Effects of tomato spotted wilt virus isolates, host plants, and temperature on survival, size, and development time of Frankliniella occidentalis

Tomato spotted wilt virus (TSWV) replicates in both its plant hosts and its thrips vectors. Replication of TSWV within thrips suggests the potential for pathological effects that could affect the fitness of its vectors directly, whereas infection of the plant may alter its suitability as a host for thrips development. This study was undertaken to examine the influence of TSWV isolate, host plant, and temperature on potential direct and host-mediated effects of virus infection of the thrips and the plant on Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), an important vector of TSWV. Neonate F. occidentalis were reared to adult eclosion on excised foliage of Datura stramonium (L.) (Solanaceae) or Emilia sonchifolia (L.) (Compositae) infected with either the CFL or RG2 isolate of TSWV, or not infected. Effects of the TSWV isolates and host plants on thrips were measured at 18.3, 23.9, and 29.4 °C. Results demonstrate significantly improved survival and a small but significant decrease in development time of F. occidentalis on TSWV-infected plants. These effects resulted from the combined influence of the direct effects of the virus on infected thrips and plant-mediated effects resulting from virus infection of the thrips’ host plant. Our results extend previous findings and help to explain inconsistencies among previously published reports by demonstrating that the manifestation and magnitude of effects of TSWV on F. occidentalis are dependent on host plant, virus isolate, and temperature.     

Thrips tabaci and tomato spotted wilt virus: inheritance of vector competence

Populations of onion thrips, Thrips tabaci Lindeman (Thysanoptera: Thripidae), were shown to differ significantly in their ability to transmit an isolate of tomato spotted wilt virus (Tospovirus: Bunyaviridae) (TSWV) collected from potato [Solanum tuberosum L. (Solanaceae)]. To gain an understanding of the basis for this variation, we generated reciprocal crosses between an efficient and an inefficient transmitting population. The resulting F₁ progeny and progeny from the parental populations were tested for their ability to transmit TSWV. Our results indicate that the ability to transmit TSWV efficiently by T. tabaci is inherited as a recessive trait.     

Does natural deposition of pine pollen affect the ovipositional behavior of Frankliniella occidentalis and Frankliniella fusca?

Tree pollen, especially Pinus spp. (Pinaceae), is shed in large quantities every spring in North America. Pine pollen deposition onto leaves was found to significantly influence the ovipositional behaviors of certain thrips species (Thysanoptera: Thripidae) in peanut and tomato leaf choice and no‐choice tests. Pine pollen (Pinus elliottii Engelm.) increased the oviposition rate 2.9‐fold for Frankliniella occidentalis (Pergande) (western flower thrips) and 1.6‐fold for Frankliniella fusca (Hinds) (tobacco thrips) in choice tests averaged over both plant species. These results support the idea that pollen has a greater impact on F. occidentalis behavior than on F. fusca behavior. The most dramatic increase was in peanut, where F. occidentalis only oviposited on leaves dusted with pollen, suggesting that the addition of pollen stimulated this flower thrips to lay eggs on a poor host‐plant part. The impact of pollen on the rate of oviposition by thrips is important because it is the early‐instar nymphs that acquire tomato spotted wilt virus (TSWV), which these two thrips species vector. In a laboratory bioassay, the addition of pine pollen to TSWV‐infected peanut foliage increased the percentage of infected F. fusca after one generation.     

Screening Capsicum germplasm for resistance to tomato spotted wilt virus (TSWV)

Resistance conferred by the Tsw locus from Capsicum chinense against Tomato spotted wilt virus (TSWV) has been widely used in breeding programmes. Nevertheless, this resistance depends on inoculation conditions, and isolates able to overcome it have already been detected. In this work 29 accessions of several Capsicum species have been mechanically inoculated with TSWV to identify new sources of resistance. Five accessions showed variable percentages of resistant plants, two of which did not show local lesions on inoculated leaves, suggesting that the response was not mediated through hypersensitivity. Two of these accessions also had a remarkable reduced viral accumulation compared to susceptible control. ECU‐973., a C. chinense accession, showed the best performance against TSWV, with 100% resistant plants. This response was confirmed after mechanical inoculation with three different TSWV isolates. The resistance was maintained when the accession was inoculated with TSWV using a high pressure of viruliferous thrips. These results open new possibilities in the development of a durable resistance to TSWV in pepper.     

寄主植物接种番茄斑萎病毒对西花蓟马种群的影响

【目的】西花蓟马Frankliniella occidentalis (Pergande)是一种入侵我国的重要害虫, 而番茄斑萎病毒是以西花蓟马传播为主的一种极具危害性的世界性病毒, 通过研究西花蓟马与番茄斑萎病毒之间的互作将有助于进一步深入理解西花蓟马以及番茄斑萎病毒的发生与猖獗机制, 同时也将为制定合理、可持续的控制西花蓟马及其传播的植物病毒防控策略提供理论依据。【方法】利用应用特定年龄-龄期及两性生命表方法, 研究了西花蓟马在辣椒3种处理（健康CK、机械损伤MD、机械接种番茄斑萎病毒MI）叶片上的生长发育、存活及种群增长。【结果】健康、机械损伤和机械接毒叶片上的发育历期依次为12.45, 11.97和11.18 d。雌雄成虫寿命和雌虫产卵量在不同处理植株叶片上差异显著(P<0.05), 在机械接毒叶片上寿命最长(雌13.51 d, 雄12.69 d); 繁殖能力最强, 产子代数高达33.01头1龄若虫/雌。健康、机械损伤和机械接毒叶片上西花蓟马内禀增长率分别为-0.009, 0.153和0.190 d-1, 净生殖率依次为0.84, 14.54和21.79。【结论】番茄斑萎病毒诱导寄主植物辣椒反应使西花蓟马发育历期缩短, 成虫寿命延长, 繁殖能力提高, 种群增长加速。     

Midgut infection by tomato spotted wilt virus and vector incompetence of Frankliniella tritici

Abstract:  The mechanism leading to vector competence of thrips species to transmit tomato spotted wilt virus (TSWV) is not well characterized. We investigated the interaction of TSWV and the non-vector species Frankliniella tritici . A monoclonal antibody to the non-structural protein (NSs) of the TSWV was used to detect TSWV replication within the thrips by immunofluorescence microscopy and enzyme-linked immonosorbent assay (ELISA). TSWV was acquired by F. tritici , replicated and moved within the alimentary canal of F. tritici similar to a known vector of TSWV, Frankliniella occidentalis . However, virus was not found in the salivary glands of F. tritici , which is a prerequisite to virus transmission. Thus, movement to the salivary glands may determine vector incompetence of F. tritici .     

Differences in tomato spotted wilt virus vector competency between males and females of Frankliniella occidentalis

Possible differences in tomato spotted wilt virus (TSWV) transmission vector competency between Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) males and females were investigated. The males of the Dutch reference population NL3 transmitted TSWV at a notably higher rate (57%) than the females (32%). The viruliferous males also transmitted more frequently within the first six days after adult emergence than the females. For both sexes, the transmission efficiency dropped with age, simultaneously with the consumption rate. The higher vector efficiency for males appeared to be a general phenomenon as this feature was also found for thirteen other F. occidentalis populations, which originated from distinct geographic regions.     

Occurrence and localization of spherical viruslike particles in tissues of apparently healthy tobacco thrips,Frankliniella fusca,a vector of tomato spotted wilt virus

Spherical viruslike particles (VLP) were found in the tissues of apparently healthy tobacco thrips, Frankliniella fusca. The particles occurred in abundance in thrips from Ontario but were absent in thrips from Oklahoma reared under identical conditions. The VLP were not transmissible to any of the seven plant hosts (in four families) of F. fusca suggesting that they may be an insect virus. Transmission of tomato spotted wilt virus (TSWV) by F. fusca, a known vector, was not affected by the presence or absence of the VLP. No TSWV particles were detected in tissues of F. fusca that transmitted TSWV to test plants. The VLP occurred in several internal organs and hemocoele of the thrips and were isolated in vitro by preparing homogenates of gut tissues. Infection of oocytes and presence of VLP in young nymphs suggested transovarial transmission of the particles. The VLP measured 62 ± 4 nm in diameter and usually occurred in dense viroplasms in the cell cytoplasm. Development of the particles within the viroplasms is discussed.     

Selection of tomato plants resistant to a local Polish isolate of tomato spotted wilt virus (TSWV)

We found that the Sw-5 gene confers resistance to one of the Polish isolates of tomato spotted wilt virus (TSWV). A series of tomato breeding accessions was analysed along with standards of resistance and susceptibility to TSWV. The presence of the Sw-5 gene was determined using the available PCR marker. Subsequently plants from these accessions were grown in the presence of the TSWV isolate from Poland. Some of them developed severe symptoms of the TSWV disease. Expression of the virus proteins was also assayed in tissues of the investigated plants. We found general agreement between either lack or presence of the disease symptoms, virus proteins and resistance gene. Some observed discrepancies of these data are also discussed. Our results indicate that marker-assisted selection can be used for breeding of the TSWV-resistant tomato in Poland.     

Spring temperature and precipitation affect tobacco thrips, Frankliniella fusca, population growth and Tomato spotted wilt virus spread within patches of the winter annual weed Stellaria media

Effects of temperature and rainfall timing, amount, and duration on the spread of Tomato spotted wilt virus (Bunyaviridae: genus Tospovirus ; TSWV) and population growth of its primary vector, Frankliniella fusca (Hinds) (Thysanoptera: Thripidae), within patches of common chickweed, Stellaria media (L.) Cyrillo (Caryophyllaceae), were examined during the spring of 2004, 2005, and 2006. Elevated temperature treatments were investigated in an attempt to alter the age structure of F. fusca populations and change the effect of precipitation, but an average increase in daily temperature of 1 °C did not increase population size until late spring. Populations of immature F. fusca were immediately and negatively influenced by large amounts of rainfall or by rainfall distributed over three or more consecutive days during late April and early May. However, when precipitation was distributed over 1–3 days during early May, it also delayed senescence of the chickweed and ultimately resulted in a larger F. fusca population late in the season. The majority of TSWV spread within patches of chickweed occurred after mid-April. The fewest TSWV-infected chickweed plants occurred in plots that received high levels of precipitation during April or throughout spring and the amount of spread was directly related to the size of the immature F. fusca population that developed in each plot.     

Transmission of tomato spotted wilt virus by Frankliniella occidentalism median acquisition and inoculation access period

To quantify the transmission of tomato spotted wilt virus (TSWV) by Frankliniella occidentalis, the median acquisition access period (AAP₅₀) and median inoculation access period (IAP₅₀) were determined. These parameters were established using transmission rates obtained after AAPs and in IAPs which both ranged from 5 to 2560 min. An AAP₅₀ of 106 min was found when larvae acquired virus from TSWV-infected Impatiens plants. IAP₅₀s of 58 or 137 min, respectively, were calculated when petunia or Datura stramonium leaf disks were used to test the inoculation efficiency of viruliferous thrips. The virus could successfully be acquired or inoculated in periods of 5 min. Transmission reached an optimum after an AAP of 21.3 h (AAP_opt) and in an IAP of 42.7 h (IAP_opt). These results show that TSWV can be acquired and transmitted efficiently by F. occidentalis in short feeding periods.     

Transmission of Tomato spotted wilt virus isolates able and unable to overcome tomato or pepper resistance by its vector Frankliniella occidentalis

Tomato spotted wilt virus (TSWV) causes serious diseases of many economically important crops. Disease control has been achieved by breeding tomato and pepper cultivars with the resistance genes Sw‐5 and Tsw, respectively. However, TSWV isolates overcoming these genetic resistances have appeared in several countries. To evaluate the risk of spread of these resistance‐breaking isolates, we tested their ability of transmission by the main vector of TSWV, the thrips Frankliniella occidentalis. We compared the transmission rate by thrips of six TSWV isolates of different biotype (able or unable to overcome this resistance in pepper and tomato), and with divergent genotype (A and B). Our results indicate that the transmission rate was related to the amount of virus accumulated in thrips but not to virus accumulation in the source plants on which thrips acquired the virus. No correlation was found between transmission efficiency by thrips and the genotype or between transmission efficiency and the ability of overcoming both resistances. This result suggests that resistance‐breaking isolates have the same potential to be transmitted as the isolates unable to infect resistant tomato and pepper cultivars.     

Decreased preference and reproduction, and increased mortality of Frankliniella occidentalis on thrips-resistant pepper plants

The effect of thrips resistance in pepper (Capsicum annuum L.) – previously shown to result in impeded thrips population development (Maris PC, Joosten NN, Goldbach RW & Peters D (2003a) Restricted spread of Tomato spotted wilt virus in thrips‐resistant pepper. Phytopathology 93: 1223–1227. Maris PC, Joosten NN, Goldbach RW & Peters D (2003b) Spread of Tomato spotted wilt virus and population development of Frankliniella occidentalis in pepper resistant to thrips. Proceedings of the Section Experimental and Applied Entomology Netherlands Entomological Society (NEV) Amsterdam 14: 95–101.) – on thrips’[Frankliniella occidentalis Pergande (Thysanoptera: Thripidae)] reproduction, mortality, host preference, and behaviour was investigated. Reproduction, studied by oviposition and larval survival, was negatively affected by the thrips‐resistant (TR) phenotype, whereas the offspring's developmental rate did not differ on TR and the thrips‐susceptible (TS) phenotype. While thrips’ behaviour was hardly affected by thrips resistance, a significant preference for TS plants over the TR plants was found in different tests. When released on either a TR or a TS plant, thrips dispersed at significantly higher rates from the TR plants, demonstrating that not only an impeded reproduction, but also a reduced residence time adds to the reported lower thrips numbers on TR plants.     

Influence of tomato spotted wilt virus on performance and behaviour of western flower thrips (Frankliniella occidentalis)

The general principles in pathogen transmission by insects involve a complex and specific interplay, in this case between thrips, tospovirus and their shared host plant, which has led to outbreaks of crop disease epidemics of economic and social importance. The possible processes and factors driving their co‐evolution were partly studied by rearing Frankliniella occidentalis [western flower thrips (WFT)] on either tomato spotted wilt virus (TSWV)–infected or uninfected Capsicum annum leaflets throughout their larval stages. Later, pupae were transferred individually on healthy leaf discs for further studies of the influence of TSWV on WFT development and behavioural patterns. The exposure of WFT to TSWV was found to improve performance with regard to longevity and survival, with mean longevity being significantly higher in TSWV‐exposed WFT compared to unexposed ones (F_(3,403) = 22.44, P < 0.0001). The observed improvement in survival was as a result of significant reduction in mortality for the WFT individuals exposed to TSWV (F_(3,383) = 849.94, P < 0.0001) compared to the unexposed. However, the results showed a significant reduction in mean daily fecundity overtime (F_10,10) = 246.66, P < 0.0001) and across the four treatments (F_(3,30) = 6.62, P = 0.001), as well as lifetime fecundity (F_(3,23) = 21.23, P < 0.0001) of the WFT exposed to TSWV compared to the unexposed reared on uninfected leaf discs. For preferential test, C. annum leaf discs infected with TSWV were more attractive to WFT as compared to healthy leaf discs (χ²_{(4, 34)} = 112.35, P < 0.0001). These results are envisaged to contribute to a clear understanding into the plant–vector–virus interaction, which is essential for accurate diagnosis and control of the TSWV epidemic, as well as the control of F. occidentalis as crop pest.     

Propagation of tomato spotted wilt virus in Frankliniella occidentalis does neither result in pathological effects nor in transovarial passage of the virus

The effect of tomato spotted wilt virus (TSWV) on Frankliniella occidentalis Pergande (Thysanoptera; Thripidae) following a 6-hour acquisition access period on infected plants was investigated. No statistically significant differences were observed among viruliferous, non-viruliferous and control thrips with respect to developmental time, reproduction rate and survival. Thrips larvae, exposed or non-exposed to TSWV, developed from egg to adult in 13.1 and 13.2 days, respectively. Exposed females produced an average of 28.3 larvae whereas control thrips produced 22.3 larvae and longevity was 13.4 and 12.5 days, respectively. None of these values were significantly different. Population reproductive statistics, net reproductive rate (R ₀), mean generation time (T) and intrinsic rate of increase (r _m) were calculated from the life fertility tables. R ₀ and r _m were higher for viruliferous thrips as compared to non-viruliferous and non-exposed thrips. Virus transmission studies revealed that viruliferous thrips were able to transmit virus until death and that TSWV was not transovarially transmitted.     

Specificity of accumulation and transmission of tomato spotted wilt virus (TSWV) in two genera, Frankliniella and Thrips (Thysanoptera: Thripidae)

The accumulation and transmission of tomato spotted wilt virus (TSWV) was examined in second instar larvae and adults of two thrips genera, Frankliniella and Thrips. The species tested were F. occidentalis (Pergande), F. intonsa (Trybom), T. tabaciLindeman, T. setosus Moulton, T. palmi Karny and T. hawaiiensis (Morgan). In a standard petunia leaf disc assay, the efficiencies of TSWV transmission by two species of Frankliniella were higher than those of any Thrips species in the adult stage. A triple antibody sandwich enzyme-linked immunosorbent assay (TAS-ELISA) showed that large amounts of the TSWV-nucleocapsid (N) protein were present in the ELISA-positive larvae of each species, with the exception of T. palmi. The ELISA titre of and the proportion of virus-infected individuals of the two Frankliniella species increased or did not significantly change from the larval to the adult stages, whereas those of the four Thrips species decreased significantly. These results show that the specificity of virus transmission by adult thrips is probably affected by the amount of viral N protein accumulation in the adults and that the accumulation pattern from the larval to the adult stages is in between the two genera tested in the present study.     

Direct and indirect effects of a thrips‐transmitted Tospovirus on the preference and fitness of its vector,Frankliniella fusca

Phytoviruses including tospoviruses are known to affect the behavior and fitness of their vectors both positively and negatively. In this study, we investigated the effects of Tomato spotted wilt virus (TSWV) (family Bunyaviridae, genus Tospovirus) infection on the fitness and feeding ability of tobacco thrips, Frankliniella fusca (Hinds) (Thysanoptera: Thripidae) using peanut, Arachis hypogaea L. (Fabaceae), as a host. Potentially viruliferous F. fusca laid more eggs than non‐viruliferous F. fusca. In contrast, fewer potentially viruliferous F. fusca developed into adults and required a longer developmental time than non‐viruliferous F. fusca, indicating a direct negative effect of the virus on thrips fitness. In addition, no‐choice feeding tests indicated that non‐viruliferous F. fusca fed more rapidly than potentially viruliferous F. fusca. Typically, phytovirus infections are known to enhance the availability of vital nutrients such as free amino acids in infected host plants and to affect other important physiological processes negatively. Free amino acids are known to play a vital role in egg production and development. Further investigations in this study revealed that leaflets of infected plants had ca. 15 times more free amino acids than non‐infected leaflets. TSWV‐infected leaflets were used to rear potentially viruliferous thrips. Higher amino acid levels in TSWV‐infected leaflets than in non‐infected leaflets could have contributed to increased oviposition by potentially viruliferous F. fusca compared to non‐viruliferous F. fusca. Taken together, these results suggest that increased concentrations of free amino acids in TSWV‐infected plants might serve as an incentive for thrips feeding on otherwise unsuitable hosts, thereby facilitating TSWV acquisition and transmission.     

Effects of elevated CO2 on life‐history traits of three successive generations of Frankliniella occidentalis and F. intonsa on kidney bean,Phaseolus vulgaris

The objective of this study was to determine how elevated CO₂ impacts on life‐history traits and life table parameters in three successive generations of invasive species Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) and its related native species, Frankliniella intonsa (Pergande), fed with kidney bean leaves grown in ambient CO₂. The oviposition period, sex ratio, net reproductive rate (R₀), intrinsic rate of increase (r_m), and finite rate of increase (λ) of F. occidentalis increased in elevated CO₂, and larval duration, survival rate, mean generation time (T), and population doubling time (DT) decreased. For F. intonsa, larval duration, survival rate, oviposition period, longevity of female adults, R₀, r_m, and λ decreased in elevated CO₂, whereas sex ratio, T, and DT increased. These results indicated that the effects of elevated CO₂ would be beneficial to F. occidentalis, whereas it would be detrimental to F. intonsa. However, the effects of elevated CO₂ on F. occidentalis and F. intonsa differed over generations. In elevated CO₂, larval duration, survival rate, oviposition period, sex ratio, r_m, and λ of F. occidentalis increased linearly through successive generations, whereas T and DT decreased linearly, which suggested that the effects of elevated CO₂ on F. occidentalis would be slowly accentuated over time. For F. intonsa, larval duration, survival rate, oviposition period, r_m, and λ decreased linearly over generations, whereas sex ratio, T, and DT increased linearly. This indicated that the effects of elevated CO₂ on F. intonsa would slowly accentuate over time. We conclude that F. occidentalis would be more adapted to elevated CO₂ than F. intonsa.     

Tomato spotted wilt virus (TSWV) infection of Physcomitrella patens gametophores

Following mechanical inoculation of the moss Physcomitrella patens (Hedw.) B.S.G. with Tomato spotted wilt virus (TSWV), the virus encoded N nucleocapsid protein was detected in gametophores harvested 11 and 29 dpi and the non-structural NSm movement protein was observed 29 dpi. The detection of both viral proteins presumes that P. patens could serve as a new lab–host for TSWV, allowing reverse genetics by gene targeting to elucidate the role of specified molecular virus–host interactions.     

Cropping system influences Tomato spotted wilt virus disease development,thrips population and yield of tomato (Lycopersicon esculentum)

Yield of tomato is limited by many diseases including Tomato spotted wilt virus disease. This study was conducted in the field at Kenya Agriculture Research Institute Njoro, Kenya, in 2004 and 2006 to determine the effect of intercropping on disease development, thrips population and yield of tomato variety Cal J grown under four intercrop systems involving kale, onion, maize and sole tomato. The experimental design was a Randomised Complete Block Design (RCBD) replicated three times. Disease scores on tomato–maize differed significantly from tomato–kale and tomato–onion in both years of the study. Maize cropping system had a low significant thrips population from the other cropping systems. Tomato–maize intercrop produced the lowest fruit weights and marketable yield in 2004 and 2006, while yield of onion, kale and maize in intercrops were not significantly different from their monocrops. Land equivalent ratio was >1 in all the cropping systems.