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1.  Effect of Watermelon Silver Mottle Virus on the Life History and Feeding Preference of Thrips palmi 
PLoS ONE  2014;9(7):e102021.
Thrips-borne tospoviruses cause numerous plant diseases that produce severe economic losses worldwide. In the disease system, thrips not only damage plants through feeding but also transmit causative agents of epidemics. In addition, thrips are infected with tospoviruses in the course of virus transmission. Most studies on the effect of tospoviruses on vector thrips have focused on the Tomato spotted wilt virus–Frankliniella occidentalis system. Thus, we focused on another thrips-borne tospovirus, Watermelon silver mottle virus (WSMoV), to examine the effect of virus infection on its vector, Thrips palmi. In this study, the direct and indirect effects of WSMoV on the life history traits and feeding preference of T. palmi were examined. The survival rate and developmental time of the WSMoV-infected larval thrips did not differ significantly from those of the virus-free thrips. Comparing the developmental time of larval thrips fed on the healthy plants, thrips-damaged plants, and thrips-inoculated plants (the WSMoV-infected plants caused by thrips feeding), feeding on the thrips-damaged plants reduced the developmental time, and the WSMoV infection in host plants partially canceled the effect of thrips damage on the developmental time. In addition, no significant variations between the virus-free and WSMoV-infected adult thrips regarding longevity and fecundity were observed. These results implied that WSMoV did not directly affect the life history traits of T. palmi, but the WSMoV infection indirectly affected the development of T. palmi through the virus-infected plants. Furthermore, feeding preference tests indicated that T. palmi preferred feeding on either the thrips-damaged plants or the thrips-inoculated plants to the healthy plants. The effect of tospoviruses on the life history and feeding preference of vector thrips might vary among host plants, virus species, vector species, and environmental factors.
PMCID: PMC4092097  PMID: 25010157
2.  Arabidopsis-thrips system for analysis of plant response to insect feeding 
Plant Signaling & Behavior  2008;3(7):446-447.
Insect feeding retards plant growth and decreases crop productivity. Plants respond to insect feeding at the molecular, cellular and physiological levels. The roles of the plant hormones jasmonic acid (JA), ethylene (ET) and salicylic acid (SA) in plant responses to insect feeding have been studied. However, these studies are focused on the plant responses to feeding by well-studied caterpillar type insects or aphid pests. In contrast, we have focused on a minute insect pest, the western flower thrips (Frankliniella occidentalis). Analyses of the responses of hormone-related mutants of Arabidopsis (i.e., JA-insensitive mutant coi1-1, ET-insensitive mutants ein2-1 and ein3-1, and SA-deficient mutant eds16-1) and transcriptome-based comparative analyses indicate the central role of JA in plant responses to thrips feeding. Our work clearly shows that JA signaling, but not JA/ET signaling, is involved in plant tolerance to thrips feeding. We intend to examine the utility and suitability of the Arabidopsis-thrips system in studies of plant responses to insect feeding.
PMCID: PMC2634423  PMID: 19704479
Arabidopsis thaliana; ethylene; Frankliniella occidentalis; insect feeding; jasmonate; western flower thrips
3.  Correlations between Colonization of Onion Thrips and Leaf Reflectance Measures across Six Cabbage Varieties 
PLoS ONE  2013;8(9):e73848.
The main purpose of this study was to reveal if the UV-A, and visible light reflection of leaves of white cabbage varieties is correlated to resistance against onion thrips. The antixenotic resistance (AR) against onion thrips and thrips damage differed between varieties Balashi, Bloktor, Riana – considered resistant – and Green Gem, Hurricane, Quisor – considered susceptible. The solar UV-A (340–400 nm) and visible (401–650 nm) light reflection of white cabbage leaves were recorded. Correlation between AR against onion thrips and reflection of leaves in UV-A and visible range of the studied white cabbage varieties were computed. According to the AR evaluation onion thrips density was always higher on susceptible than on resistant varieties. The UV-A light reflection of head forming leaves and the contrast between head and exterior leaves (H/E) was negatively correlated with onion thrips host preference at an early stage of cabbage head formation. The visible light reflection of both head forming and exterior leaves was also negatively correlated with onion thrips host preference. Susceptible varieties had greater damage ratings at harvest than resistant ones and positive correlations were observed between AR and damage. AR against onion thrips may be affected by differences in reflection of cabbage leaves at an early growth stage. It is suggested that more intensive reflection of leaves and/or higher contrast values between the reflectance intensity of head versus outer leaves made the resistant varieties less attractive to onion thrips. Our results reported here provide the first evidence of negative correlation between UV-A and visible reflection of leaves and AR of white cabbage against a dangerous insect pest, opening new perspectives for understanding the role of reflection by plant leaves in pest management.
PMCID: PMC3764121  PMID: 24040093
4.  Selenium hyperaccumulation offers protection from cell disruptor herbivores 
BMC Ecology  2010;10:19.
Hyperaccumulation, the rare capacity of certain plant species to accumulate toxic trace elements to levels several orders of magnitude higher than other species growing on the same site, is thought to be an elemental defense mechanism against herbivores and pathogens. Previous research has shown that selenium (Se) hyperaccumulation protects plants from a variety of herbivores and pathogens. Selenium hyperaccumulating plants sequester Se in discrete locations in the leaf periphery, making them potentially more susceptible to some herbivore feeding modes than others. In this study we investigate the protective function of Se in the Se hyperaccumulators Stanleya pinnata and Astragalus bisulcatus against two cell disrupting herbivores, the western flower thrips (Frankliniella occidentalis) and the two-spotted spider mite (Tetranychus urticae).
Astragalus bisulcatus and S. pinnata with high Se concentrations (greater than 650 mg Se kg-1) were less subject to thrips herbivory than plants with low Se levels (less than 150 mg Se kg-1). Furthermore, in plants containing elevated Se levels, leaves with higher concentrations of Se suffered less herbivory than leaves with less Se. Spider mites also preferred to feed on low-Se A. bisulcatus and S. pinnata plants rather than high-Se plants. Spider mite populations on A. bisulcatus decreased after plants were given a higher concentration of Se. Interestingly, spider mites could colonize A. bisulcatus plants containing up to 200 mg Se kg-1 dry weight, concentrations which are toxic to many other herbivores. Selenium distribution and speciation studies using micro-focused X-ray fluorescence (μXRF) mapping and Se K-edge X-ray absorption spectroscopy revealed that the spider mites accumulated primarily methylselenocysteine, the relatively non-toxic form of Se that is also the predominant form of Se in hyperaccumulators.
This is the first reported study investigating the protective effect of hyperaccumulated Se against cell-disrupting herbivores. The finding that Se protected the two hyperaccumulator species from both cell disruptors lends further support to the elemental defense hypothesis and increases the number of herbivores and feeding modes against which Se has shown a protective effect. Because western flower thrips and two-spotted spider mites are widespread and economically important herbivores, the results from this study also have potential applications in agriculture or horticulture, and implications for the management of Se-rich crops.
PMCID: PMC2940900  PMID: 20799959
5.  Habituation in Frankliniella occidentalis to deterrent plant compounds and their blends 
Feeding and oviposition deterrence of three secondary plant compounds and their 1:1 blends to adult female Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) and the potential for habituation of the thrips to the pure compounds and the 1:1 blends at various concentrations were investigated. In choice assays, we tested dose‐dependent feeding and oviposition deterrence of the two fatty acid derivatives methyl jasmonate and cis‐jasmone, the phenylpropanoid allylanisole, and their blends when directly applied to bean leaf discs. The concentration required to reduce the feeding damage by 50% relative to the control treatment (FDC50) was lowest for cis‐jasmone and highest for allylanisole. The feeding deterrent effect of both jasmonates was increased when blended with allylanisole. Feeding deterrence and oviposition deterrence were strongly correlated. In no‐choice assays conducted over four consecutive days, we discovered that dilutions at low concentrations (FDC15) applied to bean leaves resulted in habituation to the deterrents, whereas no habituation occurred at higher concentrations (FDC50). We observed a tendency that the 1:1 blends reduce the probability that thrips habituate to the deterrent compounds. Our results may be useful in the development of integrated crop protection strategies with the implementation of allelochemicals as pest behaviour‐modifying agents.
PMCID: PMC4164025  PMID: 25253898
Western flower thrips; secondary plant compound; feeding deterrence; methyl jasmonate; cis‐jasmone; allylanisole; Thysanoptera; Thripidae
6.  Thysanoptera (Thrips) Within Citrus Orchards in Florida: Species Distribution, Relative and Seasonal Abundance Within Trees, and Species on Vines and Ground Cover Plants 
Seven citrus orchards on reduced to no pesticide spray programs were sampled for Thysanoptera in central and south central Florida. Inner and outer canopy leaves, fruits, twigs, trunk scrapings, vines and ground cover plants were sampled monthly between January 1995 and January 1996. Thirty-six species of thrips were identified from 2,979 specimens collected from within citrus tree canopies and 18,266 specimens from vines and ground cover plants within the seven citrus orchards. The thrips species included seven predators [Aleurodothrips fasciapennis (Franklin), Karnyothrips flavipes (Jones), K. melaleucus (Bagnall), Leptothrips cassiae (Watson), L. macroocellatus (Watson), L. pini (Watson), and Scolothrips sexmaculatus (Pergande)] 21 plant feeding species [Anaphothrips n. sp., Arorathrips mexicanus (Crawford), Aurantothrips orchidaceous (Bagnall), Baileyothrips limbatus (Hood), Chaetanaphothrips orchidii (Moulton), Danothrips trifasciatus (Sakimura), Echinothrips americanus (Morgan), Frankliniella bispinosa (Morgan), F. cephalica (Crawford), F. fusca (Hinds), F. gossypiana (Hood), Frankliniella sp. (runneri group), Haplothrips gowdeyi (Franklin), Heliothrips haemorrhoidalis (Bouché), Leucothrips piercei (Morgan), Microcephalothrips abdominalis (Crawford), Neohydatothrips floridanus (Watson), N. portoricensis (Morgan), Pseudothrips inequalis (Beach), Scirtothrips sp., and Thrips hawaiiensis (Morgan)]; and eight fungivorous feeding species [Adraneothrips decorus (Hood), Hoplandrothrips pergandei (Hinds), Idolothripinae sp., Merothrips floridensis (Watson), M. morgani (Hood), Neurothrips magnafemoralis (Hinds), Stephanothrips occidentalis Hood and Williams, and Symphyothrips sp.]. Only F. bispinosa, C. orchidii, D. trifasciatus, and H. haemorrhoidalis have been considered economic pests on Florida citrus. Scirtothrips sp. and T. hawaiiensis were recovered in low numbers within Florida citrus orchards. Both are potential pest species to citrus and possibly other crops in Florida. The five most abundant thrips species collected within citrus tree canopies were: A. fasciapennis, F. bispinosa, C. orchidii, K. flavipes, and D. trifasciatus. In comparison, the following five thrips species were most abundant on vines or ground cover plants: F. bispinosa, H. gowdeyi, F. cephalica, M. abdominalis, and F. gossypiana. Fifty-eight species of vines or ground cover plants in 26 families were infested with one or more of 27 species of thrips.
PMCID: PMC2990331  PMID: 20233100
Thrips; Terebrantia; Phlaeothripinae; Idolothripinae; Thripidae; Phlaeothripidae
7.  Analysis of the Salivary Gland Transcriptome of Frankliniella occidentalis 
PLoS ONE  2014;9(4):e94447.
Saliva is known to play a crucial role in insect feeding behavior and virus transmission. Currently, little is known about the salivary glands and saliva of thrips, despite the fact that Frankliniella occidentalis (Pergande) (the western flower thrips) is a serious pest due to its destructive feeding, wide host range, and transmission of tospoviruses. As a first step towards characterizing thrips salivary gland functions, we sequenced the transcriptome of the primary salivary glands of F. occidentalis using short read sequencing (Illumina) technology. A de novo-assembled transcriptome revealed 31,392 high quality contigs with an average size of 605 bp. A total of 12,166 contigs had significant BLASTx or tBLASTx hits (E≤1.0E−6) to known proteins, whereas a high percentage (61.24%) of contigs had no apparent protein or nucleotide hits. Comparison of the F. occidentalis salivary gland transcriptome (sialotranscriptome) against a published F. occidentalis full body transcriptome assembled from Roche-454 reads revealed several contigs with putative annotations associated with salivary gland functions. KEGG pathway analysis of the sialotranscriptome revealed that the majority (18 out of the top 20 predicted KEGG pathways) of the salivary gland contig sequences match proteins involved in metabolism. We identified several genes likely to be involved in detoxification and inhibition of plant defense responses including aldehyde dehydrogenase, metalloprotease, glucose oxidase, glucose dehydrogenase, and regucalcin. We also identified several genes that may play a role in the extra-oral digestion of plant structural tissues including β-glucosidase and pectin lyase; and the extra-oral digestion of sugars, including α-amylase, maltase, sucrase, and α-glucosidase. This is the first analysis of a sialotranscriptome for any Thysanopteran species and it provides a foundational tool to further our understanding of how thrips interact with their plant hosts and the viruses they transmit.
PMCID: PMC3988053  PMID: 24736614
8.  The Green Lacewing, Chrysoperla carnea: Preference between Lettuce Aphids, Nasonovia ribisnigri, and Western Flower Thrips, Frankliniella occidentalis 
This study investigated the prey preference of 3rd instar green lacewing, Chrysoperla carnea Stephens (Neuroptera: Chrysopidae), between western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), and lettuce aphids, Nasonovia ribisnigri (Mosley) (Hemiptera: Aphididae) in laboratory experiments at 25 ± 1° C and 70 ± 5% RH with five prey ratios (10 aphids:80 thrips, 25 aphids:65 thrips, 45 aphids:45 thrips, 65 aphids:25 thrips, and 80 aphids:10 thrips). Third instar C. carnea larvae readily preyed upon both thrips and aphids, with thrips mortality varying between 40 and 90%, and aphid mortality between 52 and 98%. Chrysoperla carnea had a significant preference for N. ribisnigri at two ratios (10 aphids:80 thrips, 65 aphids:25 thrips), but no preference for either prey at the other ratios. There was no significant linear relationship between preference index and prey ratio, but a significant intercept of the linear regression indicated an overall preference of C. carnea for aphids with a value of 0.651 ± 0.054. The possible implications of these findings for control of N. ribisnigri and F. occidentalis by C. carnea are discussed.
PMCID: PMC3835039  PMID: 24205864
Aphididae; biological control; Chrysopidae; prey ratios; Thripidae
9.  Juvenile prey induce antipredator behaviour in adult predators 
Experimental & Applied Acarology  2012;59(3):275-282.
It is generally assumed that the choice of oviposition sites in arthropods is affected by the presence of food for the offspring on the one hand and by predation risk on the other hand. But where should females oviposit when the food itself poses a predation risk for their offspring? Here, we address this question by studying the oviposition behaviour of the predatory mite Amblyseius swirskii in reaction to the presence of its counterattacking prey, the western flower thrips Frankliniella occidentalis. We offered the mites a choice between two potential oviposition sites, one with and one without food. We used two types of food: thrips larvae, which are predators of eggs of predatory mite but are consumed by older predator stages, and pollen, a food source that poses no risk to the predators. With pollen as food, the predators preferred ovipositing on the site with food. This might facilitate the foraging for food by the immature offspring that will emerge from the eggs. With thrips as food, female predators preferred ovipositing on the site without thrips. Predators that oviposited more on the site with thrips larvae killed more thrips larvae than females that oviposited on the site without food, but this did not result in higher oviposition. This suggests that the females killed thrips to protect their offspring. Our results show that predators display complex anti-predator behaviour in response to the presence of counter-attacking prey.
PMCID: PMC3557378  PMID: 22923143
Phytoseiids; Thrips; Oviposition site selection; Role reversals; Predator–prey interactions; Counterattacking prey; Amblyseius swirskii
10.  Can Mass Trapping Reduce Thrips Damage and Is It Economically Viable? Management of the Western Flower Thrips in Strawberry 
PLoS ONE  2013;8(11):e80787.
The western flower thrips Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) is a cosmopolitan, polyphagous insect pest that causes bronzing to fruit of strawberry (Fragaria x ananassa). The main aim of this study was to test whether mass trapping could reduce damage and to predict whether this approach would be economically viable. In semi-protected strawberry crops, mass trapping of F. occidentalis using blue sticky roller traps reduced adult thrips numbers per flower by 61% and fruit bronzing by 55%. The addition of the F. occidentalis aggregation pheromone, neryl (S)-2-methylbutanoate, to the traps doubled the trap catch, reduced adult thrips numbers per flower by 73% and fruit bronzing by 68%. The factors affecting trapping efficiency through the season are discussed. Damage that would result in downgrading of fruit to a cheaper price occurred when bronzing affected about 10% of the red fruit surface. Cost-benefit analysis using this threshold showed that mass trapping of thrips using blue sticky roller traps can be cost-effective in high-value crops. The addition of blue sticky roller traps to an integrated pest management programme maintained thrips numbers below the damage threshold and increased grower returns by a conservative estimate of £2.2k per hectare. Further work is required to develop the F. occidentalis aggregation pheromone for mass trapping and to determine the best timing for trap deployment. Mass trapping of thrips is likely to be cost-effective in other countries and other high-value crops affected by F. occidentalis damage, such as cucumber and cut flowers.
PMCID: PMC3839998  PMID: 24282554
11.  Silicon reduces impact of plant nitrogen in promoting stalk borer (Eldana saccharina) but not sugarcane thrips (Fulmekiola serrata) infestations in sugarcane 
The stalk borer Eldana saccharina Walker (Lepidoptera: Pyralidae) is a major limiting factor in South African sugarcane production, while yield is also reduced by sugarcane thrips Fulmekiola serrata Kobus (Thysanoptera: Thripidae). Borer management options include appropriate nitrogen (N) and enhanced silicon (Si) nutrition; the effect of N on sugarcane thrips is unknown. We tested the effects of these nutrients, in combination with resistant (N33) and susceptible (N27) sugarcane cultivars, on E. saccharina and F. serrata infestation. Two pot trials with three levels of N (60, 120, and 180 kg ha-1) and two levels each of calcium silicate and dolomitic lime (5 and 10 t ha-1) were naturally infested with thrips, then artificially water stressed and infested with borer. Higher N levels increased borer survival and stalk damage, while Si reduced these compared with controls. Silicon significantly reduced stalk damage in N27 but not in N33; hence, Si provided relatively greater protection for susceptible cultivars than for resistant ones. High N treatments were associated with greater thrips numbers, while Si treatments did not significantly influence thrips infestation. The reduction in borer survival and stalk damage by Si application at all N rates indicates that under field conditions, the opportunity exists for optimizing sugarcane yields through maintaining adequate N nutrition, while reducing populations of E. saccharina using integrated pest management (IPM) tactics that include improved Si nutrition of the crop and reduced plant water stress. Improved management of N nutrition may also provide an option for thrips IPM. The contrasting effects of Si on stalk borer and thrips indicate that Si-mediated resistance to insect herbivores in sugarcane has mechanical and biochemical components that are well developed in the stalk tissues targeted by E. saccharina but poorly developed in the young leaf spindles where F. serrata occurs.
PMCID: PMC4064666  PMID: 24999349
plant nutrition; nitrogen fertilizer; sugarcane cultivars; calcium silicate; integrated pest management; silicon-mediated resistance; thrips; stalk borer
12.  Behavioural responses of Frankliniella occidentalis Pergande larvae to methyl jasmonate and cis-jasmone 
Journal of Pest Science  2013;87(1):53-59.
The larval stages of Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) cause more direct feeding damage to plants than the adults. We, therefore, investigated the behaviour-modifying effects on second instar larvae of two jasmonic acid derivatives. The artificial application of methyl jasmonate and cis-jasmone, both at 1 % concentration, deterred the larvae from settling in a dual choice bean leaf disc assay. We observed a dose-dependent feeding deterrence of both jasmonates and calculated the concentration required to reduce the feeding damage by 50 % relative to the control treatment (FDC50) for each jasmonate. The feeding damage was reduced by the application of cis-jasmone at 1 % concentration, but not by the jasmonates at the respective FDC50 in no-choice leaf disc bioassays. However, significantly more larvae left jasmonate-treated whole potted bean plants by migrating to the soil compared with control plants. Our results may be exploited extending behavioural manipulation by using plant compounds in thrips control programmes to the full lifecycle of the pest. Plant compounds could be used in integrated and biological pest management strategies against F. occidentalis in combination with the application of various above and below ground control measures.
PMCID: PMC3925295  PMID: 24563647
Thrips; Second instar; Secondary plant compounds; Jasmonates; Feeding deterrent; Leaving behaviour
13.  Species limits, quarantine risk and the intrigue of a polyphagous invasive pest with highly restricted host relationships in its area of invasion 
Evolutionary Applications  2013;6(8):1195-1207.
Scirtothrips aurantii is a generalist horticultural pest in its native African range and recently established quite widely in Australia on the invasive succulent weed Bryophyllum delagoense. Paradoxically, this thrips is not polyphagous in its incursive range. The issue is principally one of quarantine. Will the thrips in Australia shift, perhaps adaptively, to citrus, and should the primary focus be on containment around Australian citrus, or does the real quarantine risk exist offshore with thrips present on citrus in Africa? We examined the phylogenetic relationships between Bryophyllum-associated thrips populations in Australia and populations sampled from various host plant species in South Africa (including Bryophyllum) using both CO1 and 28s markers. Eight variable microsatellite markers were developed to assess the extent of gene flow between the thrips on different hosts in South Africa. The COI phylogeny resolved S. aurantii into three distinct clades with samples collected from B. delagoense in South Africa and Australia representing a single clade, a second clade associated with Gloriosa lilies and the third with horticultural hosts. The microsatellite analysis confirmed that the populations associated with citrus and Bryophyllum do not hybridize with one another in sympatry. We conclude that the citrus-damaging thrips are not currently present in Australia and remain a serious quarantine concern in relation to Australian horticulture.
PMCID: PMC3901549  PMID: 24478801
28S; Bryophyllum delagoense; citrus; COI; cryptic species; gene flow; microsatellite; quarantine; Scirtothrips aurantii
14.  Coronatine-Insensitive 1 (COI1) Mediates Transcriptional Responses of Arabidopsis thaliana to External Potassium Supply 
Molecular Plant  2010;3(2):390-405.
The ability to adjust growth and development to the availability of mineral nutrients in the soil is an essential life skill of plants but the underlying signaling pathways are poorly understood. In Arabidopsis thaliana, shortage of potassium (K) induces a number of genes related to the phytohormone jasmonic acid (JA). Using comparative microarray analysis of wild-type and coi1-16 mutant plants, we classified transcriptional responses to K with respect to their dependence on COI1, a central component of oxylipin signaling. Expression profiles obtained in a short-term experiment clearly distinguished between COI1-dependent and COI1-independent K-responsive genes, and identified both known and novel targets of JA-COI1-signaling. During long-term K-deficiency, coi-16 mutants displayed de novo responses covering similar functions as COI1-targets except for defense. A putative role of JA for enhancing the defense potential of K-deficient plants was further supported by the observation that plants grown on low K were less damaged by thrips than plants grown with sufficient K.
PMCID: PMC2845782  PMID: 20339157
Hormonal regulation; nutrition; secondary metabolism/natural products; transcriptome analysis; plant–insect interactions; Arabidopsis
15.  Phytophagous Arthropods and a Pathogen Sharing a Host Plant: Evidence for Indirect Plant-Mediated Interactions 
PLoS ONE  2011;6(5):e18840.
In ecological systems, indirect interactions between plant pathogens and phytophagous arthropods can arise when infestation by a first attacker alters the common host plant so that although a second attacker could be spatially or temporally separated from the first one, the former could be affected. The induction of plant defense reactions leading to the production of secondary metabolites is thought to have an important role since it involves antagonistic and/or synergistic cross-talks that may determine the outcome of such interactions. We carried out experiments under controlled conditions on young rose plants in order to assess the impact of these indirect interactions on life history traits of three pests: the necrotrophic fungus Botrytis cinerea Pers.: Fr. (Helotiales: Sclerotiniaceae), the aphid Rhodobium porosum Sanderson (Hemiptera: Aphididae) and the thrips Frankliniella occidentalis Pergande (Thysanoptera: Thripidae). Our results indicated (i) a bi-directional negative interaction between B. cinerea and R. porosum, which is conveyed by decreased aphid growth rate and reduced fungal lesion area, as well as (ii) an indirect negative effect of B. cinerea on insect behavior. No indirect effect was observed between thrips and aphids. This research highlights several complex interactions that may be involved in structuring herbivore and plant pathogen communities within natural and managed ecosystems.
PMCID: PMC3097179  PMID: 21611161
16.  Proteomic Analysis of Frankliniella occidentalis and Differentially Expressed Proteins in Response to Tomato Spotted Wilt Virus Infection 
Journal of Virology  2012;86(16):8793-8809.
Tomato spotted wilt virus (TSWV) is transmitted by Frankliniella occidentalis in a persistent propagative manner. Despite the extensive replication of TSWV in midgut and salivary glands, there is little to no pathogenic effect on F. occidentalis. We hypothesize that the first-instar larva (L1) of F. occidentalis mounts a response to TSWV that protects it from pathogenic effects caused by virus infection and replication in various insect tissues. A partial thrips transcriptome was generated using 454-Titanium sequencing of cDNA generated from F. occidentalis exposed to TSWV. Using these sequences, the L1 thrips proteome that resolved on a two-dimensional gel was characterized. Forty-seven percent of the resolved protein spots were identified using the thrips transcriptome. Real-time quantitative reverse transcriptase PCR (RT-PCR) analysis of virus titer in L1 thrips revealed a significant increase in the normalized abundance of TSWV nucleocapsid RNA from 2 to 21 h after a 3-h acquisition access period on virus-infected plant tissue, indicative of infection and accumulation of virus. We compared the proteomes of infected and noninfected L1s to identify proteins that display differential abundances in response to virus. Using four biological replicates, 26 spots containing 37 proteins were significantly altered in response to TSWV. Gene ontology assignments for 32 of these proteins revealed biological roles associated with the infection cycle of other plant- and animal-infecting viruses and antiviral defense responses. Our findings support the hypothesis that L1 thrips display a complex reaction to TSWV infection and provide new insights toward unraveling the molecular basis of this interaction.
PMCID: PMC3421711  PMID: 22696645
17.  Foraging on Individual Leaves by an Intracellular Feeding Insect Is Not Associated with Leaf Biomechanical Properties or Leaf Orientation 
PLoS ONE  2013;8(11):e80911.
Nearly all herbivorous arthropods make foraging-decisions on individual leaves, yet systematic investigations of the adaptive significance and ecological factors structuring these decisions are rare with most attention given to chewing herbivores. This study investigated why an intracellular feeding herbivore, Western flower thrips (WFT) Frankliniella occidentalis Pergande, generally avoids feeding on the adaxial leaf surface of cotton cotyledons. WFT showed a significant aversion to adaxial-feeding even when excised-cotyledons were turned up-side (abaxial-side ‘up’), suggesting that negative-phototaxis was not a primary cause of thrips foraging patterns. No-choice bioassays in which individual WFT females were confined to either the abaxial or adaxial leaf surface showed that 35% fewer offspring were produced when only adaxial feeding was allowed, which coincided with 32% less plant feeding on that surface. To test the hypothesis that leaf biomechanical properties inhibited thrips feeding on the adaxial surface, we used a penetrometer to measure two variables related to the ‘toughness’ of each leaf surface. Neither variable negatively co-varied with feeding. Thus, while avoiding the upper leaf surface was an adaptive foraging strategy, the proximate cause remains to be elucidated, but is likely due, in part, to certain leaf properties that inhibit feeding.
PMCID: PMC3829965  PMID: 24260510
18.  Taqman real-time quantitative PCR for identification of western flower thrip (Frankliniella occidentalis) for plant quarantine 
Biology Letters  2010;6(4):555-557.
Western flower thrip (Frankliniella occidentalis) is a major global pest of agricultural products. It directly damages crops through feeding, oviposition activity or transmission of several plant viruses. We describe a Taqman real-time quantitative PCR detection system, which can rapidly identify F. occidentalis from thrips larvae to complement the traditional morphological identification. The data showed that our detection system targeted on the ribosomal RNA gene regions of F. occidentalis has high sensitivity and specificity. The rapid method can be used for on-site testing of samples at ports-of-entry in the future.
PMCID: PMC2936211  PMID: 20129946
Frankliniella occidentalis; real-time quantitative PCR; plant quarantine
19.  Prey Preference of the Predatory Mite, Amblyseius swirskii between First Instar Western Flower Thrips Frankliniella occidentalis and Nymphs of the Twospotted Spider Mite Tetranychus urticae  
The prey preference of polyphagous predators plays an important role in suppressing different species of pest insects. In this study the prey preference of the predatory mite, Amblyseius swirskii (Athias-Henriot) (Acari: Phytoseiidae) was examined between nymphs of the twospotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae) and first instar larvae of the western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), as well as between active and chrysalis spider mite protonymphs and active and chrysalis spider mite deutonymphs. The study was done in the laboratory on bean leaf discs at 25 ± 1° C and 70 ± 5% RH. Amblyseius swirskii had a clear preference for thrips compared to both spider mite protonymphs and deutonymphs. About twice as many thrips as spider mites were consumed. Amblyseius swirskii did not show a preference between active and chrysalis stages of spider mites.
PMCID: PMC3016914  PMID: 21070175
polyphagous; biological control
20.  Invasion Genetics of the Western Flower Thrips in China: Evidence for Genetic Bottleneck, Hybridization and Bridgehead Effect 
PLoS ONE  2012;7(4):e34567.
The western flower thrips, Frankliniella occidentalis (Pergande), is an invasive species and the most economically important pest within the insect order Thysanoptera. F. occidentalis, which is endemic to North America, was initially detected in Kunming in southwestern China in 2000 and since then it has rapidly invaded several other localities in China where it has greatly damaged greenhouse vegetables and ornamental crops. Controlling this invasive pest in China requires an understanding of its genetic makeup and migration patterns. Using the mitochondrial COI gene and 10 microsatellites, eight of which were newly isolated and are highly polymorphic, we investigated the genetic structure and the routes of range expansion of 14 F. occidentalis populations in China. Both the mitochondrial and microsatellite data revealed that the genetic diversity of F. occidentalis of the Chinese populations is lower than that in its native range. Two previously reported cryptic species (or ecotypes) were found in the study. The divergence in the mitochondrial COI of two Chinese cryptic species (or ecotypes) was about 3.3% but they cannot be distinguished by nuclear markers. Hybridization might produce such substantial mitochondrial-nuclear discordance. Furthermore, we found low genetic differentiation (global FST = 0.043, P<0.001) among all the populations and strong evidence for gene flow, especially from the three southwestern populations (Baoshan, Dali and Kunming) to the other Chinese populations. The directional gene flow was further supported by the higher genetic diversity of these three southwestern populations. Thus, quarantine and management of F. occidentalis should focus on preventing it from spreading from the putative source populations to other parts of China.
PMCID: PMC3317996  PMID: 22509325
21.  Identification of the Aggregation Pheromone of the Melon Thrips, Thrips palmi 
PLoS ONE  2014;9(8):e103315.
The objective of this study was to identify the aggregation pheromone of the melon thrips Thrips palmi, a major pest of vegetable and ornamental plants around the world. The species causes damage both through feeding activities and as a vector of tospoviruses, and is a threat to world trade and European horticulture. Improved methods of detecting and controlling this species are needed and the identification of an aggregation pheromone will contribute to this requirement. Bioassays with a Y-tube olfactometer showed that virgin female T. palmi were attracted to the odour of live males, but not to that of live females, and that mixed-age adults of both sexes were attracted to the odour of live males, indicating the presence of a male-produced aggregation pheromone. Examination of the headspace volatiles of adult male T. palmi revealed only one compound that was not found in adult females. It was identified by comparison of its mass spectrum and chromatographic details with those of similar compounds. This compound had a structure like that of the previously identified male-produced aggregation pheromone of the western flower thrips Frankliniella occidentalis. The compound was synthesised and tested in eggplant crops infested with T. palmi in Japan. Significantly greater numbers of both males and females were attracted to traps baited with the putative aggregation pheromone compared to unbaited traps. The aggregation pheromone of T. palmi is thus identified as (R)-lavandulyl 3-methyl-3-butenoate by spectroscopic, chromatographic and behavioural analysis.
PMCID: PMC4125133  PMID: 25101871
22.  The NSs Protein of Tomato spotted wilt virus Is Required for Persistent Infection and Transmission by Frankliniella occidentalis 
Journal of Virology  2014;88(10):5788-5802.
Tomato spotted wilt virus (TSWV) is the type member of tospoviruses (genus Tospovirus), plant-infecting viruses that cause severe damage to ornamental and vegetable crops. Tospoviruses are transmitted by thrips in the circulative propagative mode. We generated a collection of NSs-defective TSWV isolates and showed that TSWV coding for truncated NSs protein could not be transmitted by Frankliniella occidentalis. Quantitative reverse transcription (RT)-PCR and immunostaining of individual insects detected the mutant virus in second-instar larvae and adult insects, demonstrating that insects could acquire and accumulate the NSs-defective virus. Nevertheless, adults carried a significantly lower viral load, resulting in the absence of transmission. Genome sequencing and analyses of reassortant isolates showed genetic evidence of the association between the loss of competence in transmission and the mutation in the NSs coding sequence. Our findings offer new insight into the TSWV-thrips interaction and Tospovirus pathogenesis and highlight, for the first time in the Bunyaviridae family, a major role for the S segment, and specifically for the NSs protein, in virulence and efficient infection in insect vector individuals.
IMPORTANCE Our work is the first to show a role for the NSs protein in virus accumulation in the insect vector in the Bunyaviridae family: demonstration was obtained for the system TSWV-F. occidentalis, arguably one of the most damaging combination for vegetable crops. Genetic evidence of the involvement of the NSs protein in vector transmission was provided with multiple approaches.
PMCID: PMC4019118  PMID: 24623427
23.  Onset of herbivore-induced resistance in systemic tissue primed for jasmonate-dependent defenses is activated by abscisic acid 
In Arabidopsis, the MYC2 transcription factor on the one hand and the AP2/ERF transcription factors ORA59 and ERF1 on the other hand regulate distinct branches of the jasmonic acid (JA) signaling pathway in an antagonistic fashion, co-regulated by abscisic acid (ABA) and ethylene, respectively. Feeding by larvae of the specialist herbivorous insect Pieris rapae (small cabbage white butterfly) results in activation of the MYC-branch and concomitant suppression of the ERF-branch in insect-damaged leaves. Here we investigated differential JA signaling activation in undamaged systemic leaves of P. rapae-infested plants. We found that the MYC2 transcription factor gene was induced both in the local insect-damaged leaves and the systemic undamaged leaves of P. rapae-infested Arabidopsis plants. However, in contrast to the insect-damaged leaves, the undamaged tissue did not show activation of the MYC-branch marker gene VSP1. Comparison of the hormone signal signature revealed that the levels of JA and (+)-7-iso-jasmonoyl-L-isoleucine raised to similar extents in locally damaged and systemically undamaged leaves, but the production of ABA and the JA precursor 12-oxo-phytodienoic acid was enhanced only in the local herbivore-damaged leaves, and not in the distal undamaged leaves. Challenge of undamaged leaves of pre-infested plants with either P. rapae larvae or exogenously applied ABA led to potentiated expression levels of MYC2 and VSP1, with the latter reaching extremely high expression levels. Moreover, P. rapae-induced resistance, as measured by reduction of caterpillar growth on pre-infested plants, was blocked in the ABA biosynthesis mutant aba2-1, that was also impaired in P. rapae-induced expression of VSP1. Together, these results suggest that ABA is a crucial regulator of herbivore-induced resistance by activating primed JA-regulated defense responses upon secondary herbivore attack in Arabidopsis.
PMCID: PMC3874679  PMID: 24416038
abscisic acid; jasmonic acid; priming; systemic defense; Pieris rapae; MYC2
24.  Herbivore benefits from vectoring plant virus through reduction of period of vulnerability to predation 
Oecologia  2008;156(4):797-806.
Herbivores can profit from vectoring plant pathogens because the induced defence of plants against pathogens sometimes interferes with the induced defence of plants against herbivores. Plants can also defend themselves indirectly by the action of the natural enemies of the herbivores. It is unknown whether the defence against pathogens induced in the plant also interferes with the indirect defence against herbivores mediated via the third trophic level. We previously showed that infection of plants with Tomato spotted wilt virus (TSWV) increased the developmental rate of and juvenile survival of its vector, the thrips Frankliniella occidentalis. Here, we present the results of a study on the effects of TSWV infections of plants on the effectiveness of three species of natural enemies of F. occidentalis: the predatory mites Neoseiulus cucumeris and Iphiseius degenerans, and the predatory bug Orius laevigatus. The growth rate of thrips larvae was positively affected by the presence of virus in the host plant. Because large larvae are invulnerable to predation by the two species of predatory mites, this resulted in a shorter period of vulnerability to predation for thrips that developed on plants with virus than thrips developing on uninfected plants (4.4 vs. 7.9 days, respectively). Because large thrips larvae are not invulnerable to predation by the predatory bug Orius laevigatus, infection of the plant did not affect the predation risk of thrips larvae from this predator. This is the first demonstration of a negative effect of a plant pathogen on the predation risk of its vector.
PMCID: PMC2469278  PMID: 18392858
Tritrophic interactions; Preference; Prey size; Frankliniella occidentalis; Tomato spotted wilt virus
25.  How Predictable Are the Behavioral Responses of Insects to Herbivore Induced Changes in Plants? Responses of Two Congeneric Thrips to Induced Cotton Plants 
PLoS ONE  2013;8(5):e63611.
Changes in plants following insect attack are referred to as induced responses. These responses are widely viewed as a form of defence against further insect attack. In the current study we explore whether it is possible to make generalizations about induced plant responses given the unpredictability and variability observed in insect-plant interactions. Experiments were conducted to test for consistency in the responses of two congeneric thrips, Frankliniella schultzei Trybom and Frankliniella occidentalis Pergrande (Thysanoptera: Thripidae) to cotton seedlings (Gossypium hirsutum Linneaus (Malvales: Malvaceae)) damaged by various insect herbivores. In dual-choice experiments that compared intact and damaged cotton seedlings, F. schultzei was attracted to seedlings damaged by Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), Tetranychus urticae (Koch) (Trombidiforms: Tetranychidae), Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae), F. schultzei and F. occidentalis but not to mechanically damaged seedlings. In similar tests, F. occidentalis was attracted to undamaged cotton seedlings when simultaneously exposed to seedlings damaged by H. armigera, T. molitor or F. occidentalis. However, when exposed to F. schultzei or T. urticae damaged plants, F. occidentalis was more attracted towards damaged plants. A quantitative relationship was also apparent, F. schultzei showed increased attraction to damaged seedlings as the density of T. urticae or F. schultzei increased. In contrast, although F. occidentalis demonstrated increased attraction to plants damaged by higher densities of T. urticae, there was a negative relationship between attraction and the density of damaging conspecifics. Both species showed greater attraction to T. urticae damaged seedlings than to seedlings damaged by conspecifics. Results demonstrate that the responses of both species of thrips were context dependent, making generalizations difficult to formulate.
PMCID: PMC3653804  PMID: 23691075

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