On the alleged origin of geminiviruses from extrachromosomal DNAs of phytoplasmas

Federica Saccardo,Sabrina Palmano,Emanuele Cettul,Giuseppe Firrao,Emanuela Noris

doi:10.1186/1471-2148-11-185

Abstract

BackgroundSeveral 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.ResultsHere 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.ConclusionThe 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.

Highlights

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 DNA plant viruses
DNA/Protein sequence sources and analysis The sequence data used in this work relative to 16S rDNA and single stranded DNA binding (SSB) proteins of various bacteria, plasmid replication protein, phytoplasmal EcDNAs, virus capsid and replication associated proteins, as well as environmental DNA were retrieved from the EMBL database and the community cyberinfrastructure for advanced marine microbial ecology research and analysis (CAMERA, http://camera. calit2.net)
While in the most recently discovered type of EcDNAs replication is initiated by a DNA primase encoded by dnaG, type I and type II EcDNAs replicate through an rolling circle replication (RCR) mechanism assisted by an EcDNA encoded replication associate protein

Summary

Introduction

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. Geminiviruses differ from most other plant viruses in the fact that they are single-stranded DNA (ssDNA) viruses that multiply through rolling circle replication (RCR) They constitute one of the three recognized groups of episomal replicons that use RCR, the other being circular ssDNA bacteriophages, and plasmids of bacteria or archaea [1]. The conservation of motif signatures and of the spacing between them led to the conclusion that they constitute a distinct superfamily. On this basis Koonin and Ilyina [2] advanced the

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