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Most vertebrates have three paralogous genes with identical intron-exon structures and a high degree of sequence identity that encode mitochondrial adenine nucleotide translocase ( Ant ) proteins,  Ant1  ( Slc25a4 ),  Ant2  ( Slc25a5 ) and  Ant3  ( Slc25a6 ). Recently, we and others identified a fourth mammalian  Ant  paralog,  Ant4  ( Slc25a31 ), with a distinct intron-exon structure and a lower degree of sequence identity.  Ant4  was expressed selectively in testis and sperm in adult mammals and was indeed essential for mouse spermatogenesis, but it was absent in birds, fish and frogs. Since  Ant2  is X-linked in mammalian genomes, we hypothesized that the autosomal  Ant4  gene may compensate for the loss of  Ant2  gene expression during male meiosis in mammals. Here we report that the  Ant4  ortholog is conserved in green anole lizard ( Anolis carolinensis ) and demonstrate that it is expressed in the anole testis. Further, a degenerate DNA fragment of putative  Ant4  gene was identified in syntenic regions of avian genomes, indicating that  Ant4  was present in the common amniote ancestor. Phylogenetic analyses suggest an even more ancient origin of the  Ant4  gene. Although anole lizards are presumed male (XY) heterogametic, like mammals, copy numbers of the  Ant2  as well as its neighboring gene were similar between male and female anole genomes, indicating that the anole  Ant2  gene is either autosomal or located in the pseudoautosomal region of the sex chromosomes, in contrast to the case to mammals. These results imply the conservation of  Ant4  is not likely simply driven by the sex chromosomal localization of the  Ant2  gene and its subsequent inactivation during male meiosis. Taken together with the fact that Ant4 protein has a uniquely conserved structure when compared to other somatic Ant1, 2 and 3, there may be a specific advantage for mammals and lizards to express  Ant4  in their male germ cells.

Evolutionary Genomics Implies a Specific Function of Ant4 in Mammalian and Anole Lizard Male Germ Cells