases, S-LAPs 1-8) led us to hypothesize that this gene family may have experienced such a diversification during insect evolution.

Results

To assess putative functional activities of S-LAPs, we (i) demonstrated that all S-LAPs are specifically expressed in the testis, (ii) confirmed their presence in sperm by two-dimensional gel electrophoresis and mass spectrometry, (iii) determined that they represent a major portion of the total protein in sperm and (iv) identified aminopeptidase enzymatic activity in sperm extracts using LAP-specific substrates. Functionally significant divergence at the canonical M17 active site indicates that the largest phylogenetic group of S-LAPs lost catalytic activity and likely acquired novel, as yet undetermined, functions in sperm prior to the expansion of the gene family.

Conclusions

Comparative genomic and phylogenetic analyses revealed the dramatic expansion of the S-LAP gene family during Drosophila evolution and copy number heterogeneity in the genomes of related insects. This finding, in conjunction with the loss of catalytic activity and potential neofunctionalization amongst some family members, extends empirical support for pervasive "revolving door" turnover in the evolution of reproductive gene family composition and function.

Keywords:
sperm; proteomics; gene duplication; gene family; protease; spermatogenesis; testis