Changes in the composition of the RNA virome mark evolutionary transitions in green plants.

Arcady Mushegian,Alexey Shipunov,Santiago F Elena

doi:10.1186/s12915-016-0288-8

Abstract

BackgroundThe known plant viruses mostly infect angiosperm hosts and have RNA or small DNA genomes. The only other lineage of green plants with a relatively well-studied virome, unicellular chlorophyte algae, is mostly infected by viruses with large DNA genomes. Thus RNA viruses and small DNA viruses seem to completely displace large DNA virus genomes in late branching angiosperms. To understand better the expansion of RNA viruses in the taxonomic span between algae and angiosperms, we analyzed the transcriptomes of 66 non-angiosperm plants characterized by the 1000 Plants Genomes Project.ResultsWe found homologs of virus RNA-dependent RNA polymerases in 28 non-angiosperm plant species, including algae, mosses, liverworts (Marchantiophyta), hornworts (Anthocerotophyta), lycophytes, a horsetail Equisetum, and gymnosperms. Polymerase genes in algae were most closely related to homologs from double-stranded RNA viruses leading latent or persistent lifestyles. Land plants, in addition, contained polymerases close to the homologs from single-stranded RNA viruses of angiosperms, capable of productive infection and systemic spread. For several polymerases, a cognate capsid protein was found in the same library. Another virus hallmark gene family, encoding the 30 K movement proteins, was found in lycophytes and monilophytes but not in mosses or algae.ConclusionsThe broadened repertoire of RNA viruses suggests that colonization of land and growth in anatomical complexity in land plants coincided with the acquisition of novel sets of viruses with different strategies of infection and reproduction.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-016-0288-8) contains supplementary material, which is available to authorized users.

Highlights

The known plant viruses mostly infect angiosperm hosts and have RNA or small DNA genomes
Viral RNA-dependent RNA polymerases are pervasive in the transcriptomes of non-angiosperm plants Viral RNA-dependent RNA polymerases (RdRP; EC 2.7.7.48) are a distinct group within the superfamily of nucleotidyltransferases with the catalytic right-hand palm domain
Viral RdRPs are not related to the cellular RdRPs involved in RNA interference, which possess a distinct configuration of conserved sequence elements and adopt a different double-psi barrel fold [23]

Summary

Introduction

The known plant viruses mostly infect angiosperm hosts and have RNA or small DNA genomes. Viruses and virus-like replicons in non-agricultural habitats were in the meantime being discovered serendipitously, for example when symptoms suggestive of an infection were observed in nature, but it was only recently that technological developments – large-scale sequencing of cloned DNA at first, and next-generation sequencing in the last decade – allowed virologists to screen more systematically for the presence of known and novel viruses in plant populations of choice [1]. These efforts have provided us with a relatively good understanding of the general landscape of genomic diversity in viruses of angiosperm plants. Sequence similarity analysis and phylogenetic studies have established profound, ancient relationships between each of these virus groups with viruses that infect fungi and animals; more recently, such studies have drawn the evolutionary links between these virus lineages and viruses infecting unicellular eukaryotes, bacteria, and archaea [2]

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