The promiscuous evolutionary history of the family Bromoviridae

Abstract

Recombination and segment reassortment are important contributors to the standing genetic variation of RNA viruses and are often involved in the genesis of new, emerging viruses. This study explored the role played by these two processes in the evolutionary radiation of the plant virus family Bromoviridae. The evolutionary history of this family has been explored previously using standard molecular phylogenetic methods, but incongruences have been found among the trees inferred from different gene sequences. This would not be surprising if RNA exchange was a common event, as it is well known that recombination and reassortment of genomes are poorly described by standard phylogenetic methods. In an attempt to reconcile these discrepancies, this study first explored the extent of segment reassortment and found that it was common at the origin of the bromoviruses and cucumoviruses and at least at the origin of alfalfa mosaic virus, American plum line pattern virus and citrus leaf rugose virus. Secondly, recombination analyses were performed on each of the three genomic RNAs and it was found that recombination was very common in members of the genera Bromovirus, Cucumovirus and Ilarvirus. Several cases of recombination involving species from different genera were also identified. Finally, a phylogenetic network was constructed reflecting these genetic exchanges. The network confirmed the taxonomic status of the different genera within the family, despite the phylogenetic noise introduced by genetic exchange. INTRODUCTIONRecombination and segment reassortment are important mechanisms for the genesis of new genetic variability in RNA virus populations. Proportionally, the amount of genetic variability produced after a single recombination event is larger than that produced by single point mutations. Although the importance of recombination was underappreciated in early studies of virus genome evolution, it is now recognized as a widespread phenomenon among positive-strand RNA viruses in animals (Grassly & Holmes, 1997;Holmes et al., 1999;Wilson et al., 1988) and plants (Nagy & Bujarski, 1993;Revers et al., 1996;Aranda et al., 1997;Olsthoorn et al., 2002;Bousalem et al., 2003;Cheng & Nagy, 2003;Moreno et al., 2004;Tan et al., 2004;Bonnet et al., 2005;Urbanowicz et al., 2005;Chare & Holmes, 2006;Weng et al., 2007), as well as in retroviruses such as human immunodeficiency virus type 1 Prljic et al., 2004;Althaus & Bonhoeffer, 2005;Galetto & Negroni, 2005), although it is a rare or even non-existent phenomenon among negativestrand viruses (Chare et al., 2003). There are several mechanisms by which RNA recombination may take place, the most common of which is homologous recombination (Lai, 1992). During this process, the donor replaces a highly homologous region in the acceptor, with the recombinant retaining exactly the same genomic organization of the parental RNA molecules. Therefore, the term homologous refers not only to the presence of sequence homology between both parental RNAs but also the necessity of homologous...

98% identical, 100% wrong: per cent nucleotide identity can lead plant virus epidemiology astray

“…Another is to aim not for a single, bifurcating phylogenetic tree, but a network (Huson & Bryant 2006). The blended evolutionary history of several plant viruses has been traced using split network methods in SPLITSTREES4 (Hu et al 2007;Codoner & Elena 2008;Martin et al 2009). While networks can better reflect the true ancestry of many recombinant plant viruses, the analysis of migration and hypothesis testing is more complicated on a network than bifurcating trees (Huson & Bryant 2006).…”

Natural host range, thrips and seed transmission of distinctTobacco streak virusstrains in Queensland, Australia

“…Mixed infections provide an opportunity for recombination and reassortment of genetic material from multipartite viruses (Pressing & Reanney, 1984;Roossinck, 1997). Genetic exchange occurs with other Bromoviridae members (Codoñer & Elena, 2008) to potentially result in new species which may have quite different host range and pathogenicity characteristics. It is unclear if our observations of mixed RNA segments from TSV-parthenium and TSV-crownbeard indicate these strains are capable of complementing each other or if a new hybrid strain could arise from a reassortment of RNA segments.…”

Putative Recombination Events and Evolutionary History of Five Economically Important Viruses of Fruit Trees Based on Coat Protein-Encoding Gene Sequence Analysis

“…More precisely, whereas information on recombination in PPV made available by various researchers (Cervera et al 1993;Glasa et al 2004Glasa et al , 2005Matic et al 2006;Salvador et al 2006) remains limited, knowledge on recombination in the CP gene of ACLSV, PDV, ApMV, and PNRSV is still lacking. It should be noted that recently Codoner and Elena (2008) reported that based on RNA-2 sequence analysis, PDV and PNRSV seem to be the potential minor and major parents, respectively, of Alfalfa mosaic virus (AMV). Similarly, part of the 5 0 -UTR and the 5 0 most proximal part of MP of Peanut stunt virus were predicted to be donated by PNRSV.…”