The Recent Recombinant Evolution of a Major Crop Pathogen, Potato virus Y

Abstract

Potato virus Y (PVY) is a major agricultural disease that reduces crop yields worldwide. Different strains of PVY are associated with differing degrees of pathogenicity, of which the most common and economically important are known to be recombinant. We need to know the evolutionary origins of pathogens to prevent further escalations of diseases, but putatively reticulate genealogies are challenging to reconstruct with standard phylogenetic approaches. Currently available phylogenetic hypotheses for PVY are either limited to non-recombinant strains, represent only parts of the genome, and/or incorrectly assume a strictly bifurcating phylogenetic tree. Despite attempts to date potyviruses in general, no attempt has been made to date the origins of pathogenic PVY. We test whether diversification of the major strains of PVY and recombination between them occurred within the time frame of the domestication and modern cultivation of potatoes. In so doing, we demonstrate a novel extension of a phylogenetic approach for reconstructing reticulate evolutionary scenarios. We infer a well resolved phylogeny of 44 whole genome sequences of PVY viruses, representative of all known strains, using recombination detection and phylogenetic inference techniques. Using Bayesian molecular dating we show that the parental strains of PVY diverged around the time potatoes were first introduced to Europe, that recombination between them only occurred in the last century, and that the multiple recombination events that led to highly pathogenic PVYNTN occurred within the last 50 years. Disease causing agents are often transported across the globe by humans, with disastrous effects for us, our livestock and crops. Our analytical approach is particularly pertinent for the often small recombinant genomes involved (e.g. HIV/influenza A). In the case of PVY, increased transport of diseased material is likely to blame for uniting the parents of recombinant pathogenic strains: this process needs to be minimised to prevent further such occurrences.

Phylodynamic evidence of the migration of turnip mosaic potyvirus from Europe to Australia and New Zealand

“…S6) using the method described by Visser et al (2012). Recombinant sequences were split into their separate regions and realigned using gaps.…”

“…They have spread throughout much of the subtropical and temperate zones of the world King et al, 2012). Potato virus Y (Ogawa et al, 2008;Visser et al, 2012), turnip mosaic virus (TuMV) (Ohshima et al, 2002), soybean mosaic virus (Seo et al, 2009) and zucchini yellow mosaic virus (Lecoq et al, 2009) are important potyviruses with worldwide distributions. Nevertheless, there remains a poor understanding of how and when they dispersed, and of what factors controlled that spread.…”

Potato virus Y (PVY) strains in Belgian seed potatoes and first molecular detection of the N-Wi strain

“…However, these variations are mainly introduced by recombination in different parts of the genome (Glais et al 2002, Nie & Singh 2003a, Lorenzen et al 2006a, Chikh Ali et al 2007a, b, 2010b. Three to four recombinant junctions in NTN strains and only one or two recombinant junctions in PVY N-Wi and PVY N:O have been reported (Glais et al 2002, Nie & Singh 2003a, Lorenzen et al 2006a, b, Schubert et al 2007, Visser et al 2012, Karasev & Gray 2013. Position and length of these recombinant segments, resulting in variations in recombinant junctions or breakpoints, have led to several publications on the existence of NTN variants (a and b) and on differentiating N-Wi & N:O subgroups, which have been summarized in the recent reviews of Visser et al (2012) and Karasev & Gray (2013).…”

Recombination provides evidence for ancient hybridisation in the Silene aegyptiaca (Caryophyllaceae) complex

“…Hybridisation has the potential to bring together divergent alleles into the same genome, where they can then be recombined. If a recombined allele becomes fixed and persists to be sampled, it may be possible to infer which lineages contributed to this allele, for example, by separate phylogenetic analysis of non-recombined parts of the locus (Rautenberg et al 2008;Kelly et al 2010;Schwartz et al 2015) combined with multi-labelling approaches (Visser et al 2012). However, competing explanations for the origins of chimaeric alleles need to be considered before hybridisation can be inferred (e.g.…”