Infection Dynamics of Potato Virus Y Isolate Combinations in Three Potato Cultivars.

The United States potato industry has recently experienced a strain shift; recombinant potato virus Y (PVY) strains (e.g., PVYNTN) have emerged as the predominant strains over the long dominant ordinary strain (PVYO), yet both are often found as single infections within the same field and as mixed infections within individual plants. To understand mixed infection dynamics in potato plants and in daughter tubers, three potato varieties varying for PVY resistance, 'Red Maria', 'CalWhite', and 'Pike', were mechanically inoculated either at the pre- or postflowering stage with all possible heterologous isolate combinations of two PVYO and two PVYNTN isolates. Virus titer was determined from leaves collected at different positions on the plant at different times, and tuber-borne infection was determined for two successive generations. PVYNTN accumulated to higher levels than PVYO at nearly all sampling time points in 'Pike' potato. However, both virus strains accumulated to similar amounts in 'Red Maria' and 'CalWhite' potato early in the infection when inoculated preflowering; however, PVYNTN dominated at later stages and in plants inoculated postflowering. Regardless of inoculation time, both virus strains were transmitted to daughter plants raised from the tubers for most isolate combinations. The relative titer of PVYNTN and PVYO isolates at the later stages of mother plant development was indicative of what was found in the daughter plants. Although virus titer differed among cultivars depending on their genetics and virus isolates, it did not change the strain outcome in tuber-borne infection in subsequent generations. Differential virus accumulation in these cultivars suggests isolate-specific resistance to PVY accumulation.

Virus and helper component interactions favour the transmission of recombinant potato virus Y strains.

In recent years, several recombinant strains of potato virus Y, notably PVYNTN and PVYN:O have displaced the ordinary strain, PVYO, and emerged as the predominant strains affecting the USA potato crop. Previously we reported that recombinant strains were transmitted more efficiently than PVYO when they were acquired sequentially, regardless of acquisition order. In another recent study, we showed that PVYNTN binds preferentially to the aphid stylet over PVYO when aphids feed on a mixture of PVYO and PVYNTN. To understand the mechanism of this transmission bias as well as preferential virus binding, we separated virus and active helper component proteins (HC), mixed them in homologous and heterologous combinations, and then fed them to aphids using Parafilm sachets. Mixtures of PVYO HC with either PVYN:O or PVYNTN resulted in efficient transmission. PVYN:O HC also facilitated the transmission of PVYO and PVYNTN, albeit with reduced efficiency. PVYNTN HC failed to facilitate transmission of either PVYO or PVYN:O. When PVYO HC or PVYN:O HC was mixed with equal amounts of the two viruses, both viruses in all combinations were transmitted at high efficiencies. In contrast, no transmission occurred when combinations of viruses were mixed with PVYNTN HC. Further study evaluated transmission using serial dilutions of purified virus mixed with HCs. While PVYNTN HC only facilitated the transmission of the homologous virus, the HCs of PVYO and PVYN:O facilitated the transmission of all strains tested. This phenomenon has likely contributed to the increase in the recombinant strains affecting the USA potato crop.

Different potato virus Y strains frequently co-localize in single epidermal leaf cells and in the aphid stylet.

Single aphids can simultaneously or sequentially acquire and transmit multiple potato virus Y (PVY) strains. Multiple PVY strains are often found in the same field and occasionally within the same plant, but little is known about how PVY strains interact in plants or in aphid stylets. Immuno-staining and confocal microscopy were used to examine the spatial and temporal dynamics of PVY strain mixtures (PVYO and PVYNTN or PVYO and PVYN) in epidermal leaf cells of 'Samsun NN' tobacco and 'Goldrush' potato. Virus binding and localization was also examined in aphid stylets following acquisition. Both strains systemically infected tobacco and co-localized in cells of all leaves examined; however, the relative amounts of each virus changed over time. Early in the tobacco infection, when mosaic symptoms were observed, PVYO dominated the infection although PVYNTN was detected in some cells. As the infection progressed and vein necrosis developed, PVYNTN was prevalent. Co-localization of PVYO and PVYN was also observed in epidermal cells of potato leaves with most cells infected with both viruses. Furthermore, two strains could be detected binding to the distal end of aphid stylets following virus acquisition from a plant infected with a strain mixture. These data are in contrast with the traditional belief of spatial separation of two closely related potyviruses and suggest apparent non-antagonistic interaction between PVY strains that could help explain the multitude of emerging recombinant PVY strains discovered in potato in recent years.

Sequential acquisition of Potato virus Y strains by Myzus persicae favors the transmission of the emerging recombinant strains.

In the past decade recombinant strains of Potato virus Y (PVY) have overtaken the ordinary strain, PVYO, as the predominant viruses affecting the US seed potato crop. Aphids may be a contributing factor in the emergence of the recombinant strains, but studies indicate that differences in transmission efficiency of individual PVY strains either from single or mixed infections, although variable, are not generally significant. Multiple strains of PVY are present in all potato production areas and common in many potato fields. Therefore, it is likely that individual alate aphids moving through a potato field will sequentially encounter multiple strains as they "taste test" multiple potato plants while looking for a suitable host. This study examined the transmission likelihood and efficiency of three common PVY strains when acquired sequentially by individual aphids. Green peach aphids (Myzus persicae, Sulzer) were allowed a 2-3min acquisition access period (AAP) on potato leaves infected with PVYO, PVYN:O or PVYNTN, followed by another 2-3min AAP on a second potato leaf infected with a different PVY strain before being transferred to healthy potato seedlings for a 24h inoculation access period. All possible combinations of the three strains were tested. Strain-specific infection of the recipient plants was determined by TAS-ELISA and RT-PCR 3-4wk post-inoculation. The recombinant strains, PVYN:O and PVYNTN, were transmitted more efficiently than PVYO when they were sequentially acquired regardless of the order acquired. PVYN:O and PVYNTN were transmitted with similar efficiencies when they were sequentially acquired regardless of the order. The recombinant strains appear to preferentially bind to the aphid stylet over PVYO or they may be preferentially released during inoculation. This may contribute to the increased incidence of the recombinant strains over PVYO in fields or production regions where multiple PVY strains are detected.

Responses of Aphid Vectors of Potato leaf roll virus to Potato Varieties.

Potato leaf roll virus (PLRV) can reduce tuber yield and quality in potato. Green peach aphid (Myzus persicae [Sulzer]) and potato aphid (Macrosiphum euphorbiae [Thomas]) are the two most important potato-colonizing PLRV vectors in the Pacific Northwest. We compared My. persicae and Ma. euphorbiae densities and PLRV incidences among potato varieties in the field to clarify the relationships between aphid abundance and PLRV incidence in plants. Aphids were sampled weekly over three years in the potato varieties Russet Burbank, Ranger Russet, and Russet Norkotah in a replicated field trial. In all years, My. persicae was more abundant than Ma. euphorbiae, representing at least 97% of samples. My. persicae densities did not differ among potato varieties across years; very low numbers of Ma. euphorbiae precluded such statistical comparisons for this species. PLRV infection did not differ significantly among potato varieties, although the percent of PLRV-infected plants differed among years when all varieties were combined (46% in 2013, 29% in 2011, 13% in 2012). For Ranger Russet and Russet Norkotah, PLRV incidence was positively correlated with aphid abundance as well as proportion of PLRV-positive aphids. In Russet Burbank, only aphid abundance was positively correlated with PLRV infection. Our results suggest that the three most commonly grown potato varieties in our region do not differ in their susceptibility to PLRV infection, and that aphid density was a consistent indicator of the risk of infection by this virus across varieties. Both of these findings can be used to hone PLRV monitoring and modeling efforts.

Potato virus Y Transmission Efficiency from Potato Infected with Single or Multiple Virus Strains.

There has been a recent shift in the prevalence of Potato virus Y (PVY) strains affecting potato with the ordinary strain PVYO declining and the recombinant strains PVYNTN and PVYN:O emerging in the United States. Multiple PVY strains are commonly found in potato fields and even in individual plants. Factors contributing to the emergence of the recombinant strains are not well defined but differential aphid transmission of strains from single and mixed infections may play a role. We found that the transmission efficiencies by Myzus persicae, the green peach aphid, of PVYNTN, PVYN:O, and PVYO varied depending on the potato cultivar serving as the virus source. Overall transmission efficiency was highest from sources infected with three virus strains, whereas transmission from sources infected with one or two virus strains was not significantly different. Two strains were concomitantly transmitted by individual aphids from many of the mixed-source combinations, especially if PVYO was present. Triple-strain infections were not transmitted by any single aphid. PVYO was transmitted most efficiently from mixed-strain infection sources. The data do not support the hypothesis that differential transmission of PVY strains by M. persicae is a major contributing factor in the emergence of recombinant PVY strains in the U.S. potato crop.

Contribution of Noncolonizing Aphids to Potato Virus Y Prevalence in Potato in Idaho.

Potato virus Y (PVY) is a major concern for potato production in the United States given its impact on both crop quality and yield. Although green peach aphid, Myzus persicae (Sulzer), is the most efficient PVY vector, it may be less abundant in potato-growing areas of Idaho relative to non-potato-colonizing aphid vectors of PVY that may disperse from nearby cereal fields and other crops. A field study was conducted during 2012-2013 to examine if noncolonizing aphids disperse to nearby potato fields as cereal crops dry down before harvest. The aphid fauna was sampled weekly in four different potato fields in south-central and southeastern Idaho using yellow sticky traps and yellow pan traps. Potato fields were chosen with an adjacent cereal field such that the prevailing westerly wind would facilitate aphid dispersal from cereal fields to potato. Non-potato-colonizing aphids sampled included 10 cereal aphid species, the most abundant of which were Rhopalosiphum padi L. and Metopolophium dirhodum (Walker). More than 35 species from noncereal hosts also were found. Overall, green peach aphid abundance was relatively low, ranging from 0.5-2.5% of the total aphid capture between years and among fields. In both years and all locations, cereal aphid abundance peaked in mid- to late July (cereal ripening stage) and decreased thereafter as cereal crops dried. PVY prevalence in the potato fields increased following these increases in aphid abundance. This study suggests that cereal aphids and other noncolonizing aphids are important contributors to PVY prevalence in potato in southern Idaho.

Interactions among potato genotypes, growth stages, virus strains, and inoculation methods in the potato virus Y and green peach aphid pathosystem.

Potato virus Y (PVY) is an economically important and reemerging potato pathogen in North America. PVY infection reduces yield, and some necrotic and recombinant strains render tubers unmarketable. Although PVY(O) is the most prevalent strain in the United States, the necrotic and recombinant strains PVY(NTN) and PVY(N:O) are becoming more widespread. Infection rates in aphid-inoculated (Myzus persicae (Sulzer)) and mechanically inoculated plants were compared across two potato genotypes ('Yukon Gold' and A98345-1), three PVY strains (PVY(O), PVY(N:O), and PVY(NTN)), and two growth stages at inoculation (pre- and postflowering). Susceptibility of genotypes was measured as infection rate using a double-antibody sandwich-enzyme-linked immunosorbent assay; virus titer and tuber mass also were recorded from the infected plants. Yukon Gold generally was more susceptible than A98345-1 to all three PVY strains, especially following mechanical inoculation. Within genotypes, Yukon Gold was most susceptible to PVY(O) and A98345-1 was most susceptible to PVY(N:O). Plants exhibited age-based resistance, with both genotypes showing higher susceptibility at the pre- than postflowering stage. The overall ranking pattern of virus titer in infected plants was PVY(O) > PVY(NTN) > PVY(N:O); across all three strains, infected Yukon Gold had higher titer than infected A98345-1 plants. Yukon Gold plants had lower tuber mass than A98345-1 when infected, and there were differences between the two inoculation methods in regard to tuber mass for the three stains. The results showed differences in infection response between inoculation methods and as a function of genotype, strain, inoculation stage, and their interactions. These factors should be considered when screening genotypes for resistance.