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Role of Hairy Nightshade in the Transmission of Different Potato virus Y Strains on Solanum tuberosum (L.)
Felix A. Cervantes, Department of Entomology and Nematology, University of Florida, Gainesville, FL (formerly at Aberdeen Research and Extension Center, University of Idaho); and Juan M. Alvarez, Aberdeen Research and Extension Center, Department of Plant, Soil and Entomological Sciences (PSES), University of Idaho, Aberdeen, ID 83210
Cervantes, F. A., and Alvarez, J. M. 2010. Role of hairy nightshade in the transmission of different Potato virus Y strains on Solanum tuberosum (L.). Online. Plant Health Progress doi:10.1094/PHP-2010-0526-05-RS.
The complexity of the Potato virus Y (PVY) (Potyviridae: Potyvirus) pathosystem is affected by the presence of several virus strains that differ in their ability to produce tuber necrosis and by the presence of an alternate host that could increase the amount of inoculum in potato fields. Solanum sarrachoides (Sendtner) is an invasive weed from South America present in Pacific Northwest potato agro-ecosystems. It serves as reservoir of PVY and its most efficient vectors: the green peach aphid, Myzus persicae (Sulzer), and the potato aphid, Macrosiphum euphorbiae (Thomas). The role of S. sarracoides as vector and virus reservoir in PVY epidemiology was investigated through a series of laboratory and greenhouse experiments. We studied the symptoms produced in S. sarracoides upon infection with necrotic and non-necrotic strains of PVY and looked at the percentage of infection and titer accumulation of these strains. PVY infection in S. sarrachoides produced symptoms similar to those produced in PVY-infected potato plants. Mottling and yellowing were the main symptoms of infection observed in S. sarrachoides plants, especially by PVYO and PVYNTN infection. Greenhouse transmission studies revealed that PVY-infected S. sarrachoides increased the transmission rate of PVY necrotic strains by M. persicae. The necrotic strain PVYNTN reached higher titer in S. sarrachoides than in potato plants when compared to PVYO and PVYN:O These findings have broadened our understanding of the role and importance of S. sarrachoides in the PVY epidemiology in the potato ecosystems and could potentially be included in the development or optimization of virus management programs.
More than 1 million acres of potatoes were grown in the United States in 2008 with a value of $3.7 billion (6). The Pacific Northwest (Idaho, Washington, and Oregon) accounts for approximately 74% of the potatoes produced in the United States. Potato virus Y (PVY) (Potyviridae: Potyvirus) has become the most economically important potato disease in the region, and has recently caused yield losses of 10 to 80% (7), as well as economic loss due to degraded tuber quality and rejection of over 50% of seed planted for recertification (Idaho Crop Improvement Association, personal communication). In effect, PVY infection is jeopardizing the United States potato seed production industry.
PVY can be transmitted in a non-persistent manner by at least 50 different species of aphids; however, the most efficient vector is the green peach aphid, Myzus persicae (Sulzer) (5). Since acquisition and inoculation of the virus occur in minutes following epidermal probes by the aphid, vectors do not need to colonize potatoes to transmit PVY. Despite M. persicae being the most efficient vector of PVY, it is not the most important vector in seed-potato growing areas in Idaho. In the major seed-potato production region near Rexburg, ID, only five M. persicae were trapped in 2006 compared to more than 1,100 bird cherry-oat aphids, Rhopalosiphum padi (L.) (J. M. Alvarez, unpublished data); suggesting that R. padi contributes more to the spread of PVY than the green peach aphid.
Even the most intensive aphid control may not prevent spread of potato viruses unless measures are also taken to keep virus-source plants at a minimum. Hairy nightshade, Solanum sarrachoides (Sendtner), an abundantly occurring weed in Idaho, harbor PVY (1,2) and has increasingly tested positive for PVY (J. M. Alvarez, unpublished data). Both M. persicae and the potato aphid, Macrosiphum euphorbiae (Thomas), prefer to colonize hairy nightshade over potato plants. Higher landing preference as well as higher reproduction rates of these two species have been observed on hairy nightshade plants than on potato plants (2,8,9). Thus, hairy nightshade is an important component of the PVY-potato pathosystem in the Pacific Northwest and its efficiency as a PVY inoculum source needs to be investigated.
The complexity of this pathosystem is increased by the high genetic variability of PVY. PVY strains have been classified on the basis of symptoms they cause in infected potato and tobacco. PVYO, the most common strain present in the Pacific Northwest, causes leaf mottling and secondary symptoms on potato plants including leaf crinkling and stunting. PVYN, confirmed in the Pacific Northwest for the first time in 2001 (6), causes necrosis on tobacco plants, but only mild mottling or mosaic symptoms on potato foliage. These symptoms are often difficult to detect in most potato cultivars. PVY has been evolving and a recent variant, PVYNTN, a sub-strain belonging to the necrotic PVYN strain group that causes a potato tuber ring necrotic disease, has also been confirmed in the Pacific Northwest. In recent years, new strains that have characteristics of both PVYO and PVYN have been reported in the United States and Canada (4). These new recombinant strains are known as PVYN:O because they were classified as PVYO with a serological assay (ELISA), yet unlike the O strain, produce necrosis on tobacco plants and can cause tuber ring necrotic disease representing additional economic losses for growers. The reason for the emergence of new PVY necrotic and recombinant strains in recent years is unknown.
Roguing and chemical insecticide applications are presently used to control PVY. Because the acquisition and subsequent transmission of PVY is rapid, insecticide applications have not been highly effective for management of PVY on seed potatoes. Russet Burbank, comprising 62% of Idaho potato acreage (6), has no known resistance to PVY and accumulates high titers of the virus (strain N) without displaying clear visual symptoms (3), thus nullifying the practice of roguing as an effective management strategy. For this reason, it is critical to determine the PVY strain reaction in the most commonly planted potato cultivars.
Our research aims to examine infection of S. sarrachoides by different strains of PVY and to study the symptoms and strain reactions in S. sarrachoides upon virus inoculation. Recognition of PVY infection symptoms in S. sarrachoides plants would help early identification of infected plants that might serve as virus inoculum sources. We hypothesized that PVY infection will produce visible symptoms on S. sarrachoides plants and that symptom expression will vary depending on the PVY strain. We also compared the percentage of infection in S. sarrachoides vs. potato plants and assessed the virus titer upon aphid inoculation in these two closely related plants.
PVY Infection Symptoms in Solanum sarrachoides
Two-week-old S. sarrachoides plants were mechanically inoculated with three PVY isolates [O(T1); N:O(Alturas), and NTN(RRA2)] obtained from the USDA-ARS Pathology Laboratory in Aberdeen, ID. Plants were observed daily post inoculation and symptoms were recorded since they first appeared. Infection was confirmed with DAS-ELISA using suitable positive and negative controls. All S. sarrachoides plants inoculated with the three virus strains tested positive to PVY three weeks after inoculation. However, symptoms of infection were observed first at different times for the three strains. Development of symptoms was first observed for PVYO infected plants when compared to the other two strains. PVYO infection symptoms appeared 10 days after inoculation and consisted mainly of leaf mottling and yellowing on the inoculated leaf (Fig. 1A). At 18 days the pathogen had spread systemically and leaf mottling and yellowing were observed throughout the plant. The yellowing started at the border of the leaves and extended through the rest of the leaf and was observed mainly in the middle and upper leaves. Some curling was also observed in a few leaves 25 days after virus inoculation.
Symptoms due to PVYN:O infection appeared only at 23 days after inoculation as very mild yellow spots (Fig. 1B). Severity of the symptoms did not increase greatly with time. Symptoms due to PVYNTN infection showed at 19 days post-inoculation with mild yellowing that rapidly increased in severity with time (Fig. 1C). At 32 days after inoculation the yellowing was present in most of the leaves and was greater than the one observed with the other two strains.
PVY Titer and Percentage of Infection upon Aphid Inoculation
Two-week-old virus-free S. sarrachoides and potato plants (cv. Russet Burbank) were aphid inoculated with the same three PVY isolates mentioned above (O, N:O, and NTN). Aphids were fed on infected plants with any of the three PVY isolates for 1 min for virus acquisition and then individually transferred to a S. sarrachoides or potato plant. Individual aphids were confined in a leaf cage attached to the ventral surface of a leaf of the test plant for 2 min for virus inoculation (see Table 1 for number of plants). One hundred and twenty plants were used as control (5 plants without aphids/plant host/viral strain/four replications).
Table 1. Host plant and virus strain effect on the transmission of
x Transmission was determined as percentage of plants infected
y The interaction between host plant and virus strain was not
Three weeks after inoculation, plants were sampled and 1 g of leaf tissue was used for DAS-ELISA testing to determine percentage of infection and virus titer levels. Standard curves for titer estimation were constructed using purified virus PVYO and PVYN. PVYO titers were matched with absorbance readings of the PVYO standard curve, and PVYN:O and PVYNTN were matched with absorbance readings of the PVYN standard curve. Titer levels were analyzed using PROC GLM in SAS 9.1 (SAS Institute Inc., Cary, NC). Infection and titer mean comparisons were carried out within the model using pair-wise contrasts.
PVY infection was not detected in any of the control plants. While the host plant and the virus strain affected PVY transmission, no interaction was observed between host and strain (Table 1). No difference was observed in the transmission of PVYO between S. sarrachoides (mean ± standard error) (28% ± 4) and potato plants (22% ± 2) (P = 0.4891). No difference was observed in the transmission of PVYN:O between S. sarrachoides (28% ± 4) and potato plants (20% ± 0) (P = 0.3507). Percentage infection by the necrotic strain PVYNTN was higher in S. sarrachoides plants (54% ± 2) than in potato plants (34% ± 10) (P = 0.0455). Averaged across host plants, transmission of PVYNTN was significantly higher than transmission of PVYO and PVYN:O (Table 1).
Regarding the PVY titer, a significant interaction occurred between host plant and virus strain. Within virus strains, no significant difference was observed between PVYO titer in S. sarrachoides (8.05 ng/ul ± 2.36) and potato plants (6.59 ng/ul ± 2.10) (P = 0.9044, Fig. 2). Similarly, no significant difference was observed between PVYN:O titer in S. sarrachoides (1.96 ng/ul ± 0.19) and potato plants (1.50 ng/ul ± 0.07) (P = 0.9702, Fig. 2). However, PVYNTN reached higher titer in S. sarrachoides (80.78 ng/ul ± 19.17) than in potato plants (20.81 ± 8.04) (P < 0.0001, Fig. 2) when compared to PVYO and PVYN:O (Fig. 2). When comparing all three strains in both S. sarrachoides and potato plants, PVYNTN titer in S. sarrachoides plants was significantly higher than PVYO and PVYN:O titer in both hairy nightshade and potato plants (P < 0.0001) (Fig. 2).
The present research illustrates the importance of sources of virus inoculum, aphid vectors, and virus strain in the epidemiology of PVY. Our findings are also consistent with the premise that weedy hosts contribute to epidemiological patterns and potential of PVY strains. Solanum sarrachoides is susceptible to infection by both necrotic and non-necrotic strains of PVY, potentially increasing the amount of virus inoculum present in the field where this weed is present. Infection of S. sarrachoides produced symptoms similar to those produced in PVY-infected potato plants. Mottling and yellowing were the main symptoms of infection observed in S. sarrachoides plants, especially by PVYO and PVYNTN infection. PVYN:O produced milder symptoms than PVYO and PVYNTN.
As a virus host S. sarrachoides allows higher titer concentrations of the necrotic strain PVYNTN than potato and increases the transmission of both necrotic and non-necrotic strains under greenhouse conditions. These results indicate that S. sarrachoides can serve as an equal or better reservoir and inoculum source for PVY than potato plants, with implications for spread of this virus in cultivated potato. Strains such as PVYO that were dominant are being overtaken by relatively new strains such as PVYN:O and PVYNTN. Our results suggest that the higher transmission and titers of these new necrotic strains together with the difficulty in symptom recognition or lack of symptoms might explain in part the increasing incidence of these strains in the field. These findings have broadened our understanding of the role and importance of both S. sarrachoides and the different PVY strains play in the potato ecosystems providing information that could be considered in the development or optimization of virus management programs. The influence of S. sarrachoides as virus inoculum source in the PVY epidemiology in the field remains to be investigated.
We thank Pamela J. H. Hutchinson (PSES, University of Idaho), for providing the hairy nightshade seeds to start these experiments. We also thank Harold Libby for technical support, Babu Srinivasan for technical advice, and Nilsa Bosque-Perez and Sanford Eigenbrode (PSES, University of Idaho) for reviewing earlier versions of the manuscript. Also, we gratefully acknowledge the editor his helpful suggestions. This research was partially funded by the Idaho Potato Commission and Dr. Alvarez’s Hatch funding. This is Idaho Agricultural Experiment Station manuscript PSES-0451.
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