John F. Tooker

Herbivore exploits orally secreted bacteria to suppress plant defenses

Significance The role of herbivore-associated microbes in modifying plant defenses has received scant attention. The Colorado potato beetle secretes symbiotic bacteria to wounds to manipulate plant defenses. The bacteria elicit salicylic acid (SA)-regulated defenses, and because SA signaling often negatively cross-talks with jasmonate signaling, plants are unable to fully activate their jasmonate-mediated resistance against the herbivore. From the plants’ perspective, they recognize herbivores not as such, but as microbial threats. We identified the specific bacteria from the beetle secretions and also characterized one of the bacterial effectors responsible for defense suppression. This clever, deceptive strategy for suppressing defenses has not been previously documented. Our results add a significant, unique concept to plant–insect interactions and how herbivores hijack plant defense signaling. Induced plant defenses in response to herbivore attack are modulated by cross-talk between jasmonic acid (JA)- and salicylic acid (SA)-signaling pathways. Oral secretions from some insect herbivores contain effectors that overcome these antiherbivore defenses. Herbivores possess diverse microbes in their digestive systems and these microbial symbionts can modify plant–insect interactions; however, the specific role of herbivore-associated microbes in manipulating plant defenses remains unclear. Here, we demonstrate that Colorado potato beetle (Leptinotarsa decemlineata) larvae exploit bacteria in their oral secretions to suppress antiherbivore defenses in tomato (Solanum lycopersicum). We found that antibiotic-untreated larvae decreased production of JA and JA-responsive antiherbivore defenses, but increased SA accumulation and SA-responsive gene expression. Beetles benefit from down-regulating plant defenses by exhibiting enhanced larval growth. In SA-deficient plants, suppression was not observed, indicating that suppression of JA-regulated defenses depends on the SA-signaling pathway. Applying bacteria isolated from larval oral secretions to wounded plants confirmed that three microbial symbionts belonging to the genera Stenotrophomonas, Pseudomonas, and Enterobacter are responsible for defense suppression. Additionally, reinoculation of these bacteria to antibiotic-treated larvae restored their ability to suppress defenses. Flagellin isolated from Pseudomonas sp. was associated with defense suppression. Our findings show that the herbivore exploits symbiotic bacteria as a decoy to deceive plants into incorrectly perceiving the threat as microbial. By interfering with the normal perception of herbivory, beetles can evade antiherbivore defenses of its host.

Biology, Ecology, and Management of Brown Marmorated Stink Bug (Hemiptera: Pentatomidae)

Brown marmorated stink bug, Halyomorpha halys Stal, is an invasive, herbivorous insect species that was accidentally introduced to the United States from Asia. First discovered in Allentown, PA, in 1996, H. halys has now been reported from at least 40 states in the United States. Additional invasions have been detected in Canada, Switzerland, France, Germany, Italy, and Lichtenstein, suggesting this invasive species could emerge as a cosmopolitan pest species. In its native range, H. halys is classified as an outbreak pest; however, in North America, H. halys has become a major agricultural pest across a wide range of commodities. H. halys is a generalist herbivore, capable of consuming >100 different species of host plants, often resulting in substantial economic damage; its feeding damage resulted in US

Large-Scale Deployment of Seed Treatments Has Driven Rapid Increase in Use of Neonicotinoid Insecticides and Preemptive Pest Management in U.S. Field Crops

37 million of losses in apple in 2010, but this stink bug species also attacks other fruit, vegetable, field crop, and ornamental plant species. H. halys has disrupted integrated pest management programs for multiple cropping systems. Pesticide applications, including broad-spectrum insecticides, have increased in response to H. halys infestations, potentially negatively influencing populations of beneficial arthropods and increasing secondary pest outbreaks. H. halys is also challenging because it affects homeowners as a nuisance pest; the bug tends to overwinter in homes and outbuildings. Although more research is required to better understand the ecology and biology of H. halys , we present its life history, host plant damage, and the management options available for this invasive pest species.

Seeds of Change: Corn Seed Mixtures for Resistance Management and Integrated Pest Management

Neonicotinoids are the most widely used class of insecticides worldwide, but patterns of their use in the U.S. are poorly documented, constraining attempts to understand their role in pest management and potential nontarget effects. We synthesized publicly available data to estimate and interpret trends in neonicotinoid use since their introduction in 1994, with a special focus on seed treatments, a major use not captured by the national pesticide-use survey. Neonicotinoid use increased rapidly between 2003 and 2011, as seed-applied products were introduced in field crops, marking an unprecedented shift toward large-scale, preemptive insecticide use: 34-44% of soybeans and 79-100% of maize hectares were treated in 2011. This finding contradicts recent analyses, which concluded that insecticides are used today on fewer maize hectares than a decade or two ago. If current trends continue, neonicotinoid use will increase further through application to more hectares of soybean and other crop species and escalation of per-seed rates. Alternatively, our results, and other recent analyses, suggest that carefully targeted efforts could considerably reduce neonicotinoid use in field crops without yield declines or economic harm to farmers, reducing the potential for pest resistance, nontarget pest outbreaks, environmental contamination, and harm to wildlife, including pollinator species.

Gall insects can avoid and alter indirect plant defenses

ABSTRACT The use of mixtures of transgenic insecticidal seed and nontransgenic seed to provide an in-field refuge for susceptible insects in insect-resistance-management (IRM) plans has been considered for at least two decades. However, the U.S. Environmental Protection Agency has only recently authorized the practice. This commentary explores issues that regulators, industry, and other stakeholders should consider as the use of biotechnology increases and seed mixtures are implemented as a major tactic for IRM. We discuss how block refuges and seed mixtures in transgenic insecticidal corn, Zea mays L., production will influence integrated pest management (IPM) and the evolution of pest resistance. We conclude that seed mixtures will make pest monitoring more difficult and that seed mixtures may make IRM riskier because of larval behavior and greater adoption of insecticidal corn. Conversely, block refuges present a different suite of risks because of adult pest behavior and the lower compliance with IRM rules expected from farmers. It is likely that secondary pests not targeted by the insecticidal corn as well as natural enemies will respond differently to block refuges and seed mixtures.

Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant.

Parasitic species can dramatically alter host traits. Some of these parasite-induced changes can be considered adaptive manipulations that benefit the parasites. Gall-inducing insects are parasites well known for their ability to alter host-plant morphology and physiology, including the distribution of plant defensive compounds. Here it was investigated whether gall-inducing species alter indirect plant defenses, involving the release of volatile compounds that are attractive to foraging natural enemies. Using field and factorial laboratory experiments, volatile production by goldenrod (Solidago altissima) plants was examined in response to attack by two gall-inducing species, the tephritid fly Eurosta solidaginis and the gelechiid moth Gnorimoschema gallaesolidaginis, as well as the meadow spittlebug, Philaenus spumarius, and the generalist caterpillar Heliothis virescens. Heliothis virescens elicited strong indirect defensive responses from S. altissima, but the gall-inducing species and spittlebugs did not. More significantly, infestation by E. solidaginis appeared to suppress volatile responses to subsequent attack by the generalist caterpillar. The extensive control that E. solidaginis apparently exerts over host-plant defense responses may reduce the predation risk for the gall inducer and the subsequent herbivore, and could influence community-level dynamics, including the distribution of herbivorous insect species associated with S. altissima parasitized by E. solidaginis.

Bee nutrition and floral resource restoration

Caterpillars produce oral secretions that may serve as cues to elicit plant defenses, but in other cases these secretions have been shown to suppress plant defenses. Ongoing work in our laboratory has focused on the salivary secretions of the tomato fruitworm, Helicoverpa zea. In previous studies we have shown that saliva and its principal component glucose oxidase acts as an effector by suppressing defenses in tobacco. In this current study, we report that saliva elicits a burst of jasmonic acid (JA) and the induction of late responding defense genes such as proteinase inhibitor 2 (Pin2). Transcripts encoding early response genes associated with the JA pathway were not affected by saliva. We also observed a delayed response to saliva with increased densities of Type VI glandular trichomes in newly emerged leaves. Proteomic analysis of saliva revealed glucose oxidase (GOX) was the most abundant protein identified and we confirmed that it plays a primary role in the induction of defenses in tomato. These results suggest that the recognition of GOX in tomato may represent a case for effector-triggered immunity. Examination of saliva from other caterpillar species indicates that saliva from the noctuids Spodoptera exigua and Heliothis virescens also induced Pin2 transcripts.

Shared genes related to aggression, rather than chemical communication, are associated with reproductive dominance in paper wasps (Polistes metricus)

Bee-population declines are linked to nutritional shortages caused by land-use intensification, which reduces diversity and abundance of host-plant species. Bees require nectar and pollen floral resources that provide necessary carbohydrates, proteins, lipids, and micronutrients for survival, reproduction, and resilience to stress. However, nectar and pollen nutritional quality varies widely among host-plant species, which in turn influences how bees forage to obtain their nutritionally appropriate diets. Unfortunately, we know little about the nutritional requirements of different bee species. Research must be conducted on bee species nutritional needs and host-plant species resource quality to develop diverse and nutritionally balanced plant communities. Restoring appropriate suites of plant species to landscapes can support diverse bee species populations and their associated pollination ecosystem services.

Influence of Plant Community Structure on Natural Enemies of Pine Needle Scale (Homoptera: Diaspididae) in Urban Landscapes

BackgroundIn social groups, dominant individuals may socially inhibit reproduction of subordinates using aggressive interactions or, in the case of highly eusocial insects, pheromonal communication. It has been hypothesized these two modes of reproductive inhibition utilize conserved pathways. Here, we use a comparative framework to investigate the chemical and genomic underpinnings of reproductive dominance in the primitively eusocial wasp Polistes metricus. Our goals were to first characterize transcriptomic and chemical correlates of reproductive dominance and second, to test whether dominance-associated mechanisms in paper wasps overlapped with aggression or pheromone-related gene expression patterns in other species. To explore whether conserved molecular pathways relate to dominance, we compared wasp transcriptomic data to previous studies of gene expression associated with pheromonal communication and queen-worker differences in honey bees, and aggressive behavior in bees, Drosophila, and mice.ResultsBy examining dominant and subordinate females from queen and worker castes in early and late season colonies, we found that cuticular hydrocarbon profiles and genome-wide patterns of brain gene expression were primarily associated with season/social environment rather than dominance status. In contrast, gene expression patterns in the ovaries were associated primarily with caste and ovary activation. Comparative analyses suggest genes identified as differentially expressed in wasp brains are not related to queen pheromonal communication or caste in bees, but were significantly more likely to be associated with aggression in other insects (bees, flies), and even a mammal (mice).ConclusionsThis study provides the first comprehensive chemical and molecular analysis of reproductive dominance in paper wasps. We found little evidence for a chemical basis for reproductive dominance in P. metricus, and our transcriptomic analyses suggest that different pathways regulate dominance in paper wasps and pheromone response in bees. Furthermore, there was a substantial impact of season/social environment on gene expression patterns, indicating the important role of external cues in shaping the molecular processes regulating behavior. Interestingly, genes associated with dominance in wasps were also associated with aggressive behavior in bees, solitary insects and mammals. Thus, genes involved in social regulation of reproduction in Polistes may have conserved functions associated with aggression in insects and other taxa.

Flowering Plant Hosts of Adult Hymenopteran Parasitoids of Central Illinois

Abstract Pine needle scale, Chionaspis pinifoliae (Fitch), is a pest of many species of conifers in urban habitats and Christmas tree farms. We found that the scale was abundant in impoverished habitats, such as ornamental landscapes, and scarce in more natural, park-like habitats. Rates of parasitism were highest in impoverished habitats, suggesting that parasitoids were not effective in suppressing scale populations. Generalist predators, however, were more diverse and abundant in natural habitats and appear to be more effective in controlling scales in structurally complex plant communities. Total densities of arthropods and densities of plant-feeding species were greatest in impoverished habitats, suggesting that populations were poorly regulated. Outbreaks of pine needle scale in ornamental landscapes and Christmas tree farms may be discouraged by increasing plant structural and species diversity to favor natural enemies.