Evolutionary significance and diversification of the phosphoglucose isomerase genes in vertebrates

Mbaye Tine

Phosphoglucose isomerase (PGI) genes are important multifunctional proteins whose evolution has, until now, not been well elucidated because of the limited number of completely sequenced genomes. Although the multifunctionality of this gene family has been considered as an original and innate characteristic, PGI genes may have acquired novel functions through changes in coding sequences and exon/intron structure, which are known to lead to functional divergence after gene duplication. A whole-genome comparative approach was used to estimate the rates of molecular evolution of this protein family. The results confirm the presence of two isoforms in teleost fishes and only one variant in all other vertebrates. Phylogenetic reconstructions grouped the PGI genes into five main groups: lungfishes/coelacanth/cartilaginous fishes, teleost fishes, amphibians, reptiles/birds and mammals, with the teleost group being subdivided into two subclades comprising PGI1 and PGI2. This PGI partitioning into groups is consistent with the synteny and molecular evolution results based on the estimation of the ratios of nonsynonymous to synonymous changes (Ka/Ks) and divergence rates between both PGI paralogs and orthologs. Teleost PGI2 shares more similarity with the variant found in all other vertebrates, suggesting that it has less evolved than PGI1 relative to the PGI of common vertebrate ancestor. The diversification of PGI genes into PGI1 and PGI2 is consistent with a teleost-specific duplication before the radiation of this lineage, and after its split from the other infraclasses of ray-finned fishes. The low average Ka/Ks ratios within teleost and mammalian lineages suggest that both PGI1 and PGI2 are functionally constrained by purifying selection and may, therefore, have the same functions. By contrast, the high average Ka/Ks ratios and divergence rates within reptiles and birds indicate that PGI may be involved in different functions. The synteny analyses show that the genomic region harbouring PGI genes has independently undergone genomic rearrangements in mammals versus the reptile/bird lineage in particular, which may have contributed to the actual functional diversification of this gene family.