Abstract

The plant-infecting Secoviridae family of viruses forms part of the Picornavirales order, an important group of non-enveloped viruses that infect vertebrates, arthropods, plants and algae. The impact of the secovirids on cultivated crops is significant, infecting a wide range of plants from grapevine to rice. The overwhelming majority are transmitted by ecdysozoan vectors such as nematodes, beetles and aphids. In this study, we have applied a variety of computational methods to examine the evolutionary traits of these viruses. Strong purifying selection pressures were calculated for the coat protein (CP) sequences of nine species, although for two species evidence of both codon specific and episodic diversifying selection were found. By using Bayesian phylogenetic reconstruction methods CP nucleotide substitution rates for four species were estimated to range from between 9.29×10−3 to 2.74×10−3 (subs/site/year), values which are comparable with the short-term estimates of other related plant- and animal-infecting virus species. From these data, we were able to construct a time-measured phylogeny of the subfamily Comovirinae that estimated divergence of ninety-four extant sequences occurred less than 1,000 years ago with present virus species diversifying between 50 and 250 years ago; a period coinciding with the intensification of agricultural practices in industrial societies. Although recombination (modularity) was limited to closely related taxa, significant and often unique similarities in the protein domains between secovirid and animal infecting picorna-like viruses, especially for the protease and coat protein, suggested a shared ancestry. We discuss our results in a wider context and find tentative evidence to indicate that some members of the Secoviridae might have their origins in insects, possibly colonizing plants in a number of founding events that have led to speciation. Such a scenario; virus infection between species of different taxonomic kingdoms, has significant implications for virus emergence.

Highlights

  • The Picornavirales order contains viruses that infect a wide range of eukaryotic organisms including vertebrates (Picornaviridae), arthropods (Dicistroviridae), plants (Secoviridae), insects (Iflaviridae) and algae (Marnaviridae) [1]

  • Full-length sequences were analyzed in Vector NTI (Invitrogen) with each open reading frame separated into its putative functional domains - Protease co-factor (ProCo), Helicase (HEL), Viral protein genome-linked (VPg), Protease (PRO), RNAdependent RNA-polymerase (RdRp), Movement protein (MP) and Coat protein (CP) - as determined by reported cleavage sites, determined either experimentally or in silico

  • The coat protein dataset was divided into two formats for analysis; fulllength (ArMV, Bean pod mottle virus (BPMV) and Rice tungro spherical virus (RTSV)), corresponding to discrete domain sequences with predicted cleavage product ends and shorter partial sequences (Table S2)

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Summary

Introduction

The Picornavirales order contains viruses that infect a wide range of eukaryotic organisms including vertebrates (Picornaviridae), arthropods (Dicistroviridae), plants (Secoviridae), insects (Iflaviridae) and algae (Marnaviridae) [1]. The agronomic importance of members of the Secoviridae is significant: Grapevine fanleaf virus (GFLV) is the oldest and most widespread viral disease to affect grapevine, being first documented in 1865 [9], while rice tungro disease, caused by a combination of two viruses, one of which is the secovirid Rice tungro spherical virus (RTSV) emerged in the 1960s to seriously disrupt rice production in Asia [10]. More recently multiple members of the newly described Torradovirus genus show signs of emergence in tomatoes [11,12]. Their present impact on a wide range of agronomically important crops combined with their continuing emergence means that understanding the Secoviridae from an evolutionary perspective will enhance our ability to develop adequate control strategies against present and future threats

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