Sweet potato is among the most important root crops worldwide, particularly in developing countries, and its production is affected severely by a variety of virus diseases. During the last decade, a number of new viruses have been discovered in sweet potatoes through next-generation sequencing studies. Among them are viruses belonging to the genus Badnavirus and collectively assigned to the species sweet potato pakakuy virus (SPPV). We determined the complete genome sequence of two SPPV isolates and show the ubiquitous presence of similar viruses in germplasm and field material from around the globe. We show that SPPV is not integrated into the sweet potato genome, occurs only at extremely low titers, and is efficiently transmitted through seeds and cuttings. They are unaffected by virus elimination therapy and do not induce discernible symptoms in sweet potatoes or indicator host plants. They show considerable variation in their nucleotide sequences and correspond to several genetic lineages. Studies of their interaction with the two most important sweet potato viruses showed only limited synergistic increase in the titers of one of two SPPV isolates. We contend that these viruses may pose little threat to sweet potato production and more likely represent a new type of persistent virus in sweet potato.

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.

LAMP on-site sweetpotato virus detection workflow.

Breeders have made important efforts to develop genotypes able to resist virus attacks in sweetpotato, a major crop providing food security and poverty alleviation to smallholder farmers in many regions of Sub-Saharan Africa, Asia and Latin America. However, a lack of accurate objective quantitative methods for this selection target in sweetpotato prevents a consistent and extensive assessment of large breeding populations. In this study, an approach to characterize and classify resistance in sweetpotato was established by assessing total yield loss and virus load after the infection of the three most common viruses (SPFMV, SPCSV, SPLCV). Twelve sweetpotato genotypes with contrasting reactions to virus infection were grown in the field under three different treatments: pre-infected by the three viruses, un-infected and protected from re-infection, and un-infected but exposed to natural infection. Virus loads were assessed using ELISA, (RT-)qPCR, and loop-mediated isothermal amplification (LAMP) methods, and also through multispectral reflectance and canopy temperature collected using an unmanned aerial vehicle. Total yield reduction compared to control and the arithmetic sum of (RT-)qPCR relative expression ratios were used to classify genotypes into four categories: resistant, tolerant, susceptible, and sensitives. Using 14 remote sensing predictors, machine learning algorithms were trained to classify all plots under the said categories. The study found that remotely sensed predictors were effective in discriminating the different virus response categories. The results suggest that using machine learning and remotely sensed data, further complemented by fast and sensitive LAMP assays to confirm results of predicted classifications could be used as a high throughput approach to support virus resistance phenotyping in sweetpotato breeding.

Sweetpotato is among the most important root-crops worldwide, particularly in developing countries, and its production is affected severely by a variety of virus diseases. During the last decade a number of new viruses have been discovered in sweetpotatoes from different continents through next generation sequencing studies, among them belonging to the genus Badnavirus and collectively assigned to the species Sweet potato pakkakuy virus (SPPV). We determined the complete genome sequence of two SPPV isolates and show the ubiquitous presence of similar viruses in germplasm and field material from around the globe. We show SPPV is not integrated into the sweetpotato genome, occurs only at extremely low titers but is nevertheless efficiently transmitted through seeds and cuttings. They are unaffected by virus elimination therapy and lack any discernible symptoms in sweetpotatoes or indicator host plants. Nevertheless, they show considerable variation in their nucleotide sequences and correspond to several genetic lineages. Studies of their interaction with the two most important sweetpotato viruses showed only limited synergistic increase in the titres of one of two SPPV isolates. We contend that these viruses may pose little threat to sweetpotato production and more likely represent a new type of persistent virus in a possibly commensal or mutualistic relationship with sweetpotato. Importance: Next generation sequencing approaches have in the last few years led to the discovery of many virus like sequences in different crop plants including sweetpotatoes. The significance of such discoveries can sometimes be elusive when they have not been associated with specific symptoms due to mixed infections or have been found in apparently healthy plants. Badnavirus sequences found in sweetpotatoes provide a typical case. Considering they have now been reported globally, it was important to determine how common these viruses are and what their possible impact may be on sweetpotato production. The significance of our research lies in resolving the case of badnaviruses, providing evidence they represent a new type of vertically transmitted persistent and apparently harmless episomal viruses living in a state of commensalism with their host.