In this review, encouraged by the dictum of Theodosius Dobzhansky that “Nothing in biology makes sense except in the light of evolution”, we outline the likely evolutionary pathways that have resulted in the observed similarities and differences of the extant molecules, biology, distribution, etc. of the potyvirids and, especially, its largest genus, the potyviruses. The potyvirids are a family of plant-infecting RNA-genome viruses. They had a single polyphyletic origin, and all share at least three of their genes (i.e., the helicase region of their CI protein, the RdRp region of their NIb protein and their coat protein) with other viruses which are otherwise unrelated. Potyvirids fall into 11 genera of which the potyviruses, the largest, include more than 150 distinct viruses found worldwide. The first potyvirus probably originated 15,000–30,000 years ago, in a Eurasian grass host, by acquiring crucial changes to its coat protein and HC-Pro protein, which enabled it to be transmitted by migrating host-seeking aphids. All potyviruses are aphid-borne and, in nature, infect discreet sets of monocotyledonous or eudicotyledonous angiosperms. All potyvirus genomes are under negative selection; the HC-Pro, CP, Nia, and NIb genes are most strongly selected, and the PIPO gene least, but there are overriding virus specific differences; for example, all turnip mosaic virus genes are more strongly conserved than those of potato virus Y. Estimates of dN/dS (ω) indicate whether potyvirus populations have been evolving as one or more subpopulations and could be used to help define species boundaries. Recombinants are common in many potyvirus populations (20%–64% in five examined), but recombination seems to be an uncommon speciation mechanism as, of 149 distinct potyviruses, only two were clear recombinants. Human activities, especially trade and farming, have fostered and spread both potyviruses and their aphid vectors throughout the world, especially over the past five centuries. The world distribution of potyviruses, especially those found on islands, indicates that potyviruses may be more frequently or effectively transmitted by seed than experimental tests suggest. Only two meta-genomic potyviruses have been recorded from animal samples, and both are probably contaminants.
Potato virus Y (PVY) causes disease in potatoes and other solanaceous crops. The appearance of its necrogenic strains in the 1980s made it the most economically important virus of potatoes. We report the isolation and genomic sequences of 32 Peruvian isolates of PVY which, together with 428 published PVY genomic sequences, gave an alignment of 460 sequences. Of these 190 (41%) were non-recombinant, and 162 of these provided a dated phylogeny, that corresponds well with the likely history of PVY, and show that PVY originated in South America which is where potatoes were first domesticated. The most basal divergences of the PVY population produced the N and C: O phylogroups; the origin of the N phylogroup is clearly Andean, but that of the O and C phylogroups is unknown, although they may have been first to establish in European crops. The current PVY population originated around 156 CE. PVY was probably first taken from South America to Europe in the 16th century in tubers. Most of the present PVY diversity emerged in the second half of the 19th century, after the Phytophthora infestans epidemics of the mid-19th century destroyed the European crop and stimulated potato breeding. Imported breeding lines were shared, and there was no quarantine. The early O population was joined later by N phylogroup isolates and their recombinants generated the R1 and R2 populations of damaging necrogenic strains. Our dating study has confirmed that human activity has dominated the phylodynamics of PVY for the last two millennia.
The 206 complete genomic sequences of Plum pox virus in GenBank (January 2019) were downloaded. Their main open reading frames (ORF)s were compared by phylogenetic and population genetic methods. All fell into the nine previously recognized strain clusters; the PPV-Rec and PPV-T strain ORFs were all recombinants, whereas most of those in the PPV-C, PPV-CR, PPV-CV, PPV-D, PPV-EA, PPV-M and PPV-W strain clusters were not. The strain clusters ranged in size from 2 (PPV-CV and PPV-EA) to 74 (PPV-D). The isolates of eight of the nine strains came solely from Europe and the Levant (with an exception resulting from a quarantine breach), but many PPV-D strain isolates also came from east and south Asia and the Americas. The estimated time to the most recent common ancestor (TMRCA) of all 134 non-recombinant ORFs was 820 (865-775) BCE. Most strain populations were only a few decades old, and had small intra-strain, but large inter-strain, differences; strain PPV-W was the oldest. Eurasia is clearly the 'centre of emergence' of PPV and the several PPV-D strain populations found elsewhere only show evidence of gene flow with Europe, so have come from separate introductions from Europe. All ORFs and their individual genes show evidence of strong negative selection, except the positively selected pipo gene of the recently migrant populations. The possible ancient origins of PPV are discussed.
On several occasions over the past century it has been proposed that Latinized (Linnaean) binomial names (LBs) should be used for the formal names of virus species, and the opinions expressed in the early debates are still valid. The use of LBs would be sensible for the current Taxonomy if confined to the names of the specific and generic taxa of viruses of which some basic biological properties are known (e.g. ecology, hosts and virions); there is no advantage in filling the literature with formal names for partly described viruses or virus-like gene sequences. The ICTV should support the time-honoured convention that LBs are only used with biological (phylogenetic) classifications. Recent changes have left the ICTV Taxonomy and its Code uncoordinated, and its aims and audience uncertain.
The family Apiaceae comprises approximately 3700 species of herbaceous plants, including important crops, aromatic herbs and field weeds. Here we report a study of 10 preserved historical or recent virus samples of apiaceous plants collected in the United Kingdom (UK) import interceptions from the Mediterranean region (Egypt, Israel and Cyprus) or during surveys of Australian apiaceous crops. Seven complete new genomic sequences and one partial sequence, of the apiaceous potyviruses apium virus Y (ApVY), carrot thin leaf virus (CaTLV), carrot virus Y (CarVY) and celery mosaic virus (CeMV) were obtained. When these 7 and 16 earlier complete non-recombinant apiaceous potyvirus sequences were subjected to phylogenetic analyses, they split into 2 separate lineages: 1 containing ApVY, CeMV, CarVY and panax virus Y and the other CaTLV, ashitabi mosaic virus and konjac virus Y. Preliminary dating analysis suggested the CarVY population first diverged from CeMV and ApVY in the 17th century and CeMV from ApVY in the 18th century. They also showed the “time to most recent common ancestor” of the sampled populations to be more recent: 1997 CE, 1983 CE and 1958 CE for CarVY, CeMV and ApVY, respectively. In addition, we found a new family record for beet western yellows virus in coriander from Cyprus; a new country record for carrot torradovirus-1 and a tentative novel member of genus Ophiovirus as a co-infection in a carrot sample from Australia; and a novel member of the genus Umbravirus recovered from a sample of herb parsley from Israel.
Potato virus X (PVX) occurs worldwide and causes an important potato disease. Complete PVX genomes were obtained from 326 new isolates from Peru, which is within the potato crop′s main domestication center, 10 from historical PVX isolates from the Andes (Bolivia, Peru) or Europe (UK), and three from Africa (Burundi). Concatenated open reading frames (ORFs) from these genomes plus 49 published genomic sequences were analyzed. Only 18 of them were recombinants, 17 of them Peruvian. A phylogeny of the non-recombinant sequences found two major (I, II) and five minor (I-1, I-2, II-1, II-2, II-3) phylogroups, which included 12 statistically supported clusters. Analysis of 488 coat protein (CP) gene sequences, including 128 published previously, gave a completely congruent phylogeny. Among the minor phylogroups, I-2 and II-3 only contained Andean isolates, I-1 and II-2 were of both Andean and other isolates, but all of the three II-1 isolates were European. I-1, I-2, II-1 and II-2 all contained biologically typed isolates. Population genetic and dating analyses indicated that PVX emerged after potato’s domestication 9000 years ago and was transported to Europe after the 15th century. Major clusters A–D probably resulted from expansions that occurred soon after the potato late-blight pandemic of the mid-19th century. Genetic comparisons of the PVX populations of different Peruvian Departments found similarities between those linked by local transport of seed potato tubers for summer rain-watered highland crops, and those linked to winter-irrigated crops in nearby coastal Departments. Comparisons also showed that, although the Andean PVX population was diverse and evolving neutrally, its spread to Europe and then elsewhere involved population expansion. PVX forms a basal Potexvirus genus lineage but its immediate progenitor is unknown. Establishing whether PVX′s entirely Andean phylogroups I-2 and II-3 and its Andean recombinants threaten potato production elsewhere requires future biological studies.
High Plains wheat mosaic virus (HPWMoV) causes a serious disease in major wheat-growing regions worldwide. We report here the complete or partial genomic sequences of five HPWMoV isolates from Australian wheat samples. Phylogenetic analysis of the nucleotide sequences of the eight genomic segments of these five isolates together with others from Genbank found all eight genes formed two lineages, L1 and L2. L1 contained a single isolate from Colorado in the North American Great Plains Region (GPR), and L2 had two unresolved clusters, A and B, of isolates from Australia and the GPR. A quarter of the L2B isolate sequences of the nucleocapsid gene (RNA3) were recombinant, which is unexpected as little evidence of recombination exists in viruses with negative single-stranded RNA genomes. Phylogenies calculated from the amino acid sequences of HPWMoV’s RNA-dependent RNA-polymerase (RNA1), glycoprotein (RNA2), and nucleocapsid protein (RNA3) showed they were closest to those of Palo Verde broom virus. However, its movement protein (RNA4) was closer to those of Ti ringspot-associated and common oak ringspot-associated viruses, indicating the RNA4 segments of their ancestors reassorted to produce the current emaraviruses. To avoid increased yield losses from co-infection, biosecurity measures are advised to avoid HPWMoV introduction to countries where wheat streak mosaic virus already occurs.
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