The western flower thrips (Frankliniella occidentalis) is a polyphagous herbivore that causes serious damage to many agricultural plants. In addition to causing feeding damage, it is also a vector insect that transmits tospoviruses such as Tomato spotted wilt virus (TSWV). We previously reported that thrips feeding on plants induces a jasmonate (JA)-regulated plant defense, which negatively affects both the performance and preference (i.e. host plant attractiveness) of the thrips. The antagonistic interaction between a JA-regulated plant defense and a salicylic acid (SA)-regulated plant defense is well known. Here we report that TSWV infection allows thrips to feed heavily and multiply on Arabidopsis plants. TSWV infection elevated SA contents and induced SA-regulated gene expression in the plants. On the other hand, TSWV infection decreased the level of JA-regulated gene expression induced by thrips feeding. Importantly, we also demonstrated that thrips significantly preferred TSWV-infected plants to uninfected plants. In JA-insensitive coi1-1 mutants, however, thrips did not show a preference for TSWV-infected plants. In addition, SA application to wild-type plants increased their attractiveness to thrips. Our results suggest the following mechanism: TSWV infection suppresses the anti-herbivore response in plants and attracts its vector, thrips, to virus-infected plants by exploiting the antagonistic SA-JA plant defense systems.

Native insects can become epidemic pests in agro-ecosystems. A population genetics approach was applied to analyze the emergence and spread of outbreak populations of native insect species. Outbreaks of the mirid bug, Stenotus rubrovittatus, have rapidly expanded over Japan within the last two decades. To characterize the outbreak dynamics of this species, the genetic structure of local populations was assessed using polymorphisms of the mtDNA COI gene and six microsatellite loci. Results of the population genetic analysis suggested that S. rubrovittatus populations throughout Japan were genetically isolated by geographic distance and separated into three genetic clusters occupying spatially segregated regions. Phylogeographic analysis indicated that the genetic structure of S. rubrovittatus reflected post-glacial colonization. Early outbreaks of S. rubrovittatus in the 1980s occurred independently of genetically isolated populations. The genetic structure of the populations did not fit the pattern of an outbreak expansion, and therefore the data did not support the hypothesis that extensive outbreaks were caused by the dispersal of specific pestiferous populations. Rather, the historical genetic structure prior to the outbreaks was maintained throughout the increase in abundance of the mirid bug. Our study indicated that changes in the agro-environment induced multiple outbreaks of native pest populations. This implies that, given suitable environmental conditions, local populations may have the potential to outbreak even without invasion of populations from other environmentally degraded areas.

The phylogenetic relationships among 16 species including 10 thrips vector species of tospoviruses were analysed using partial sequences of three genes: mitochondrial COI, nuclear 28S ribosomal DNA and the elongation factor-1a (EF-1a) in order to reveal the influence of lineage among thrips vector species on the vector competence of tospoviruses. The phylogenetic trees of thrips suggested that distinct clades were formed between the genera Frankliniella and Thrips including vector species at least in combined nuclear DNA data, although COI data showed a similar result despite low bootstrap value in the root of Thrips clade. Scirtothrips had an ambiguous phylogenetic position in this study. Vector and non-vector species were found within the same clade in the genus Thrips. Compared with the phylogenetic tree of thrips, the virus phylogeny inferred from the nucleocapsid (N) protein sequence were likely to correspond to the phylogeny of thrips, genera Frankliniella, Thrips and Scirtothrips, respectively, and also to the primary host plants under natural conditions. These results suggested that the vector competence of thrips for tospoviruses might be influenced by the lineages of thrips vectors as well as host plants.

Five thrips species known as vectors of tospoviruses in Japan, Frankliniella occidentalis, F. intonsa, Thrips setosus, T. palmi and T. tabaci, were studied for their transmission competence of Impatiens necrotic spot virus (INSV). The competence was examined for adults that acquired the virus as newly hatched larvae using a petunia leaf disk assay. No members of the genus Thrips transmitted the virus; the INSV-N protein was not detected in them by DAS-ELISA. On the other hand, two species of the genus Frankliniella were confirmed as vectors of INSV. Both sexes of F. occidentalis transmitted the virus efficiently (males: 80.5%, females: 78.7%). In F. intonsa, however, the transmission efficiency was relatively low and differed between the sexes (males: 18.3%, females: 3.7%). Most F. occidentalis adults showing ELISA-positive values transmitted INSV; however, only one third of ELISA-positive F. intonsa adults did so. The amounts of the INSV-N protein in ELISA-positive and transmitting adults were larger in F. occidentalis than in F. intonsa by sex. These results show that the transmission of INSV may be characteristic of the genus Frankliniella, and that F. occidentalis is probably the primary vector of INSV in Japan.

The effect of tomato spotted wilt virus (TSWV) infection on the life span of thelytokous Thrips tabaci, which is known as a TSWV vector with a low transmission rate, was studied in two populations, Shimane (SM) and Iwate (IW). No effects of virus infection were found in the developmental period and mortality of the thrips before adult emergence, but a significant increase was observed in age-specific mortality during the adult lifespan of the TSWVexposed thrips group when compared with the non-exposed group (mean total longevity of thrips exposed and not exposed to virus was 18.1 and 20.1 d in the SM population and 19.9 and 21.5 d in the IW population). The latent period (LP) was 14.2 d in the SM population and 17.2 d in the IW population, indicating a relatively longer LP than the LPs reported for Frankliniella occidentalis and F. fusca. The potential transmission period (PTP) from the end of the LP to vector death was only 3.3 d in both of the populations. The higher the level of virus infection, the greater the reduction in adult thrips survival. These results suggest that a long LP and TSWV-induced reduction of thrips survival shorten the PTP. This may be responsible for the low transmissibility of TSWV as well as the low transmission rate in thelytokous T. tabaci populations.

No abstract

Frankliniella cephalica (Crawford) is an invasive species of thrips found in the islands of Yaeyama in the Okinawa Prefecture, Japan. During the late 1990s to early 2000s, a species of thrips was isolated from wild flowers of Bidens pilosa L. and Ipomoea batatas L. growing close to cultivated fields. They were subsequently identified as F. cephalica using fine morphological characteristics with the help of Steve Nakahara (U.S. Department of Agriculture, Beltsville, MD) and Laurence Mound (CSIRO, Australia). Voucher specimens were deposited in the Laboratory of Insect Resources, Faculty of Agriculture, Tokyo University of Agriculture by Shuji Okajima (2). We investigated the ability of F. cephalica to vector Tomato spotted wilt virus (TSWV) by experimentally determining virus transmission efficiency. Newly hatched larvae as much as 12 h old underwent a viral acquisition-access period (AAP) of 24 h, during which they fed on the leaves of Datura stramonium infected with TSWV-O, a Japanese type isolate. Transmission efficiency of adults 4 days after emergence from molt (14 days after the AAP) was determined by a petunia leaf disk assay (3) in which the adults were individually allowed to feed for successive 24-h inoculation access periods (IAP) on two different leaf disks of Petunia × hybrida cv. Polo Blue. Transmission of the virus by the adults was considered positive if at least one of the leaf disks showed viral necrotic spot. We tested 20 randomly selected leaf disks with clear necrotic spots using a simplified rapid immunofilter paper assay. All selected disks were positive for TWSV. The transmission efficiencies were 24.6% for female (n = 57) and 54.4% for male (n = 125) adults. The efficiency was significantly different between sexes (Fisher's exact probability test, P < 0.001). We also examined changes in the virus infection site at different developmental stages in thrips using immunofluorescence microscopy with a polyclonal antibody to N protein of the virus (4). After a 6-h AAP feeding by first instar larvae, the virus was found initially to infect the epithelial cells and then spread throughout the midgut tissue in the second instar larvae 5 days after acquisition of the virus. In viruliferous adults, the virus was present in the salivary glands and on the basement membrane of the midgut tissue. These data indicate that F. cephalica is a new insect vector for TSWV. F. cephalica is a major insect pest of tropical crops in tropical and subtropical coastal belts (1). The presence of a thrips vector in weed hosts surrounding cultivated fields might increase the chance of crops in this habitat becoming infected with viruses. References: (1) M. Lamberts and J. H. Crane. Page 337 in: Advances in New Crops. J. Janick and J. E. Simon, eds. Timber Press, Portland, OR, 1990. (2) M. Masumoto and S. Okajima. Jpn. J. Appl. Entomol. Zool. 48:225, 2004. (3) T. Sakurai et al. Appl. Entomol. Zool. 39:71, 2004. (4) S. Tsuda et al. Ann. Phytopathol. Soc. Jpn. 60:216, 1994.

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.