Deciphering the origins of guanylate-binding proteins in mammals (Monotreme, Marsupials and Placentals).

Abstract

Background: Guanylate-binding proteins (GBPs) belong to the large guanosine triphosphatases (GTPases) family and have specialised in host defence in vivo against a broad spectrum of invading pathogens. This ancient evolutionary group of genes was first studied in humans and rodents, but its evolution remained largely unknown for nearly 20 years. In recent years, more studies have emerged deepening the knowledge of GBP evolution in specific mammalian groups: Primates, Tupaia, Muroids (Rodents), Bats and Lagomorphs.

Results: Here, we aimed to present a comprehensive analysis of mammals GBP evolution. Our phylogenetic analysis demonstrates that mammals' GBPs share a common ancestor and that each major mammalian group has evolved a specific GBP repertoire. Two Monotreme GBP groups, GBP8 and GBP9, cluster independently in the phylogenetic tree and do not share the synteny of the other mammalian GBP genes. The other two Monotreme GBP groups, GBP1/2/3/5 and GBP4/6/7, are at the basal position of the main mammalian groups. Marsupials have two GBP groups, Marsupial GBP1/2/3/5, basal to Placental GBP1/2/3/5, and Marsupial GBP4/6/7, basal to Placental GBP4/6/7. Marsupial GBP1/2/3/5 can be subdivided into three sub-groups, similarly to what is observed in the Placental GBPs, whereas Marsupial GBP4/6/7 underwent several duplication events across species. We also examined the GBP tissue expression pattern in Monodelphis domestica and found that GBPs are ubiquitously expressed in most tissues, with some differences. Noteworthy was the presence of GBP transcripts in late foetal and newborn opossum tissues.

Conclusions: The GBP genes revealed a distinct evolutionary pattern in each main mammalian group. Phylogenetic analysis shows that Monotremes and Marsupials have specific GBPs. Particularly intriguing is the presence of GBP8 and GBP9 only in Monotremes.