Aphid Vectors Research Articles

Transgenic plum Prunus domestica L., clone C5 (cv. HoneySweet) for protection against sharka disease

Sharka caused by Plum pox virus (PPV) is the most harmful disease of stone fruits in Europe and elsewhere in the world. There is no highly PPV resistant cultivar of plum. Biotech approach has led to the development of resistance through genetic engineering. In this study, we evaluated a transgenic plum Prunus domestica L., clone C5 (cv. HoneySweet), where the PPV resistance is based on RNA interference (RNAi). Resistance in C5 plums has been evaluated for PPV, Prune dwarf virus (PDV), and Apple chlorotic leaf spot virus (ACLSV) in a regulated field trial in the Czech Republic for 12 years (2002–2013). Even under high and permanent infection pressure introduced through graft inoculation of the viruses, PPV has been detected in C5 trees only in several leaves situated close to the point of inoculum grafting in the first nine years. Mild symptoms of PPV disappeared year by year. No PPV symptoms were observed in the last three years and results of ELISA detection were negative. Similar results were obtained, when RT-PCR was used for PPV detection. No natural infection of PPV by aphids was recorded in C5 plums, even if PPV infected plants were growing in the same experimental field in close vicinity. Co-infections of PPV with PDV and/or ACLSV had practically no influence on stability of resistance in C5 trees. Twelve years of field testing in the Czech Republic clearly demonstrated the high level of resistance of C5 either to PPV infection by graft inoculation or natural infection through aphid vectors.

Investigating the viral causes of internal necrosis in carrot

Internal necrosis has been observed in UK carrots for at least 10 years and has been linked anecdotally to virus infection. In the 2009 growing season some growers had up to 10% loss of yield with these symptoms. By using a metagenomic approach with high throughput sequencing technology and a statistical analysis Carrot yellow leaf virus (CYLV) has been putatively linked to internal necrosis. Additionally a torrado virus has been identified and putatively named 'Carrot torrado virus' (CTV). Preliminary investigations into the prevalence of CYLV and CTV in UK carrot crops have found virus infection levels of up to 46% virus and incidence of CYLV of up to 35%; and CTV of up to 25% plants affected. These data suggest that CTV may have a similar epidemiology to CYLV, implicating an aphid vector for transmission.

Selective autophagy limits cauliflower mosaic virus infection by NBR1-mediated targeting of viral capsid protein and particles

Autophagy plays a paramount role in mammalian antiviral immunity including direct targeting of viruses and their individual components, and many viruses have evolved measures to antagonize or even exploit autophagy mechanisms for the benefit of infection. In plants, however, the functions of autophagy in host immunity and viral pathogenesis are poorly understood. In this study, we have identified both anti- and proviral roles of autophagy in the compatible interaction of cauliflower mosaic virus (CaMV), a double-stranded DNA pararetrovirus, with the model plant Arabidopsis thaliana We show that the autophagy cargo receptor NEIGHBOR OF BRCA1 (NBR1) targets nonassembled and virus particle-forming capsid proteins to mediate their autophagy-dependent degradation, thereby restricting the establishment of CaMV infection. Intriguingly, the CaMV-induced virus factory inclusions seem to protect against autophagic destruction by sequestering capsid proteins and coordinating particle assembly and storage. In addition, we found that virus-triggered autophagy prevents extensive senescence and tissue death of infected plants in a largely NBR1-independent manner. This survival function significantly extends the timespan of virus production, thereby increasing the chances for virus particle acquisition by aphid vectors and CaMV transmission. Together, our results provide evidence for the integration of selective autophagy into plant immunity against viruses and reveal potential viral strategies to evade and adapt autophagic processes for successful pathogenesis.

A viral protease relocalizes in the presence of the vector to promote vector performance

Vector-borne pathogens influence host characteristics relevant to host–vector contact, increasing pathogen transmission and survival. Previously, we demonstrated that infection with Turnip mosaic virus, a member of one of the largest families of plant-infecting viruses, increases vector attraction and reproduction on infected hosts. These changes were due to a single viral protein, NIa-Pro. Here we show that NIa-Pro responds to the presence of the aphid vector during infection by relocalizing to the vacuole. Remarkably, vacuolar localization is required for NIa-Pro’s ability to enhance aphid reproduction on host plants, vacuole localization disappears when aphids are removed, and this phenomenon occurs for another potyvirus, Potato virus Y, suggesting a conserved role for the protein in vector–host interactions. Taken together, these results suggest that potyviruses dynamically respond to the presence of their vectors, promoting insect performance and transmission only when needed.

Crop‐dominated landscapes have higher vector‐borne plant virus prevalence

Summary Landscape composition affects local arthropod biodiversity, including herbivorous insects and their predators, yet to date landscape effects on insect‐vectored plant diseases have received little attention. Here, we examine how landscape composition affects the prevalence of a viral pathogen in host plants, and the role the arthropod vector assemblage plays in mediating landscape effects. We measured the effect of landscape composition (measured as percentage of cropland and unmanaged land) on the plant virus Potato virus Y (PVY), its aphid vectors, and their coccinellid predators during the 2012 and 2013 field seasons at 19–21 farms. In both years, we found a positive relationship between final virus prevalence and percentage of cropland within 500, 1000 and 1500 m surrounding study sites. Percentage of cropland also had a significant negative effect on aphid species richness, and the aphid community composition in turn affected PVY prevalence. By contrast, landscape composition had no measurable effect on coccinellid abundance or species richness in this study. Synthesis and applications. Our work demonstrates that landscape composition plays an important role in vector‐borne pathogen spread, and that pathogen spread appears to be mediated by the effects of the landscape on the insect vector community. The small spatial scale (≤1500 m) of the effects seen in our study indicates that on‐farm management practices have the potential to reduce virus prevalence on small‐scale farms. Farmers may be able to reduce Potato virus Y prevalence by on‐farm diversification, by isolating potato fields from other agricultural crops, and by not using saved potato seed.

TRANSMISSION OF VIRUSES ASSOCIATED WITH CARROT MOTLEY DWARF BY MYZUS PERSICAE

Co-infection of Carrot red leaf virus (CtRLV), Carrot mottle virus (CMoV) and Carrot red leaf virus associated RNA (CtRLVaRNA) causes Carrot motley dwarf (CMD) disease. This study examined the capacity of the aphid Myzus persicae at transmitting viruses associated with CMD. M. persicae exposed to CMD-infected chervil plants transmitted CtRLV-, CMoV- and CtRLVaRNA to disease-free chervil, fennel, celery, carrot, cilantro, and parsley, as shown by RT-PCR using specific primers. Recipient plants developed typical CMD symptoms. Sequence analysis of the amplified virus genes showed high sequence diversity with corresponding sequences available in GenBank. This study expands on Cavariella aegopodii, the only previously recognized aphid vector of CMD-causing viruses.

Role of Pea Enation Mosaic Virus Coat Protein in the Host Plant and Aphid Vector.

Understanding the molecular mechanisms involved in plant virus–vector interactions is essential for the development of effective control measures for aphid-vectored epidemic plant diseases. The coat proteins (CP) are the main component of the viral capsids, and they are implicated in practically every stage of the viral infection cycle. Pea enation mosaic virus 1 (PEMV1, Enamovirus, Luteoviridae) and Pea enation mosaic virus 2 (PEMV2, Umbravirus, Tombusviridae) are two RNA viruses in an obligate symbiosis causing the pea enation mosaic disease. Sixteen mutant viruses were generated with mutations in different domains of the CP to evaluate the role of specific amino acids in viral replication, virion assembly, long-distance movement in Pisum sativum, and aphid transmission. Twelve mutant viruses were unable to assemble but were able to replicate in inoculated leaves, move long-distance, and express the CP in newly infected leaves. Four mutant viruses produced virions, but three were not transmissible by the pea aphid, Acyrthosiphon pisum. Three-dimensional modeling of the PEMV CP, combined with biological assays for virion assembly and aphid transmission, allowed for a model of the assembly of PEMV coat protein subunits.

Lower incidence of yellow dwarf disease in autumn-sown wheat crops in New Zealand is linked with sowing dates, insecticide regimes and aerial aphid numbers

Symptoms of yellow dwarf disease caused by Luteoviridae viruses (YDV) in each of 43–75 autumn-sown wheat crops per year were monitored for six years during 1998–2005 in Canterbury, New Zealand. They were related to seed and foliar insecticide applications and the numbers of YDV aphid vectors from one to four regional 7.5 m high suction traps during the crop emergence–GS 30 virus infection-risk period. Over the five years when YDV was assessed in each crop on visual symptoms at flag leaf, the YDV incidence in untreated crops tended to increase with increasing numbers of flying aphids. When aphid numbers were below a relatively low threshold during the risk period for each crop, YDV incidence was low irrespective of insecticide treatments. Above this aphid threshold, the incidence of YDV was lowest in crops with an insecticide programme of an imidacloprid seed treatment followed by one foliar application of lambda-cyhalothrin at 17–24 g ai ha−1. This regime was estimated to provide protection from aphid-transmitted virus infection for approximately 50 % of the risk period irrespective of sowing date. Wheat crops treated with an imidacloprid-seed treatment plus one insecticide foliar application had 96 % less virus incidence than untreated crops, and one foliar application alone had 70 % less incidence. These results suggest that a tool incorporating aphid flight patterns and wheat growth stages could be developed to optimise insecticide applications for control of secondary aphid incursions in autumn sown wheat crops in New Zealand.

WATERMELON MOSAIC VIRUS OF PUMPKIN (Cucurbita maxima) FROM SULAWESI: IDENTIFICATION, TRANSMISSION, AND HOST RANGE

A mosaic disease of pumpkin (Cucurbita maxima) was spread widely in Sulawesi. Since the virus had not yet been identified, a study was conducted to identify the disease through mechanical inoculation, aphid vector transmission, host range, and electron microscopic test. Crude sap of infected pumpkin leaf samples was rubbed on the cotyledons of healthy pumpkin seedlings for mechanical inoculation. For insect transmission, five infective aphids were infected per seedling. Seedlings of eleven different species were inoculated mechanically for host range test. Clarified sap was examined under the electron microscope. Seeds of two pumpkin fruits from two different infected plants were planted and observed for disease transmission up to one-month old seedlings. The mosaic disease was transmitted mechanically from crude sap of different leaf samples to healthy pumpkin seedlings showing mosaic symptoms. The virus also infected eight cucurbits, i.e., cucumber (Cucumis sativus), green melon (Cucumis melo), orange/rock melon (C. melo), zucchini (Cucurbita pepo), pumpkin (Cucurbita maxima), water melon (Citrulus vulgaris), Bennicosa hispida, and blewah (Cucurbita sp.). Aphids transmitted the disease from one to other pumpkin seedlings. The virus was not transmitted by seed. The mosaic disease of pumpkin at Maros, South Sulawesi, was associated with flexious particles of approximately 750 nm length, possibly a potyvirus, such as water melon mosaic virus rather than papaya ringspot virus or zucchini yellow mosaic virus.

WATERMELON MOSAIC VIRUS OF PUMPKIN (Cucurbita maxima) FROM SULAWESI: IDENTIFICATION, TRANSMISSION, AND HOST RANGE

A mosaic disease of pumpkin (Cucurbita maxima) was spread widely in Sulawesi. Since the virus had not yet been identified, a study was conducted to identify the disease through mechanical inoculation, aphid vector transmission, host range, and electron microscopic test. Crude sap of infected pumpkin leaf samples was rubbed on the cotyledons of healthy pumpkin seedlings for mechanical inoculation. For insect transmission, five infective aphids were infected per seedling. Seedlings of eleven different species were inoculated mechanically for host range test. Clarified sap was examined under the electron microscope. Seeds of two pumpkin fruits from two different infected plants were planted and observed for disease transmission up to one-month old seedlings. The mosaic disease was transmitted mechanically from crude sap of different leaf samples to healthy pumpkin seedlings showing mosaic symptoms. The virus also infected eight cucurbits, i.e., cucumber (Cucumis sativus), green melon (Cucumis melo), orange/rock melon (C. melo), zucchini (Cucurbita pepo), pumpkin (Cucurbita maxima), water melon (Citrulus vulgaris), Bennicosa hispida, and blewah (Cucurbita sp.). Aphids transmitted the disease from one to other pumpkin seedlings. The virus was not transmitted by seed. The mosaic disease of pumpkin at Maros, South Sulawesi, was associated with flexious particles of approximately 750 nm length, possibly a potyvirus, such as water melon mosaic virus rather than papaya ringspot virus or zucchini yellow mosaic virus.

MOSAIC DISEASE OF MAIZE CAUSED BY SUGARCANE MOSAIC POTYVIRUS IN SULAWESI

Mosaic disease of maize and grasses is commonly found in Sulawesi. The symptoms resemble the common mosaic symptoms of virus infection, but the pathogen has not been identified. The objective of this study was to identify the causal agent of the mosaic disease of maize and grasses in Sulawesi. Transmissions of the virus were studied by mechanical inoculation and the insect vector aphid. Serological study was done by using enzyme linked immunosorbent assay (ELISA). Results of mechanical inoculation showed that the disease was caused by a virus which was transmitted from diseased maize and grasses to healthy sweet corn seedlings. The disease was also transmitted by aphid (Rhopalosiphum maidis). Serological study indicated that the virus was closely related to the sugarcane mosaic virus (SCMV). Based on these results, it can be concluded that the maize and grass mosaic disease was caused by SCMV. <br /><br />

MOSAIC DISEASE OF MAIZE CAUSED BY SUGARCANE MOSAIC POTYVIRUS IN SULAWESI

Mosaic disease of maize and grasses is commonly found in Sulawesi. The symptoms resemble the common mosaic symptoms of virus infection, but the pathogen has not been identified. The objective of this study was to identify the causal agent of the mosaic disease of maize and grasses in Sulawesi. Transmissions of the virus were studied by mechanical inoculation and the insect vector aphid. Serological study was done by using enzyme linked immunosorbent assay (ELISA). Results of mechanical inoculation showed that the disease was caused by a virus which was transmitted from diseased maize and grasses to healthy sweet corn seedlings. The disease was also transmitted by aphid (Rhopalosiphum maidis). Serological study indicated that the virus was closely related to the sugarcane mosaic virus (SCMV). Based on these results, it can be concluded that the maize and grass mosaic disease was caused by SCMV. <br /><br />

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.

Aphid vectors of Papaya ringspot virus and their weed hosts in orchards in the major papaya producing and exporting region of Brazil

Papaya ringspot, one of the most important diseases of papaya, is caused by Papaya ringspot virus type P (PRSV-P), which is transmitted by various aphid species. Objectives of this research were to identify the aphid species and their weed hosts of papaya orchards in the major papaya producing and exporting region of Brazil in northern Espírito Santo State. Aphids were collected from weed hosts, and with Möericke-type traps in papaya orchards of twenty farms in Linhares, Sooretama and Aracruz municipalities of Espírito Santo, Brazil. A total of forty aphid species were collected, of which 22 are new records in the State. Thirty-eight aphid species were identified from traps, including Aphis craccivora Koch, A. gossypii Glover, A. spiraecola Patch, Myzus persicae (Sulzer), and Toxoptera citricidus (Kirkaldy), known vectors of PRSV-P. Cryptomyzus Oestlund (Aphididae) is recorded for the first time in Brazil. Thirteen aphid species associated with 22 weed species of 14 families were collected. Aphis gossypii, which has been reported to be one of the most efficient vectors of PRSV-P, infested the greatest number of weed hosts. Chamaesyce hyssopifolia (L.) Small, Euphorbia hirta L. (Euphorbiaceae), Commelina benghalensis L. (Commelinaceae), Lepidium virginicum L. (Brassicaceae) and Sida sp. (Malvaceae) were the most frequently infested weeds. Commelina benghalensis was infested by the greatest number of aphid species during this study. Integrated management of weed hosts of aphids to reduce aphid populations in papaya orchards may be useful for control of PRSV-P. Based on accurate knowledge of the aphid and weed species present in papaya orchards obtained in this study, integrated pest management efforts may be more efficiently directed toward eliminating the most frequently infested weed species that serve as hosts for aphid vectors of PRSV-P.

Landscape composition is more important than local management for crop virus–insect vector interactions

Managing crop viruses is difficult due to complex interactions among vectors, reservoirs, and mediating factors such as land cover. Identifying the appropriate ecological neighborhood, or the spatial area in which the most influential interactions occur affecting virus epidemiology, would therefore be beneficial in exposing which of the many explanatory variables to target in the plant-pathogen system. We constructed partial least squares path models to find the neighborhood size for vectors of stylet-borne nonpersistent viruses infecting pumpkins, and compare the relative influence of within-field and extra-field land cover. Two economically important aphid-vectored viruses in the U.S. Midwest are included in these analyses: papaya ringspot virus (PRSV) and watermelon mosaic virus (WMV). In 2010 and 2011, we used commercial pumpkin fields to quantify virus infection, vector (aphid) alightment (i.e., landing rates), and within-field weed communities, and subsequently analyzed extra-field cover from 1 to 5km concentric buffer zones within the surrounding landscape. Alightment rates of total noncolonizing vectors and the top three numerically dominant species (Aphis craccivora Koch, Therioaphis trifolii (Monell), and Rhopalosiphum padi [L.]) were included in individual path models. Overall, we found that extra-field landscape composition had a far stronger influence on vector alightment than within-field weed cover; this pattern was consistent for seven of eight statistical models. In one exception, weed cover influenced alightment of the putative PRSV vector, A. craccivora, while surrounding landscape had no effect. In this case, weed coverage and vector alightment were inversely related, demonstrating that aphids were less likely to land in weed-infested fields. However, weed cover did not predict alightment of T. trifolii or total noncolonizers. The neighborhood size scales for total noncolonizers’ tended to be larger than for individual species (4–5km), suggesting future studies of dispersal by multi-species aphid groups may benefit from an extended gradient. On balance, our results indicate that while surrounding land cover interactions are complex, they exert greater influence over vector dispersal than within-field weed cover, calling into question whether management of local weeds is an effective method of crop virus prevention in some systems.

Possible induction of potato plant defences against Potato virus Y by mineral oil application

In recent decades, mineral oil spray has been considered an effective means to reduce aphid-mediated spread of non-persistent viruses such as Potato virus Y (PVY). However, the mechanism by which mineral oil prevents viral outbreaks is not well-characterized. Despite the fact that several studies have investigated the effects of mineral oil on aphid feeding behaviour, vector fitness and virus attachment to vector mouthparts, the effect of oil treatment on the plant response has not been studied. To address this need, the current study has assessed the impact of Vazyl-Y mineral oil on the plant-vector-virus (i.e. potato-aphid-PVY) pathosystem in potato, with a particular focus on the plant response. These results show for the first time that oil treatment induces the expression of plant-virus interaction related genes in both local and systemic non-infected tissues, as well as in PVY-infected plants. Finally, the oil’s elicitation properties in reducing viral infectivity are discussed.

Minor Coat and Heat Shock Proteins Are Involved in the Binding of Citrus Tristeza Virus to the Foregut of Its Aphid Vector, Toxoptera citricida

Limited information is known about the specific interactions between citrus tristeza virus and its aphid vectors. These interactions are important for the process of successful transmission. In this study, we localized the CTV retention site as the cibarium of the aphid foregut. Moreover, we demonstrated that the nature of these interactions is protein-carbohydrate binding. The viral proteins, including the minor coat protein and two heat shock proteins, bind to sugar moieties on the surface of the foregut. These findings will help in understanding the transmission mechanism of CTV by the aphid vector and may help in developing control strategies which interfere with the CTV binding to its insect vector to block the transmission.

New aphid vectors and efficiency of transmission of Potato virus A and strains of Potato virus Y in the UK

The aphid‐transmitted viruses Potato virus Y (PVY) and Potato virus A (PVA) commonly affect seed potatoes in the UK. The transmission efficiency for aphid species is used to calculate a potential transmission risk and is expressed as a relative efficiency factor (REF). These REFs have not previously been calculated for UK strains of viruses or aphid clones. Using a previously published method, REFs have been calculated for the aphid species and viruses commonly occurring in UK potatoes. The efficiency of transmission of Myzus persicae is nominally set to a REF of 1 and REFs for other species are calculated relative to this. These data represent the first set of REFs calculated for PVA transmission. Macrosiphum euphorbiae (REF 0.91) was almost as efficient as M. persicae at PVA transmission. The data were further analysed to compare transmission rates of PVY and PVA using a binomial (logit) generalized mixed model to take into account the potential influence of variation in virus titre between leaves. This approach found that there is little variation between the efficiency of transmission between clones of each aphid species or between strains within a virus species. This is a first report that Aphis fabae, Metopolophium dirhodum, Sitobion avenae, Acyrthosiphon pisum and Cavariella aegopodii have the ability to vector PVA. This study also represents a first report that C. aegopodii has the ability to vector PVY and confirms the potential of S. avenae, A. fabae, M. euphorbiae and Rhopalosiphum padi as important PVY vectors.

Aphid vector population density determines the emergence of necrogenic satellite RNAs in populations of cucumber mosaic virus.

The satellite RNAs of cucumber mosaic virus (CMV) that induce systemic necrosis in tomato plants (N-satRNA) multiply to high levels in the infected host while severely depressing CMV accumulation and, hence, its aphid transmission efficiency. As N-satRNAs are transmitted into CMV particles, the conditions for N-satRNA emergence are not obvious. Model analyses with realistic parameter values have predicted that N-satRNAs would invade CMV populations only when transmission rates are high. Here, we tested this hypothesis experimentally by passaging CMV or CMV+N-satRNAs at low or high aphid densities (2 or 8 aphids/plant). As predicted, high aphid densities were required for N-satRNA emergence. The results showed that at low aphid densities, random effects due to population bottlenecks during transmission dominate the epidemiological dynamics of CMV/CMV+N-satRNA. The results suggest that maintaining aphid populations at low density will prevent the emergence of highly virulent CMV+N-satRNA isolates.

Development of Molecular Markers Closely Linked to the Potato Leafroll Virus Resistance Gene, Rlr etb , for use in Marker-Assisted Selection

Potato leafroll virus (PLRV) is a major pathogen of potato with worldwide impact on seed and commercial production of potato. In North America, the primary potato cultivars grown by industry are not resistant to PLRV and require the application of insecticides to control the aphid vector of PLRV, so as to prevent PLRV infection of the crop. The Solanum etuberosum- derived dominant gene Rlretb confers resistance to PLRV and has been mapped to chromosome 4. The previous closest marker to Rlretb, C2_At1g42990, was mapped 13.6 cM from the gene in a BC3 population. Cleaved amplified polymorphic sequence markers were developed in the region surrounding C2_At1g42990 and mapped along with Rlretb in 102 BC4 progeny. Sixteen markers were identified surrounding Rlretb, with flanking markers at 2.1 and 9.3 cM. Two markers, 1367-8a and DMB32-11, both 2.1 cM from Rlretb, are shown to be well suited for marker assisted selection. The development of additional molecular markers more closely linked to Rlretb will greatly facilitate its use in potato breeding and its continued introgression into cultivated potato for the development of PLRV-resistant cultivars.