Studies On The Origin And Evolution Of Plant Retroviruses

Retroviruses cause a variety of diseases in animals,such as AIDS and cancer.Retroviruses and Metaviruses(Ty3/ Gypsy retrotransposons)are very similar in structure and evolutionary relationships.However,there are two significant structural differences between retroviruses and macroviruses: 1)Retroviruses encode an env-like gene with predicted transmembrane domains;2)The pol gene of some retroviruses elements encode a dual ribonuclease H domain.Unique among the Ty3/Gypsy retrotransposons,some Athila/Tat elements encode an env-like gene with predicted transmembrane domains,and the pol gene of some Athila/Tat elements encode a dual ribonuclease H domain.Both features appear to arise independently in the Athila/Tat retrotransposons and retroviruses.The Athila/Tat retrotransposons have sometimes been referred to as “plant retroviruses”.We used a similarity search and phylogenetic analysis combined approach to identify the Athila/Tat retrotransposons in a total of 106 representative plant species.We found the Athila/Tat retrotransposons are present in all the land plants screened in this study.However,we did not identify any Athila/Tat retrotransposon in non-land plants.The Athila/Tat retrotransposon lineage comprises of a significant component of land plant retrotransposons,and there are up to 100,000 copies in some plant genomes.To explore the potential source of land plant Athila/Tat retrotransposons,we used the similarity search and phylogenetic analysis combined approach to identify retrotransposons that are closely related to land plant Athila/Tat retrotransposons in the currently available genomes of eukaryotes outside plants(a total of 2,095 genomes).The phylogenetic analyses also show that land plant Athia/Tat retrotransposons are more closely related to retrotransposons of fungi from the phylum Mucoromycota(two species of Glomeromycotina and two species of Mortierellomycotina).Members in Glomeromycotina are mutualistically associated with roots of vascular plants,forming arbuscular mycorrhizas.Taken together,all these lines of evidence suggest plants might have acquired the Athila/Tat retrotransposons horizontally from fungi during the conquest of terrestrial environments.The Athila/Tat element appears to be active in plant and fungal genomes for millions of years.To explore the diversity and evolution of the Athila/Tat retrotransposon structures,we analyzed the domain architectures of representative complete or nearly complete Athila/Tat elements from land plants and fungi.We found the Athila/Tat elements from fungi do not encode a dual RNH domain or an env-like gene,representing the original Athila/Tat structure.In contrast,several independent land plant Athila/Tat lineages encode a RNH domains,and the positions of a RNH vary among different Athila/Tat lineages,advocating that a RNH in land plant.Only one lineage of the plant Athila/Tat element acquires a capsule-like protein,forming what is called a plant retrovirus.The Athila/Tat retrotransposons have multiple independent origins.The Athila/Tat retrotransposons frequently acquired and lost novel domains and evolved into diverse forms after horizontal transfer from fungi to land plants.It is widely believed that fungi played an important role in the adaptation of early land plants to their terrestrial environment,and this study provides new molecular evidence for the early close relationship between fungi and plants and the ancient land plant-fungus interactions might shape the evolution of genome complexity of both partners.Our results provide novel insights into the origin and evolution of retrotransposons in land plants as well as the influence of ancient plant-fungus symbiosis on the evolution of plant genome complexity.