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PLoS One
2012 Jan 01;79:e44548. doi: 10.1371/journal.pone.0044548.
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Evolution of genes involved in gamete interaction: evidence for positive selection, duplications and losses in vertebrates.
Meslin C
,
Mugnier S
,
Callebaut I
,
Laurin M
,
Pascal G
,
Poupon A
,
Goudet G
,
Monget P
.
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Genes encoding proteins involved in sperm-egg interaction and fertilization exhibit a particularly fast evolution and may participate in prezygotic species isolation [1], [2]. Some of them (ZP3, ADAM1, ADAM2, ACR and CD9) have individually been shown to evolve under positive selection [3], [4], suggesting a role of positive Darwinian selection on sperm-egg interaction. However, the genes involved in this biological function have not been systematically and exhaustively studied with an evolutionary perspective, in particular across vertebrates with internal and external fertilization. Here we show that 33 genes among the 69 that have been experimentally shown to be involved in fertilization in at least one taxon in vertebrates are under positive selection. Moreover, we identified 17 pseudogenes and 39 genes that have at least one duplicate in one species. For 15 genes, we found neither positive selection, nor gene copies or pseudogenes. Genes of teleosts, especially genes involved in sperm-oolemma fusion, appear to be more frequently under positive selection than genes of birds and eutherians. In contrast, pseudogenization, gene loss and gene gain are more frequent in eutherians. Thus, each of the 19 studied vertebrate species exhibits a unique signature characterized by gene gain and loss, as well as position of amino acids under positive selection. Reflecting these clade-specific signatures, teleosts and eutherian mammals are recovered as clades in a parsimony analysis. Interestingly the same analysis places Xenopus apart from teleosts, with which it shares the primitive external fertilization, and locates it along with amniotes (which share internal fertilization), suggesting that external or internal environmental conditions of germ cell interaction may not be the unique factors that drive the evolution of fertilization genes. Our work should improve our understanding of the fertilization process and on the establishment of reproductive barriers, for example by offering new leads for experiments on genes identified as positively selected.
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22957080
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Figure 2. Rate of gene appearance, gene duplication, pseudogenization, loss and intensity of positive selection in Teleostei, Aves and Eutheria. a.Rate of events per million years (Myr) per lineage for the set of genes studied. This includes up to 69 genes, but in most cases, the number of relevant genes is lower because some types of events cannot happen in some taxa (losses or duplications cannot happen if a gene is primitively absent, and gains cannot occur in a clade if the gene appeared before the base of a given clade), and we have incorporated that factor into our calculations to obtain comparable rates across taxa. The geological age of lineages is used in the rate calculation through the phylogenetic diversity of the clades. b and c. Proportion of genes under positive selection in Teleostei, Aves and Eutheria for genes belonging to the third step, the sperm-oolemma fusion (B), and for all genes (C). Three types of confidence intervals are shown: 78%, 90% and 97% representing testing at 0.05, 0.01 and 0.001 probability thresholds, respectively. Statistically significant comparisons, for which confidence intervals do not overlap, are indicated.
Figure 3. 3D structures of N and C domain of ACE in platypus, Xenopus, chimpanzee and zebrafish.ACE structures have been modeled for four species based on human PDB structure (PDB: 1O8A) [36]. This enzyme is composed of two homolog N and C domains, each containing a catalytic site composed by two histidines in a conserved -HEXXH- zinc-binding motif [37] and a glutamate as the third ligand 24 residues downstream this motif [38]. These three binding sites are indicated in yellow, whereas amino acids under positive selection are in pink. ACE protein is expressed by sperm. Gene knockout experiments of ACE in mouse results in an impaired uterotubular sperm migration and a reduced ability to bind the zona pellucida of the egg [39], [40], [41].
Figure 1. Signature of evolution of genes involved in sperm-oocyte interaction in Vertebrates.Genes (names are indicated on the top) are classified into three main functional groups (from left to right): sperm-zona pellucida binding, acrosome reaction, and sperm-oolemma fusion. Species are indicated in the tree (left). Blue square: duplication; purple square: positive selection; pink square: duplication + positive selection. Black square: pseudogene; Black dot: no event. Black circle: no calculation of positive selection. White square: no gene found.
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