On the alleged origin of geminiviruses from extrachromosomal DNAs of phytoplasmas

Background: Several phytoplasmas, wall-less phloem limited plant pathogenic bacteria, have been shown to contain extrachromosomal DNA (EcDNA) molecules encoding a replication associated protein (Rep) similar to that of geminiviruses, a major group of single stranded (ss) DNA plant viruses. On the basis of that observation and of structural similarities between the capsid proteins of geminiviruses and the Satellite tobacco necrosis virus, it has been recently proposed that geminiviruses evolved from phytoplasmal EcDNAs by acquiring a capsid protein coding gene from a co-invading plant RNA virus. Results: Here we show that this hypothesis has to be rejected because (i) the EcDNA encoded Rep is not of phytoplasmal origin but has been acquired by phytoplasmas through horizontal transfer from a geminivirus or its ancestor; and (ii) the evolution of geminivirus capsid protein in land plants implies missing links, while the analysis of metagenomic data suggests an alternative scenario implying a more ancient evolution in marine environments. Conclusion: The hypothesis of geminiviruses evolving in plants from DNA molecules of phytoplasma origin contrasts with other findings. An alternative scenario concerning the origin and spread of Rep coding phytoplasmal EcDNA is presented and its implications on the epidemiology of phytoplasmas are discussed.