Metagenomic analysis of nepoviruses: diversity, evolution and identification of a genome region in members of subgroup A that appears to be important for host range

J M Hily,A S Spilmont,J Kubina,J S Reynard,N Poulicard,E Vigne,O Lemaire,M Fuchs

doi:10.1007/s00705-021-05111-0

Abstract

Data mining and metagenomic analysis of 277 open reading frame sequences of bipartite RNA viruses of the genus Nepovirus, family Secoviridae, were performed, documenting how challenging it can be to unequivocally assign a virus to a particular species, especially those in subgroups A and C, based on some of the currently adopted taxonomic demarcation criteria. This work suggests a possible need for their amendment to accommodate pangenome information. In addition, we revealed a host-dependent structure of arabis mosaic virus (ArMV) populations at a cladistic level and confirmed a phylogeographic structure of grapevine fanleaf virus (GFLV) populations. We also identified new putative recombination events in members of subgroups A, B and C. The evolutionary specificity of some capsid regions of ArMV and GFLV that were described previously and biologically validated as determinants of nematode transmission was circumscribed in silico. Furthermore, a C-terminal segment of the RNA-dependent RNA polymerase of members of subgroup A was predicted to be a putative host range determinant based on statistically supported higher π (substitutions per site) values for GFLV and ArMV isolates infecting Vitis spp. compared with non-Vitis-infecting ArMV isolates. This study illustrates how sequence information obtained via high-throughput sequencing can increase our understanding of mechanisms that modulate virus diversity and evolution and create new opportunities for advancing studies on the biology of economically important plant viruses.

Highlights

New viral sequences are being discovered at an unprecedented rate since the advent of high-throughput sequencing (HTS)
We focused on RNA1 and RNA2 coding sequences to gain new insights into viral diversity and evolution, and we identified a hitherto undescribed conserved region of the genome that is putatively involved in determining the host range of two subgroup A nepoviruses
Complete open reading frame (ORF) sequences of RNA1 (ORF1) and RNA2 (ORF2) of nepoviruses were considered in this study

Summary

Introduction

New viral sequences are being discovered at an unprecedented rate since the advent of high-throughput sequencing (HTS). F‐68000 Colmar, France 3 PHIM, Université Montpellier, IRD, INRAE, Cirad, SupAgro, Montpellier, France 4 Institute for Plant Production Science, Agroscope, 1260 Nyon, Switzerland 5 Cornell University, Geneva, NY, USA (i.e., environmental, human, veterinary, plant) has allowed previously unknown virus genomes to be described and their diversity to be studied This wealth of information is creating the possibility of using the pangenome for virus taxonomy [17] and increasing our understanding of the mechanisms that modulate virus diversity, evolution, vector and host specificity, and epidemiology [37]. Taxonomy traditionally relies on the genetic relationships among sequences of a few viral coding regions, primarily the replicase and/or coat protein coding domains, and on biological properties such as vector species and host range, among other features [48] This type of biological information is critical for the taxonomic classification of currently known plant viruses, but it is generally lacking when only metagenomic data are available

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