Evolutionary genomics of mycovirus-related dsRNA viruses reveals cross-family horizontal gene transfer and evolution of diverse viral lineages

Abstract

BackgroundDouble-stranded (ds) RNA fungal viruses are typically isometric single-shelled particles that are classified into three families, Totiviridae, Partitiviridae and Chrysoviridae, the members of which possess monopartite, bipartite and quadripartite genomes, respectively. Recent findings revealed that mycovirus-related dsRNA viruses are more diverse than previously recognized. Although an increasing number of viral complete genomic sequences have become available, the evolution of these diverse dsRNA viruses remains to be clarified. This is particularly so since there is little evidence for horizontal gene transfer (HGT) among dsRNA viruses.ResultsIn this study, we report the molecular properties of two novel dsRNA mycoviruses that were isolated from a field strain of Sclerotinia sclerotiorum, Sunf-M: one is a large monopartite virus representing a distinct evolutionary lineage of dsRNA viruses; the other is a new member of the family Partitiviridae. Comprehensive phylogenetic analysis and genome comparison revealed that there are at least ten monopartite, three bipartite, one tripartite and three quadripartite lineages in the known dsRNA mycoviruses and that the multipartite lineages have possibly evolved from different monopartite dsRNA viruses. Moreover, we found that homologs of the S7 Domain, characteristic of members of the genus phytoreovirus in family Reoviridae are widely distributed in diverse dsRNA viral lineages, including chrysoviruses, endornaviruses and some unclassified dsRNA mycoviruses. We further provided evidence that multiple HGT events may have occurred among these dsRNA viruses from different families.ConclusionsOur study provides an insight into the phylogeny and evolution of mycovirus-related dsRNA viruses and reveals that the occurrence of HGT between different virus species and the development of multipartite genomes during evolution are important macroevolutionary mechanisms in dsRNA viruses.

Fungal negative-stranded RNA virus that is related to bornaviruses and nyaviruses

“…At present, mycoviruses with RNA genomes are classified into 12 families, of which 4 contain dsRNA viruses, 6 comprise (+)ssRNA viruses, and 2 families (Metaviridae and Pseudoviridae) accommodate RNA reverse-transcribing genomes (1). However, an increasing number of mycoviruses that differ from those classified have been found (7)(8)(9). Recently, Kondo et al (10) identified L protein-like gene sequences of a putative (−)ssRNA virus in the genome of Erysiphe pisi, a fungal plant pathogen, and they also assembled incomplete genomic sequences of (−)ssRNA viruses in transcriptome shotgun assembly libraries of another fungal pathogen, Sclerotinia homoeocarpa, and suggested that (−)ssRNA viruses are most likely to exist in fungi (10).…”

A Novel Partitivirus That Confers Hypovirulence on Plant Pathogenic Fungi

“…As more partitiviruses were isolated and their genomes were sequenced, it became clear that some fungal partitiviruses are phylogenetically more closely related to plant partitiviruses than to some other fungal partitiviruses (18,19); therefore, the host-based taxonomic classification of partitiviruses is no longer suitable. To address this inconsistency, the classification of genera in this family has recently been reevaluated (20)(21)(22). A proposal to have the family Partitiviridae be reorganized to include four new genera, Alphapartitivirus, Betapartitivirus, Gammapartitivirus, and Deltapartitivirus, was recently approved by the International Committee for Taxonomy of Viruses (http://talk.ictvonline.org/files/proposals/taxonomy_proposals _fungal1/m/fung04/4772.aspx).…”

Characterization of a Novel Megabirnavirus from Sclerotinia sclerotiorum Reveals Horizontal Gene Transfer from Single-Stranded RNA Virus to Double-Stranded RNA Virus

“…The events of horizontal gene transfer (HGT) commonly occur not only between distinct evolutionary lineages of ssRNA, dsRNA, or DNA viruses but also between DNA and ssRNA viruses (7,54,55,56,57,58,59,60). These HGT events have been a major contributor of evolutionary innovation and a driver of speciation and environmental adaptation for viruses.…”

“…Mycoviruses with dsRNA genomes are usually encapsidated in rigid particles and are so far classified into six families, including two newly established families, Megabirnaviridae and Quadriviridae (1,5,6). However, an increasing number of newly discovered and characterized dsRNA mycoviruses remain unassigned (7,8).…”