The Recent Recombinant Evolution of a Major Crop Pathogen, Potato virus Y (original) (raw)

The phylogenetics of the global population of potato virus Y and its necrogenic recombinants

Virus Evolution, 2017

Potato virus Y (PVY) is a major pathogen of potatoes and other solanaceous crops worldwide. It is most closely related to potyviruses first or only found in the Americas, and it almost certainly originated in the Andes, where its hosts were domesticated. We have inferred the phylogeny of the published genomic sequences of 240 PVY isolates collected since 1938 worldwide, but not the Andes. All fall into five groupings, which mostly, but not exclusively, correspond with groupings already devised using biological and taxonomic data. Only 42 percent of the sequences are not recombinant, and all these fall into one or other of three phylogroups; the previously named C (common), O (ordinary), and N (necrotic) groups. There are also two other distinct groups of isolates all of which are recombinant; the R-1 isolates have N (5 0 terminal minor) and O (major) parents, and the R-2 isolates have R-1 (major) and N (3 0 terminal minor) parents. Many isolates also have additional minor intra-and inter-group recombinant genomic regions. The complex interrelationships between the genomes were resolved by progressively identifying and removing recombinants using partitioned sequences of synonymous codons. Least squared dating and BEAST analyses of two datasets of gene sequences from non-recombinant heterochronously-sampled isolates (seventy-three non-recombinant major ORFs and 166 partial ORFs) found the 95% confidence intervals of the TMRCA estimates overlap around 1,000 CE (Common Era; AD). We attempted to identify the most accurate datings by comparing the estimated phylogenetic dates with historical events in the worldwide adoption of potato and other PVY hosts as crops, but found that more evidence from gene sequences of non-potato isolates, especially from South America, was required.

Phylogeography and molecular evolution of potato virus Y

PloS one, 2012

Potato virus Y (PVY) is an important plant pathogen, whose host range includes economically important crops such as potato, tobacco, tomato, and pepper. PVY presents three main strains (PVY(O), PVY(N) and PVY(C)) and several recombinant forms. PVY has a worldwide distribution, yet the mechanisms that promote and maintain its population structure and genetic diversity are still unclear. In this study, we used a pool of 77 complete PVY genomes from isolates collected worldwide. After removing the effect of recombination in our data set, we used bayesian techniques to study the influence of geography and host species in both PVY population structure and dynamics. We have also performed selection and covariation analyses to identify evolutionarily relevant amino acid residues. Our results show that both geographic and host-driven adaptations explain PVY diversification. Furthermore, purifying selection is the main force driving PVY evolution, although some indications of positive select...

Recombination in viruses: Mechanisms, methods of study, and evolutionary consequences

Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases, 2015

Recombination is a pervasive process generating diversity in most viruses. It joins variants that arise independently within the same molecule, creating new opportunities for viruses to overcome selective pressures and to adapt to new environments and hosts. Consequently, the analysis of viral recombination attracts the interest of clinicians, epidemiologists, molecular biologists and evolutionary biologists. In this review we present an overview of three major areas related to viral recombination: (i) the molecular mechanisms that underlie recombination in model viruses, including DNA-viruses (Herpesvirus) and RNA-viruses (Human Influenza Virus and Human Immunodeficiency Virus), (ii) the analytical procedures to detect recombination in viral sequences and to determine the recombination breakpoints, along with the conceptual and methodological tools currently used and a brief overview of the impact of new sequencing technologies on the detection of recombination, and (iii) the major...

Recombination Every Day: Abundant Recombination in a Virus during a Single Multi-Cellular Host Infection

PLoS Biology, 2005

Viral recombination can dramatically impact evolution and epidemiology. In viruses, the recombination rate depends on the frequency of genetic exchange between different viral genomes within an infected host cell and on the frequency at which such co-infections occur. While the recombination rate has been recently evaluated in experimentally co-infected cell cultures for several viruses, direct quantification at the most biologically significant level, that of a host infection, is still lacking. This study fills this gap using the cauliflower mosaic virus as a model. We distributed four neutral markers along the viral genome, and co-inoculated host plants with marker-containing and wild-type viruses. The frequency of recombinant genomes was evaluated 21 d post-inoculation. On average, over 50% of viral genomes recovered after a single host infection were recombinants, clearly indicating that recombination is very frequent in this virus. Estimates of the recombination rate show that all regions of the genome are equally affected by this process. Assuming that ten viral replication cycles occurred during our experiment-based on data on the timing of coat protein detection-the per base and replication cycle recombination rate was on the order of 2 3 10 À5 to 4 3 10 À5. This first determination of a virus recombination rate during a single multi-cellular host infection indicates that recombination is very frequent in the everyday life of this virus.

Recombination hotspots and host susceptibility modulate the adaptive value of recombination during maize streak virus evolution

BMC Evolutionary …, 2011

Background: Maize streak virus -strain A (MSV-A; Genus Mastrevirus, Family Geminiviridae), the maize-adapted strain of MSV that causes maize streak disease throughout sub-Saharan Africa, probably arose between 100 and 200 years ago via homologous recombination between two MSV strains adapted to wild grasses. MSV recombination experiments and analyses of natural MSV recombination patterns have revealed that this recombination event entailed the exchange of the movement protein -coat protein gene cassette, bounded by the two genomic regions most prone to recombination in mastrevirus genomes; the first surrounding the virion-strand origin of replication, and the second around the interface between the coat protein gene and the short intergenic region. Therefore, aside from the likely adaptive advantages presented by a modular exchange of this cassette, these specific breakpoints may have been largely predetermined by the underlying mechanisms of mastrevirus recombination. To investigate this hypothesis, we constructed artificial, low-fitness, reciprocal chimaeric MSV genomes using alternating genomic segments from two MSV strains; a grass-adapted MSV-B, and a maize-adapted MSV-A. Between them, each pair of reciprocal chimaeric genomes represented all of the genetic material required to reconstruct -via recombination -the highly maize-adapted MSV-A genotype, MSV-MatA. We then coinfected a selection of differentially MSV-resistant maize genotypes with pairs of reciprocal chimaeras to determine the efficiency with which recombination would give rise to high-fitness progeny genomes resembling MSV-MatA. Results: Recombinants resembling MSV-MatA invariably arose in all of our experiments. However, the accuracy and efficiency with which the MSV-MatA genotype was recovered across all replicates of each experiment depended on the MSV susceptibility of the maize genotypes used and the precise positions -in relation to known recombination hotspots -of the breakpoints required to re-create MSV-MatA. Although the MSV-sensitive maize genotype gave rise to the greatest variety of recombinants, the measured fitness of each of these recombinants correlated with their similarity to MSV-MatA. Conclusions: The mechanistic predispositions of different MSV genomic regions to recombination can strongly influence the accessibility of high-fitness MSV recombinants. The frequency with which the fittest recombinant MSV genomes arise also correlates directly with the escalating selection pressures imposed by increasingly MSV-resistant maize hosts.

Bayesian Inference of Viral Recombination: Topology distance between DNA segments and its Distribution

2008

Abstract Recombinant DNA sequences can not be represented by a single topology since recombinant segments support distinct evolutionary histories. Existing methods for recombination detection can handle only a limited number of taxa, constraining the recombination analysis to cases where the phylogeny can be assumed known for the parental sequences. If the analysis is conducted independently for each putative recombinant sequence, potential recombinations between them are neglected.

Full-genome analyses of a Potato Virus Y (PVY) isolate infecting pepper (Capsicum annuum L.) in the Republic of South Africa

Virus Genes, 2014

Potato Virus Y (PVY) is a pathogen of economic importance in pepper and other major crop species in the family Solanaceae. Three major PVY strain groups: O, C, and N, have been distinguished on the basis of genome sequencing. In this study, the first full-genome sequence of a PVY isolate (JVW-186) infecting pepper from the province of KwaZulu-Natal, Republic of South Africa is reported. The complete genome sequence of JVW-186 was assembled from overlapping RT-PCR clones using MEGA 5 software. Two ORFs were identified at position 186 and 2915 of the sequence encoding the viral polyprotein and the frameshift translated protein P3NPIPO, respectively. RDP4 software confirmed three recombination breakpoints at position 343, 1365, and 9308 of the sequence. At each recombination event, a 1,021-bp fragment at the 50 end in the region of the P1/HC-Pro protein and a 392-bp fragment in the region of the coat protein shared a high sequence similarity of 91.8 and 98.89 % to the potato borne PVYC isolate PRI-509 and the PVYO isolate SASA-110, respectively. The non-recombinant fragment 1 (342-bp) clustered within the C clade of PVY isolates; however, the large 7,942-bp fragment 3 did not cluster within any of the clades. This suggests the possibility of a PVY isolate that has evolved due to the dynamics of selection pressure or the likelihood of an ancestral PVY strain.

Co-variation of viral recombination with single nucleotide variants during virus evolution revealed by CoVaMa

2021

Adaptation of viruses to their environments occurs through the acquisition of both novel Single-Nucleotide Variants (SNV) and recombination events including insertions, deletions, and duplications. The co-occurrence of SNVs in individual viral genomes during their evolution has been well-described. However, unlike covariation of SNVs, studying the correlation between recombination events with each other or with SNVs has been hampered by their inherent genetic complexity and a lack of bioinformatic tools. Here, we expanded our previously reported CoVaMa pipeline (v0.1) to measure linkage disequilibrium between recombination events and SNVs within both short-read and long-read sequencing datasets. We demonstrate this approach using long-read nanopore sequencing data acquired from Flock House virus (FHV) serially passaged in vitro. We found SNVs that were either correlated or anti-correlated with large genomic deletions generated by nonhomologous recombination that give rise to Defecti...

Detecting Recombination in TT Virus: A Phylogenetic Approach

Journal of Molecular Evolution, 2002

TT virus (TTV) has a remarkable genetic heterogeneity. To study TTV evolution, phylogenetic analyses were performed on 739 DNA sequences mapping in the N22 region of ORF1. Analysis of neighbor-joining consensus trees shows signi®cant dierences between DNA and protein phylogeny. Median joining networks phylogenetic clustering indicates that DNA sequence analysis is biased by homoplasy (i.e., genetic variability not originated by descent), indicative of either hypermutation or recombination. Statistical analysis shows that the signi®cant excess of homoplasy is due to frequent recombination among closely related strains. Recombination events imply that the transmission of TTV is not clonal and provide the necessary basis to explain (i) the high degree of genetic divergence between TTV isolates, (ii) the lack of population structure on a world scale, and (iii) the number of highly divergent strains that seems typical of this virus. We show that recombination phenomena can be detected by phylogenetic analyses in very short sequences when a suciently large data set is available.