The Phylogeography of Potato Virus X Shows the Fingerprints of Its Human Vector

Abstract

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.

Keywords: Andean crop domestication center; Andean lineages; South America; biosecurity significance; dating; evolution; high-throughput sequencing; interpretation; phylogenetics; population genetics; potato; potato virus X; prehistory; strain groups; virus disease.

Figure 1

Map of sample collection sites in the Andean Highlands showing where potato leaf samples were obtained. Peru’s Andean highlands are shown as brown, the country′s coastal desert and Amazonian jungle regions as green and surrounding countries as white. The red dots marked on the main map represent the locations sampled, and the names marked on it are those of the countries’ regional departments sampled (black lines are departmental boundaries). The red dots marked on the individual department maps clustered on either side show each collection site, and the numbers indicate each individual infected sample collected. Individual collection sites are numbered (Supplementary Materials (SM) File S1, column C). The names of the Departments also provide the first three letters of each isolate name (SM File S1, column F).

Figure 2

A Maximum Likelihood phylogeny of the 370 non-rec potato virus X concats. The phylogroups and minor phylogroups have Latin-Arabic numbers, and the clusters (SM File S2) have a capital letter, and in brackets next to them, the number of isolates within each. The Accession Codes of singletons are shown. Singletons or clusters of isolates only from South America, mostly Peru, are green, whereas singletons from other regions of the world, or clusters containing such isolates, are in red. All details are given in SM File S1. Red disks mark the nodes with >0.95 SH support. Scale bar: s/s means substitutions/site. SM File S2 shows the Accession Codes of the isolates in the different clusters shown in this figure.

Figure 3

The mean genetic diversity of the aligned concats from 322 (Peruvian, blue) and 47 (non-Peruvian, red) potato virus X genomes. Estimates of π (substitution/sites) and of Tajima′s D metric were made in a window of 100 nts with a step of 25 nts.

Figure 4

Cartoon showing the most significant genetic linkages between the potato virus X populations of different Peruvian Departments. Linkages are indicated by their F_ST values [97,98].

Figure 5

Graph of the number of Peruvian Departments in which an isolate of each potato virus X cluster was found, plotted against the number of isolates in each cluster. Letters A–L stand for the clusters A–L in Table 2 and Figure 2. As there were no Peruvian isolates within cluster E, it is not included in this Figure.

Figure 6

Graph of the number of recombinants found in each Department plotted against the total number of potato virus X isolates collected from each Department.

Figure 7

A maximum likelihood phylogeny of 44 potexviruses calculated from the concatenated nucleotide sequences of their replicase and coat protein genes. Midpoint of the phylogeny is circled. Acronyms and Accession Codes: ActVX, Actinidia virus X (KR872420); AlstVX, Alstroemeria virus X (NC_007408); AltMV, Alternanthera mosaic virus (GQ179647, LC107515, NC_007731); AlVX, Allium virus X (FJ670570); AspV3, Asparagus virus 3 (AB304848, KJ544560); BabMV, Babaco mosaic virus (MF978248); BamVX, Bamboo mosaic virus (AB636266, KU936346, KX648527, NC_001642); CasCMV, Cassava common mosaic virus (MN428639); CasVX, Cassava virus X (KY288487); CaVX, Cactus virus X (AF308158. JF937699); ClYMV, Clover yellow mosaic virus (D29630); CnVX, Cnidium virus X (LC460456); CyMV, Cymbidium mosaic virus (EF125180); EYMtaV, Euonymus yellow mottle associated virus (MK572000); EYVV, Euonymus yellow vein virus (NC_035190); FxMV, Foxtail mosaic virus (AY121833, MF573299, NC_001483); HoVX, Hosta virus X (NC_011544); HRSV, Hydrangea ringspot virus (NC_006943); LilVX, Lily virus X (NC_007192); LVX, Lettuce virus X (AM745758, NC_010832); MalMV(Chenopodium mosaic virus), NC_008251); MVX, Mint virus X (NC_006948); NanMV, Nandina mosaic virus (AY800279); NerVX, Nerine virus X (NC_007679); NMV, Narcissus mosaic virus (KF752593, NC_001441); OpVX, Opuntia virus X (KY348771, NC_006060); PAMV, Potato aucuba mosaic virus (KY123701, MG356506, NC_003632); PapMV, Papaya mosaic virus (D13957, MN203140, MN203142); PepMV, Pepino mosaic virus (FJ212288, JN133846, MT018444); PhaVX, Phaius virus X (NC_010295); PitVX, Pitaya virus X (NC_024458); PlaMV, Plantago asiatica mosaic virus (AB360796, LC155795, LC422371, NC_003849); PVX, Potato virus X (EU021215, KM659859, MT264741, X55802, MT708134, MT708143, MK116552); SchlVX, Schlumbergera virus X (NC_011659); SeMV, Senna mosaic virus (NC_030746); StMYEV, Strawberry mild yellow edge virus (AJ577359, NC_003794); TaRMV, Tamus red mosaic virus (JN389521); TGVX, Turtle grass virus X (MH077559, NC_040644); TuVX, Tulip virus X (NC_004322); VVX, Vanilla virus X (NC_035205); WCMV, White clover mosaic virus (X06728, X16636, MN814316); YVX-WX1, Yam virus X (NC_025252); YVX-XZ4, Yam virus X (1) (KJ789134); ZygVX, Zygocactus virus X (NC_006059).