Progress 12/01/14 to 09/30/19
Outputs
Target Audience:The USDA-APHIS, USDA-Forest Service and state agricultural agencies benefit from the results of our research, particularly on spotted lanternfly (SLF) and Asian longhorned beetle. Master gardeners affiliated with Penn State Extension and the Extension agencies of regional land grant institutions also benefit from research on SLF. The scientific community are also a target audience and benefit from our findings in chemical ecology, insect physiology, and microbial symbioses. In addition to the general scientific community, beekeepers and commercial bumblebee suppliers (e.g. Koppert) benefit from our work on bee thermoregulatory function; work on Monarch (and other lepidopterans) flight physiology targets Monarch and other pollinator conservation programs, such as Master Gardeners. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?Postdocs participated in grant writing and gave presentations at numerous conferences. Graduate students presented talks at national and international conferences and wrote graduate student fellowships (including NIFA and NSF graduate student fellowships) and other funding applications. Postdocs and graduate students have participated in several outreach and research activities reaching stakeholders at state legislative and local regulatory levels (e.g. PA DMV, Great Insect Fair, "Skype a Scientist", etc., PDA) as well as for primary and secondary schools. These activities provided extensive training in oral communication at the scientific and lay-person's levels. One graduate student wrote several articles for the general public about various scientific topics. Urban's lab presented an SLF exhibit at the Pennsylvania Farm Show that won the award for outstanding educational exhibit. How have the results been disseminated to communities of interest?Results have been disseminated through publications, presentations at conferences and as invited talks, and through outreach efforts on spotted lanternfly. The postdoc, some grad students, and two of the faculty gave numerous presentations for legislators, regulatory agencies, and other stakeholders at multiple venues. Urban organized a Spotted Lanternfly Working Group conference with over 100 participants in July of 2018 and has been heavily involved in working and communicating with stakeholders on PSU efforts to fill knowledge gaps about spotted lanternfly biology and ecology. What do you plan to do during the next reporting period to accomplish the goals?
Nothing Reported
Impacts
What was accomplished under these goals?
Goal 1: Field experiments in China and lab experiments in the U.S. showed that resistance in several species of poplar to Asian longhorned beetle (ALB) is conferred by higher levels of salicinoids in the bark of trees. Bark is fed on by adults but not larvae. Because eggs are laid beneath the bark in the wood, which is low in salicinoids, this allows larvae to escape these toxins. Salicinoids reduced adult feeding and egg production in a dose-dependent manner, and at high levels caused severe damage to the anterior midgut. Impact: Knowledge that plants containing salicinoids are likely to be resistant to ALB will assist with survey efforts to facilitate eradication and replacement of trees cut down due to ALB infestation. (Hoover) Goal 4: Enterobacter ludwigii is a gut-associated bacteria identified from field-collected caterpillars, and it indirectly induces defenses in tomato by triggering biosynthesis of salivary elicitors. Inoculating lab-reared caterpillars with E. ludwigii did not significantly affect larval growth, but two immunity-related genes, glucose oxidase (GOX) and lysozyme, were more highly expressed in both salivary glands and midguts compared with carrier-treated caterpillars. Saliva and its main component protein GOX from E. ludwigii-inoculated larvae played a role in inducing maize anti-herbivore responses. We developed axenic and gnotobiotic methods for fall armyworm and tested how particular gut microbiota influence interactions with plant defenses that can alter peritrophic matrix permeability. Axenic insects grew more but displayed lower immune based responses compared with those possessing bacterial isolates from field-collected larvae. While gut bacteria reduced performance of larvae fed on plants, none of the isolates produced mortality when injected directly into the hemocoel, indicating that plant physical and chemical defenses not only act directly upon the insect, but also have some interplay with the herbivore's microbiome. Combined direct and indirect, microbe-mediated assaults by maize defenses on the fall armyworm on the insect digestive and immune system reduced growth and elevated mortality. Impact: These findings suggest that microbial associates of lepidopterans could be used to enhance plant resistance against caterpillar pests. (Felton and Hoover) Goal: Effects of neonicotinoid seed treatments on plant defenses and interactions with herbivores and their natural enemies. Neonicotinoids (neonics) are translocated to the extra floral nectar (EFN) of clothianidin- and imidacloprid-treated greenhouse-grown cotton plants. But there were no differences in the quantity of EFN produced by neonic-treated plants compared to untreated controls. In bioassays with female parasitoid wasps fed EFN from untreated, clothianidin-treated, or imidacloprid-treated plants, there was no difference in mortality or parasitization success. Acute toxicity assays for the parasitoid fed on spiked honey were done to determine LC50 values 48 h after treatment for clothianidin and imidacloprid. Although the LC50 values were markedly higher than neonic concentrations detected in EFN, caution should be used when translating these results to the field. (Felton and Hoover, New Goal) Goal: Develop new genetic markers to identify the origin of invading populations of spotted lanternfly (SLP), a recent invasive species introduced into PA with a broad host range. We sequenced SLF DNA sampled across the genome. Using these data and the recently published complete SLF genome, we identified ~150 candidate loci that are potential new genetic markers that may be informative in determining SLF origin, as well as in tracking SLF population movement and expansion. We are testing the first 50 of these loci to arrive at a final pool of 20 loci that we estimate can thoroughly track SLF populations and determine origin. Impacts: These markers will allow us to inexpensively genotype specimens intercepted in areas outside the currently known distribution of SLF to determine if they originated from the PA population or are new introductions from Asia. Determination of the origin of SLF in Asia will aid in the identification of natural enemies of SLF in its native range. The new genetic loci will also be used by colleagues at Temple University to test and validate their models of SLF spread in the US and abroad. (Urban, New Goal) Goal: Characterize the bacterial and fungal associates of spotted lanternfly (SLF) to allow us to assess the potential for pathogen transmission, to identify host plant requirements and/or preferences associated with microbial symbionts harbored by SLF, or to identify potential natural microbial pathogens of SLF that can be used for control. We sequenced and assembled the genomes of the 3 obligate bacterial endosymbionts of SLF. Preliminary gene prediction analyses and annotation indicate that the 2 most ancient endosymbionts (Sulcia muelleri and Vidania fuloroideae) function to synthesize essential amino acids missing in the phloem diet of this insect. The third endosymbiont genome is of a novel bacterial species. This endosymbiont is present in SLF and in species throughout the planthopper family Fulgoridae. It has genes involved with lipid and fatty acid biosynthesis and may play a role in synthesizing waxy components of the egg mass. Surveys of other bacteria in the SLF digestive tract did not reveal the presence of any known potential pathogens. Impacts: Identifying the function of bacterial endosymbionts of SLF provides information on the fundamental biology that is needed to better predict its potential distribution and damage it may cause in agriculture and in other commodities. Targeting genes specific to SLF bacterial endosymbionts, and potentially disrupting the development or transmission of these bacteria, may offer highly specific methods of controlling SLF. (Urban, New Goal) Goal: Characterize microbial communities in sooty mold: Across the life cycle of nymphs and adults of SLF in 2017, we sampled microbial communities present on several preferred host plants fed upon by SLF when plants were healthy and over time as sooty mold developed. We amplified a region of a fungal gene that will allow us to identify specific taxa that proliferate in SLF honeydew and comprise "sooty mold." We have sequenced and analyzed these samples and are currently performing additional analyses and culturing experiments to verify the identity of the key fungal taxa comprising sooty mold on cultivated grape and tree of heaven. Impacts: Characterizing key microbial taxa that comprise sooty mold and cultivating these taxa under controlled lab conditions will enable a more thorough understanding of the mechanisms by which SLF induced sooty mold damages grapevines and other plants. (Urban, New Goal) Goal: To understand the adaptations of flight musculoskeletal systems that allow large insects to fly and disperse. Studies on variation in molecular composition and performance characteristics of insect flight muscle in response to environmental factors/cues continue to be addressed in various insect systems. These factors include diet, infection and temperature, as well as perturbations such as pesticide exposure. In addition to several papers on functional morphology of locomotor- and other systems in wasps and hawkmoths, we reported how infections modify the molecular composition and function of insect flight muscle. We also studied thermal stress responses of hawkmoth flight muscles to flight and high ambient temperature. We discovered that SLF generates significantly higher than ambient body temperature through an as of yet unknown mechanism. Impacts: Our findings have direct implications for detection of specimens in the field and will likely increase our understanding of their success as invasive species. (Schilder, New Goal)
Publications
- Type:
Journal Articles
Status:
Under Review
Year Published:
2019
Citation:
Jones, A.G., K. Hoover, K. Pearsons, J.F. Tooker, and G.W. Felton. 2019. Potential impacts of translocation of neonicotinoid insecticides to cotton (Gossypium hirsutum [Malvales: Malvaceae]) extrafloral nectar on parasitoids, in review.
- Type:
Journal Articles
Status:
Under Review
Year Published:
2019
Citation:
Paudel, S., P.A. Lin, K, Hoover, G.W. Felton and E.G. Rajotte. 2019. Asymmetric responses to climate change: Temperature differentially alters a herbivore salivary elicitor and host plant responses to herbivory. Plant, Cell, and Environment, in review.
- Type:
Journal Articles
Status:
Published
Year Published:
2019
Citation:
Hoover, K. 2019. Editorial overview: Insect behavior and parasites: From manipulation to self-medication. Current Opinion in Insect Science 33: vi-viii. https://doi.org/10.1016/j.cois.2019.06.012.
- Type:
Journal Articles
Status:
Published
Year Published:
2019
Citation:
Pan, Q., I. Shikano, K. Hoover, T-X Liu, and G.W. Felton. 2019. Pathogen-mediated tritrophic interactions: Baculovirus-challenged caterpillars induce higher plant defenses than healthy caterpillars. J. Chem. Ecol. 45: 515-524.
- Type:
Journal Articles
Status:
Published
Year Published:
2019
Citation:
Mason, C.J., S. Ray, I. Shikano, M. Peiffer, A.G. Jones, D.S. Luthe, K. Hoover and G.W. Felton. 2019. Plant defenses interact with insect enteric bacteria by initiating a leaky gut syndrome. Proceedings of the National Academy of Sciences 116(32): 5991-15996.
- Type:
Journal Articles
Status:
Published
Year Published:
2019
Citation:
Jones, A. G., C. J. Mason, G. W. Felton and K. Hoover. 2019. Host plant and population source drive diversity of microbial gut communities in two polyphagous insects. Scientific Reports 9(1): 2792.
- Type:
Journal Articles
Status:
Published
Year Published:
2019
Citation:
Mason, C. J., D. C. Long, R. L. Lindroth and K. Hoover. 2019. Divergent host plant utilization by adults and offspring is related to intra-plant variation in chemical defences. Journal of Animal Ecology, https://doi.org/10.1111/1365-2656.13063.
- Type:
Journal Articles
Status:
Accepted
Year Published:
2019
Citation:
Miko, I., Rahman, S. R., Jones, A., Townley, M. A., *Gominho, B., Paudel, S., *Stupski, D., Hines, H. M., Schilder, R. J. (2019). From spinning silk to spreading saliva: mouthpart remodeling in Manduca sexta (Lepidoptera: Sphingidae). Insect Systematics and Diversity (accepted 05/16/19).
- Type:
Journal Articles
Status:
Published
Year Published:
2019
Citation:
Schilder, R. J., Stewart, H. (2019). Parasitic gut infection causes functional and molecular resemblance of dragonfly flight muscle to skeletal muscle of obese vertebrates. The Journal of Experimental Biology doi: 10.1242/jeb.18850.
- Type:
Journal Articles
Status:
Published
Year Published:
2019
Citation:
Mik�, I., Rahman, S. R., Anzaldo, S., van de Kamp, T., Parslow, B. A., Tatarnic, N. J., Wetherington, M. T., Anderson, J., Schilder, R. J., Ulmer, J. M., Deans, A. R., Hines, H. M. (2019). Fat in the leg: function of the expanded hind leg in gasteruptiid wasps (Hymenoptera: Gasteruptiidae). Insect Systematics and Diversity 3(1): 2.
- Type:
Journal Articles
Status:
Under Review
Year Published:
2019
Citation:
Gominho, B., Stupski, S. D., Schilder, R. J.. Heat shock protein responses to high ambient temperature and hovering flight in the hawkmoth, Manduca sexta.
- Type:
Journal Articles
Status:
Under Review
Year Published:
2019
Citation:
Munoz, D., Miller, D., Schilder, R. J., Campbell Grant, E. H. Range-wide impacts of intraspecific variation in metabolic rate and thermal plasticity under two current and future climates.
- Type:
Journal Articles
Status:
Published
Year Published:
2019
Citation:
Urban JM. 2019. Perspective: Shedding light on spotted lanternfly impacts in the USA. Pest Management Science. http://doi.org/10.1002/ps.5619.
- Type:
Journal Articles
Status:
Published
Year Published:
2019
Citation:
Kingan SB, Urban J, Lambert CC, Baybayan P, Childers AK, Coates B, Scheffler B, Hackett K, Korlach J, Geib SM. 2019. A high-quality genome assembly from a single field-collected spotted lanternfly (Lycorma delicatula) using the PacBio Sequel II system. Gigascience 8(10). https://doi.org/10.1093/gigascience/giz122.
- Type:
Journal Articles
Status:
Published
Year Published:
2019
Citation:
Wolfin MS, Binyameen M, Wang Y, Urban J, Roberts D, and Baker T. 2019. Flight dispersal capabilities of female spotted lanternflies (Lycorma delicatula) related to size and mating status. Journal of Insect Behavior. https://doi.org/10.1007/s10905-019-09724-x.
- Type:
Journal Articles
Status:
Published
Year Published:
2019
Citation:
Leach H, Biddinger DJ, Krawczyk G, Smyers E, and Urban JM. 2019. Evaluation of insecticides for control of the spotted lanternfly, Lycorma delicatula, (Hemiptera: Fulgoridae), a new pest of fruit in the Northeastern U.S. Crop Protection, 124:1-6.
- Type:
Journal Articles
Status:
Published
Year Published:
2019
Citation:
Baker TC, Smyers EC, Urban JM, Meng Z, Pagadala Damadaram KJ, Myrick AJ, Cooperband MF, and Domingue MJ. 2019. Progression of seasonal activities of adults of the spotted lanternfly, Lycorma delicatula, during the 2017 season of mass flight dispersal behavior in eastern Pennsylvania. Journal of Asia Pacific Entomology, 22: 705-713.
|
Progress 10/01/17 to 09/30/18
Outputs
Target Audience:Target audiences include the USDA-APHIS, USDA-Forest Serviceand state agricultural agencies benefit from the results of our research, particularly on spotted lanternfly and Asian longhorned beetle. The scientific community are also a target audience and benefit from our findings in chemical ecology, insect physiology, and microbial symbioses. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?Graduate students gave talks and presented posters at several conferences. Grad students and postdocs wrote and received funding for competititve grants from USDA NIFA and College-level awards. Graduate students in Schilder's lab presented at international conferences and wrote fellowship/award applications. Several graduate students conducted numerous outreach activities for a variety of stakeholders from legislative staff to regulatory agencies and for primary and secondary schools. This provided extensive training in oral communication at the scientific and lay-person's levels. How have the results been disseminated to communities of interest?Results have been disseminated through publications, presentations at conferences and as invited talks, and through outreach efforts on spotted lanternfly. The postdoc, some grad stuents, and two of the faculty gave numerous presentations for legislators, regulatory agencies, and other stakeholders at multiple venues. Urban organized a Spotted Lanternfly Working Group conference with over 100 participants in July of 2018 and has been heavily involved in working and communicating with stakeholders on PSU efforts to fill knowledge gaps about spotted lanternfly biology and ecology. What do you plan to do during the next reporting period to accomplish the goals?Felton and Hoover's labs continue to explore interactions between gut bacteria and lepidoptera in multitrophic and plant defenses contexts. We will evaluate the roles of gut bacteria in mediating interactions between plant defenses and natural enemies in several notcuids. Additionally, we are developing quantitative methods to assess how bacterial communities interact in different dietary contexts. We will also explore the interactions between gut bacteria and enteric pathogens in fall armyworm, corn earworm, and gypsy moth. Urban will continue to work on developing novel genetic markers for SLF in Pennsylvania. We are beginning a collaboration with investigators in China who have generated genetic data for subpopulations of SLF within multiple regions in China. We will collaborate on analyses and publication of a combined data set to identify the origin of SLF in PA with greater resolution given their extensive sampling in that country. We are analyzing the data to determine what bacteria are harbored in SLF digestive tracts, and determining its association with bacteria (and potential plant pathogens) typically associated with plants to determine SLF's capacity for transmission of plant-associated microbes. We are also currently assembling the genomes of the three bacterial endosymbionts of SLF to reveal role(s) they play in the biology and nutritional requirements of SLF. We are also dissecting SLF females sampled to reflect a range of reproductive maturation to characterize how SLF transmits endosymbionts to developing eggs. We will continue to characterize the sooty mold community using DNA sequencing and culturing to identify and isolate fungi present in these communities, and test the interaction of these taxa with other microbes typically present (known pathogens and potential beneficial taxa) on grapevines. We will conduct culturing experiments to isolate specific microbes and conduct bioassays to search for potential antimicrobial compounds some may produce that could reduce levels of sooty mold damage to plants. Hoover's lab will be addressing new goals in the coming year on the requirement of tree-of-heaven for reproduction of SLF, host preferences and performance of SLF by life stage on preferred tree species, dispersal distances into contiguous forest habitats, and impacts of SLF on tree health and physiology. Another new goal is to determine if there is a pollination deficiency issue with black cherry on the Allegheny National Forest and if so, why this might be happening. Black cherry regeneration and seed production has declined considerably in the past decade. Schilder will continue the flight muscle performance and thermoregulation research projects in hawkmoth, bumblebee and dragonfly systems, but also expand his research program with work on the Monarch butterfly. We have recently initiated a project examining effects of larval dietary history (i.e. food plant quality) on the ability of adult monarchs to migrate. One of the central theses of this project is that dietary quality (or varying levels of toxicity, such as is the case for Monarch butterfly milkweed host plants) affects flight muscle ability due to energetic trade-offs that are hypothesized to exist between traits related to chemical detoxification, energy store biosynthesis, and flight muscle design quality. Thus, this project will define the importance of trophic interactions across insect life history (i.e. not limited to the larval stages, as is common), and new mechanistic paradigms relating diet and dispersal ability in the insects under study in Schilder's lab. More generally, it will highlight the importance of larval stressors to the fitness and dispersive capacity of flying adults, i.e. the life stages that directly affect the spread and location of many (pest) herbivore insects.
Impacts
What was accomplished under these goals?
Goal: Characterize mechanisms of resistance of Chinese poplar to ALB. We identified salicinoids as the compounds primarily responsible for mediating poplar resistance to ALB, and found that resistance occurs entirely against the adult life stages. Poplars differentially express salicinoids; bark has high concentrations while wood has negligible amounts. Adults encounter these compounds during feeding on bark-covered twigs, while larval stages are able to avoid them because they feed exclusively in wood. We found that salicinoids are affect adults in a dose-dependent manner, reducing feeding and egg production. Goal: Determine the role of bacteria in mediating induced plant responses by caterpillar feeding. The polyphagous caterpillar pestHelicoverpa zea harbors certain microbes in their digestive systems.Enterobacter ludwigiiis one of the gut-associated bacteria identified from field-collected caterpillars, and it has been shown to indirectly induce defenses in the dicot plant tomato by triggering the biosynthesis of salivary elicitors, but there are no clear mechanisms to show how gut microbes alter these salivary cues and how a different host plant responds to these inducible elicitors. Inoculating lab-reared caterpillars withE. ludwigii, did not significantly affect the growth of caterpillars, but two immunity-related genesglucose oxidase(GOX)andlysozyme(LYZ) were more highly expressed in both salivary glands and midguts compared with MgCl2solution-treated caterpillars. Oral elicitors were evaluated for their role in triggering maize-specific defense responses. Our results show that saliva and its main component protein glucose oxidase (GOX) fromE. ludwigii-inoculated caterpillars played a role in inducing maize anti-herbivore responses. We have developed a germ-free and gnotobiotic system for fall armyworm, and have performed bioassays with this species using a defined bacterial consortia. Gut bacteria can interact to exacerbate the negative consequences of gut-targeted plant defenses. Mechanisms of negative effects on herbivores occurs by compromising the peritrophic membrane, allowing opportunistic colonization of bacteria in the insect hemolymph. Goal: Effects of neonicotinoid seed treatments on plant defenses and interactions with herbivores and their natural enemies. There is no difference in the quantity of extrafloral nectar produced by neonicotinoid-treated plants. We identified neonicotinoid active ingredients in the extrafloral nectar using ELISA, indicating that this could be a route of exposure of these pesticides to parasitoid wasps and other insects that use extrafloral nectar as a food resource. When fall armyworm ingest baculovirus on neonicotinoid-treated cotton plants, there is slower time to death. We plan to repeat these experiments and investigate the effects of induced plant defenses on baculovirus mortality in both treated and untreated plants. Preliminary data suggest that roots of neonicotinoid-treated maize plants may be more attractive than untreated plants to the entomopathogenic nematode Heterorhabditis bacteriophora. Goal: Develop new genetic markers to identify the origin of invading populations of spotted lanternfly (SLP), a recent invasive species introduced into PA with a broad host range. We initially used genetic markers developed in Korea where SLF invaded in 2004 and from this work, concluded that SLF in PA did not originate from Korea. These markers did not provide the information needed to identify the origin of invasion, as they failed to match up to sampled populations in China and Vietnam. This has demonstrated the need to develop new genetic markers to study SLF. Goal: Characterize the bacterial and fungal associates of spotted lanternfly (SLF) to allow us to assess the potential for pathogen transmission, to identify host plant requirements and/or preferences associated with microbial symbionts harbored by SLF, or to identify potential natural microbial pathogens of SLF that can be used for control. We used next-gen DNA sequencing to characterize the microbiome of SLF. SLF abdominal tissue harbors a bacterial community dominated by three endosymbionts (Sulcia muelleri, Vidania fulgoroideae, and an uncharacterized Gammaproteobacterium). The SLF microbiome was statistically significantly different from that of other closely related taxa within the same planthopper family. We compared bacterial associates of SLF from Korea and China and found that the microbiome of SLF in invaded ranges (PA and Korea) is significantly less taxonomically diverse than that of SLF in their natural range. Therefore, while all SLF share the same obligate bacterial endosymbionts, populations differ with respect to the facultative (non-obligate) bacteria they harbor, likely residing within the SLF digestive tract. To test this hypothesis, we subsequently dissected the digestive tract from a sample of SLF adults and used amplicon sequencing to characterize bacteria harbored therein. Urban's lab has also sequenced the genomes for the three obligate SLF endosymbionts and is currently assembling these to determine their role in SLF biology. Goal: Characterize microbial communities in sooty mold: Across the life cycle of nymphs and adults of SLF in 2017, we sampled microbial communities present on plants (the SLF preferred host "tree of heaven", black walnut, cultivated grape, and wild grape) fed upon by SLF when plants were in their healthy state and over time as sooty mold developed. We amplified a region of a fungal gene that will allow us to identify specific taxa that proliferate in SLF honeydew and comprise "sooty mold." These samples have been submitted for sequencing. This work will allow us to identify sooty mold taxa, characterize its growth and interactions with other fungi that are the primary pathogens affecting grapevines in PA. Goal: To understand the molecular mechanisms of flight muscles that allow large insects to fly and disperse. Studies relating variation in molecular composition and performance characteristics of insect flight muscle in response to environmental factors/cues continue to be addressed. A manuscript on dragonfly troponin T expression effects of parasitic infections is in revision at the Journal of Experimental Biology. Continuing work is relating larval exposure to environmental stressors (i.e. low water and soil pH) to susceptibility to this infection and the gut microbiome. Significant progress was made on a new project related to thermal physiology in another beneficial insect, the bumblebee. In summary, exposure to immune stressors (in the form of heat-killed bacteria) significantly affects bumblebee abilities to regulate the temperature of their thoracic musculature, and thus flight ability and brood incubation (among other colony fitness components) are negatively affected under such conditions. We are currently preparing a manuscript on this project. A preliminary project was undertaken to assess ALB thermoregulatory capacities (they do need to raise their thoracic temperature significantly above ambient temperature!) relating to the initiation of flight (i.e. dispersal).
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Wang, J., M. Yang; Y. Song; F.E. Acevedo; K. Hoover; R. Zeng; G.W. Felton. 2018. Gut-associated bacteria of Helicoverpa zea indirectly trigger plant defenses in maize. J Chem Ecol https://doi.org/10.1007/s10886-018-0970-0.
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Paladini, A., D.M. Takiya, J.M. Urban, J.R. Cryan. 2018. New World spittlebugs (Hemiptera: Cercopidae: Ischnorhininae): Dated molecular phylogeny, classification Molecular Phylogenetics and Evolution 120:321-334.
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Mason, C.J., Jones, A.G. & Felton, G.W. (2018). Co-option of microbial associates by insects and their impacts on plantfolivore interactions. Plant, Cell & Environment. https://doi.org/10.1111/pce.13430
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Mason, CJ, Campbell, AM, Scully, ED, & K Hoover. 2018. Bacterial and fungal midgut community dynamics and transfer between mother and brood in the Asian longhorned beetle (Anoplophora glabripennis), an invasive xylophage. Microbial Ecology https://doi.org/10.1007/s00248-018-1205-1.
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Scully, ED, Geib, SM, Mason, CJ, Carlson, JE, Tien, M, Tsai, CJ, Harding, S, Chen, Y, & K Hoover. 2018. Host-plant induced changes in microbial community structure and midgut gene expression in an invasive polyphage (Anoplophora glabripennis). Scientific Reports 9620.
- Type:
Journal Articles
Status:
Under Review
Year Published:
2018
Citation:
Mason, CJ, Long, DC, Lindroth, RL, & K Hoover. 2018. Differential exploitation of host plants by adult and larval conspecifics are intraplant variation in plant defenses. Journal of Animal Ecology, in revision.
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Wei, J., Q. Zhou, L. Hall, A. Myrick, K. Hoover, K. Shields and T. C. Baker. 2018. Olfactory sensory neurons of the Asian longhorned beetle, Anoplophora glabripennis, specifically responsive to its two aggregation-sex pheromone components. J Chem. Ecol. 44(7), 637-649.
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Mason, C.J., A.M. Campbell, E.D. Scully and K. Hoover. 2018. Bacterial and fungal midgut community dynamics and transfer between mother and brood in the Asian longhorned beetle (Anoplophora glabripennis), an invasive xylophage. Microbial Ecology https://doi.org/10.1007/s00248-018-1205-1.
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Pan, Q., I. Shikano, K. Hoover, T.-X. Liu, and G.W. Felton. 2018. Enterobacter ludwigii, isolated from the gut microbiota of Helicoverpa zea, promotes tomato plant growth and yield without compromising anti-herbivore defenses. Arthropod-Plant Interactions https://doi.org/10.1007/s11829-018-9634-9.
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Shikano, I., Q. Pan, K. Hoover, and G.W. Felton. 2018. Herbivore-induced defenses in tomato plants enhance the lethality of the entomopathogenic bacterium, Bacillus thuringiensis var. kurstaki. J. Chem Ecol. 44: 946-956,
- Type:
Journal Articles
Status:
Published
Year Published:
2018
Citation:
Shikano, I., E.M. McCarthy, J.M. Slavicek and K. Hoover. 2018. Jasmonic acid-induced plant defenses delay caterpillar developmental resistance to a baculovirus: Slow-growth, high-mortality hypothesis in plantinsectpathogen interactions, J. Invertebr. Pathol. 158: 16-23.
- Type:
Journal Articles
Status:
Under Review
Year Published:
2018
Citation:
Trautwein, M., D. Fergus, B. Simison, I. Fernandez-Silva, M., Leong, B. Cruz, M.S., Thoemmes, M. Evans, W. Foster, K. Norville, M. Palopoli, J. Urban, R. Dunn. Two human follicle mite species reflect African origin and divergences of human populations. PLoS One, in review.
- Type:
Journal Articles
Status:
Under Review
Year Published:
2018
Citation:
Jones, AG, Mason, CJ, Felton, GW, & K Hoover. Population source and diet drive fall armyworm midgut and regurgitant bacterial communities. Scientific Reports, in review.
|
Progress 10/01/16 to 09/30/17
Outputs
Target Audience:The USDA-APHIS, USDA-Forest Service, crop consultants, arborists, and state agricultural agencies benefit from these research projects. Results related to the biology and management of spotted lanternfly have been conveyed to the appropriate USDA-APHIS personnel and PA Department of Agriculture. Aspects of this reseach were also used to educate students in courses on insect ecology, insect physiology, chemical ecology, forestry and pest management. Changes/Problems:RNAi does not work in ALB with feeding, only by injection. This goal will no longer be pursued. What opportunities for training and professional development has the project provided?Eight graduate students and 2 postdocs were trained on this project this year. Several of the students and postdocs attended and gave presentations at scientific conferences, and attended grant writing workshops or teaching workshops. Postdocs on this project wrote and contributed to writing grant proposals and served as co-PIs on these proposals. Postdoc Charles Mason served as the primary instructor for ENT314 Pests of Ornamental and Landscape Trees, and provided four guest lectures in Insect Physiology. He also gave two lectures on management of forest insects for a pesticide recertification course for Penn State Extension. Several grad students wrote competitive grant proposals and received practical training by serving as teaching asisstants in courses. How have the results been disseminated to communities of interest?Results have been reported to USDA APHIS PPQ and Pennsylvania Department of Agriculture from research on spotted lanternfly, hemlock woolly adelgid, and ALB. All findings this year have been or will be reported in scientific, peer reviewed publications, scientific meetings as oral or poster presentations, and in some cases through interviews with the popular press and web postings. What do you plan to do during the next reporting period to accomplish the goals?We will complete ongoing work on resistance in poplar to ALB adults and on the use of gnotobiotic larvae to address the roles the fungal gut symbiont Fusarium solani play in mediating digestion and detoxification of plant defenses in the ALB gut. Hoover's lab will also begin studies to address impacts of plant defenses on microbial symbiont complexes in fallarmyworm and corn earworm that impact plant and insect performance. The studies on hemlock woolly adelgid biological control using the predator Scymnus camptodromus will not continue due to collapse of the predator colony and lack of funding to travel to China to collect more predators. We will continue to work on developing novel genetic markers for SLF in Pennsylvania. We are beginning a collaboration with investigators in China who have generated genetic data for subpopulations of SLF within multiple regions in China. We will collaborate on analyses and publication of a combined data set to identify the origin of SLF in PA with greater resolution given their extensive sampling in that country. We are presently sequencing bacterial DNA from dissected digestive tracts of PA SLF feeding on Ailanthus altissima and grape and will compare these to specimens sampled from China and Korea. These differences may reveal insight into host plant preferences of SLF. We are also currently sequencing the genomes of the three bacterial endosymbionts of SLF to reveal role(s) they play in the biology and nutritional requirements of SLF. We will extract and sequence DNA to characterize microbial communities present on plants we sampled throughout 2017. We will characterize the sooty mold community and we hope to identify beneficial bacteria that are present in healthy plants that are out-competed by sooty mold. We will conduct culturing experiments to isolate specific microbes and conduct bioassays to search for potential antimicrobial compounds some may produce. Schilder will continue flight muscle research in fruit fly, hawkmoth, bumblebee and dragonfly systems. His group will start the study of mechanisms controlling heat production by insect flight muscles. Larger insects, such as ALB (and hawkmoths, dragonflies, bumblebees), require their flight muscles to be at ~35 degrees C prior to flight take-off. They can sense the environmental temperature, and in response to that sensory information, can raise flight muscle temperature by contracting all their flight muscles simultaneously (similar to human shivering when cold). We are currently defining the genes that control this ability in insects. Ultimately, this information may allow us to use pharmacological or genetic inhibition of this process, thus preventing flight altogether. Felton's group will continue to research the impacts of FAW oral-associated bacteria on plant volatiles/parasitoid attractiveness in cotton, and possibly soybean or tomato. Study will address the effects of neonicotinoid seed treatments on tritrophic interactions using cotton. We will study the quantity and quality of extrafloral nectar and effects on parasitoids in addition to oviposition by FAW in response to plants from neonic treated seeds. Additional goals being addressed are to: Determine if baculoviruses and parasitoids (and their symbiotic polydnaviruses) modulate the synthesis and activity of caterpillar salivary HAMPs or elicitors and effectors; 2/ Examine how baculoviruses and parasitoids/polydnaviruses alter the feeding behavior of their insect hosts and affect induced plant defenses; and 3/ Determine if baculoviruses and parasitoids/polydnaviruses manipulate plant defenses to their own benefit.
Impacts
What was accomplished under these goals?
Impacts: Asian longhorned beetle (ALB) was introduced into the U.S. in the early 1990's from China and large infestations are under quarantine in OH, MA, and NY where USDA continues to employ survey and eradication efforts. ALB has the potential to eliminate 35% of the urban trees in the US with economic impacts in the billions of dollars if it spreads across the U.S. Findings on mechanisms of resistance to ALB in Hoover's lab has implications for decision-making on what tree species/genotypes are safe to replant in locations at risk from ALB attack. Most poplar genotypes are not good hosts for adult feeding and higher levels of chemicals called phenolic glycosides are associated with resistance. Results from a joint project between Felton and Hoover has shown that genetic variation and plant defenses induced by herbivore feeding can influence the outcomes of insect-pathogen interactions. In general, insect viral pathogens are more effective for pest management on plants that are lower in phenolic content. Spotted lanternfly (SLF) is a very serious pest introduced into PA in 2014 from Asia. This pest poses a significant threat to the state's more than $20.5 million grape, $134 million apple, and $24 million stone fruit industries. Urban's research program is using genetic markers to identify the origin of the invading population of SLF, which will allow her to focus on where to look in the native range for natural enemies to control SLF and to better understand the PA population's phenology (timing of life stages and tolerances to a range of temperatures). Urban is also working to characterize the microbial associates of SLF, which will help to assess potential for pathogen transmission, identify host plant requirements and/or preferences associated with microbial symbionts harbored by SLF, and to identify potential natural microbial pathogens of SLF. Schilder's studies on flight muscles in dragonflies, bumblebees and fruit flies can be used to design suppression approaches (i.e. control of the process of Troponin T alternative splicing) that affect flight performance as a control measure for pest insects. Goal: Characterize mechanisms of resistance of poplar (Populus sp.) to ALB. We found that Populus resistance to ALB primarily affects the adult life stage, and larvae are able to use Populus species by avoiding these defenses. Resistance to poplars involves tree phenolic glycoside content, which acts as a feeding deterrent at high concentrations and a toxin at mid- to low concentrations. Larvae growing inside the tree do not come into contact with these compounds except at very low levels because the concentrations in wood are orders of magnitude higher in the bark than in wood. The gut fungal symbiont of ALB was found to be required for the insect to degrade the core lignin molecule in wood. Goal: Determine the role of bacteria in mediating induced plant responses by beetle and caterpillar feeding. Sampling of FAW collected from different fields and different crop plants showed that caterpillar gut communities were based more on food source (soybean vs. corn) than egg source, suggesting that most gut bacteria are acquired from the environment. However, FAW and corn earworm from the same site had different gut communities even when fed on the same food source. Regurgitant and gut communities were not different from each other, indicating that bacteria in regurgitant are derived from the gut of the larvae. There was no evidence that FAW gut bacteria affected attraction ofthe parasitoid wasp C. marginiventris to damaged corn plants, but we did find some evidence that FAW oral bacteria partially suppressed the production of extra-floral nectar in cotton plants. Goal: Determine the impact of induced defenses in soybean on performance and pathogenesis of SfMNPV against S. frugiperda. Induction of defenses in soybean foliage reduced the ability of a viral insect pathogen (baculovirus) to kill FAW. However, there was variability among soybean varieties in whether induced defenses interfered with baculovirus infections. Soybean varieties and induced defenses influenced the number of progeny virus produced in infected hosts. Genetic variation and induced defenses in plants against herbivores can influence the performance of insect pathogens and viral fitness. Goal: Use genetic markers to identify the origin of invading populations of spotted lanternfly (SLP), a recent invasive species introduced into PA with a broad host range. We initially used genetic markers developed in Korea where SLF invaded in 2004 and from this work, concluded that SLF in PA did not originate from Korea. These markers did not provide the information needed to identify the origin of invasion, as they failed to match up to sampled populations in China and Vietnam. Goal: Characterize the bacterial and fungal associates of spotted lanternfly (SLF) to allow us to assess the potential for pathogen transmission, to identify host plant requirements and/or preferences associated with microbial symbionts harbored by SLF, or to identify potential natural microbial pathogens of SLF that can be used for control. We used next-gen DNA sequencing to test for the presence of microbial communities in SLF salivary glands, the proboscis (used for feeding) and in abdominal tissue. We found that salivary gland and proboscis tissue did not harbor any detectable levels of microbes, indicating that it is unlikely that SLF is directly transmitting specific microbial pathogens to plants through feeding. SLF abdominal tissue harbors a bacterial community dominated by three endosymbionts (Sulcia muelleri, Vidania fulgoroideae, and an uncharacterized Gammaproteobacterium). The SLF microbiome was statistically significantly different from that of other closely related taxa within the same planthopper family. We compared bacterial associates of SLF from Korea and China and found that the microbiome of SLF in invaded ranges (PA and Korea) is significantly less taxonomically diverse than that of SLF in their natural range. Therefore, while all SLF share the same obligate bacterial endosymbionts, populations differ with respect to the facultative (non-obligate) bacteria they harbor, likely residing within the SLF digestive tract. Across the life cycle of nymphs and adults of SLF in 2017, we sampled microbial communities present on plants (the SLF preferred host "tree of heaven", black walnut, cultivated grape, and wild grape) fed upon by SLF when plants were in their healthy state and over time as sooty mold developed. We will use DNA sequencing to characterize microbial communities present on plants over time. We hope to identify beneficial bacteria (and through culturing, potentially the antimicrobial compounds they produce) that are present in healthy plants but swamped out by sooty mold. These may be used to reduce and even kill sooty mold associated with SLF honeydew deposition. Goal: To understand the molecular mechanisms of flight muscles that allow large insects to fly and disperse. Studies on flight mechanisms in dragonflies, hawkmoths, and bumblebees were addressed. In two of these insect systems, the muscle protein Troponin T was found to control the ability of insects to support their full body weight in flight. We recently found (publication in preparation) that parasitic infections negatively affect Troponin T expression in dragonflies, and are working on extending these findings to the hawkmoth and bumblebee systems. We recently published an experimental method using fruit flies to allow us to identify the genetic mechanisms controlling flight muscle protein Troponin T expression. Based on this fruit fly work, we aim to develop Troponin T expression suppression approaches in other insect systems,.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Limbu, S., M. Keena, F. Chen, G. Cook, H. Nade, and K. Hoover. 2017. Effects of temperature on development of Lymantria dispar asiatica and Lymantria dispar japonica (Lepidoptera: Erebidae). Environ. Entomol., 46(4):10121023.
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Shikano, I., E. McCarthy, B. D. Elderd and K. Hoover. 2017. Plant genotype and induced defenses affect the productivity of an insect-killing obligate viral pathogen. J Invertebr. Pathol. 148:34-42.
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Mason, CJ, Long, DL, Nagachar, N, McCarthy, EM, Scully, ED, Rosa, C, Tien, K Hoover. 2017. Within gut physicochemical variation does not correspond to distinct fungal and bacterial communities in the tree-killing xylophage, Anoplophora glabripennis. J Insect Phys. 102 (2017) 2735
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Shikano, I., K.L. Shumaker, M. Peiffer, G.W. Felton and K. Hoover. 2017. Compatibility of baculoviruses with plant defence against insect pests depends on intraspecific genetic variation in plant defence traits. Oecologia 183:11211134.
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Wang, J., M. Peiffer, K. Hoover, C. Rosa, R. Zeng, G. W. Felton. 2017. Helicoverpa zea gut-associated bacteria indirectly induce defenses in tomato through mediating salivary elicitor(s). New Phytologist doi: 10.1111/nph.14429.
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Chung, S.H., E.D. Scully, M. Peiffer, S.M. Geib, C. Rosa, K. Hoover and G.W. Felton. 2017. Host plant species determines symbiotic bacterial community mediating suppression of plant defenses. Scientific Reports 7:39690 DOI: 10.1038/srep39690.
- Type:
Journal Articles
Status:
Published
Year Published:
2016
Citation:
Limbu, S., K. Cassidy, P. Tobin, M. Keena, and K. Hoover. 2016. Host specificity of Scymnus camptodromus for biological control of hemlock woolly adelgid. Environ. Entomol. 17 doi: 10.1093/ee/nvv174.
- Type:
Journal Articles
Status:
Under Review
Year Published:
2017
Citation:
A. Black, R. J. Schilder, S. R. Kimball (2017). Palmitate- and C6 ceramide-induced Tnnt3 pre-mRNA alternative splicing occurs in a PP2A dependent manner. Cellular Signaling (in review).
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Black, A. J., Ravi, S., Jefferson, L. S., Kimball, S. R., Schilder, R. J. (2017). Dietary fat quantity and type induces transcriptome-wide effects on alternative splicing of pre-mRNA in rat skeletal muscle. Journal of Nutrition 147(9):1648-1657
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Schilder, R. J., Raynor, M. (2017). Molecular plasticity and functional enhancements of leg muscles in response to hypergravity in the fruit fly Drosophila melanogaster. J Experimental Biology 220 (Pt 19):3508-3518.
- Type:
Journal Articles
Status:
Under Review
Year Published:
2017
Citation:
Paladini, A., Takiya, D., Urban, J.M., and Cryan, J.R. In review. A time-calibrated phylogeny and evolution of aposematic coloration in New World spittlebugs (Hemiptera: Cercopidae: Ischnorhininae). Molecular Phylogenetics & Evolution (in review).
- Type:
Journal Articles
Status:
Under Review
Year Published:
2017
Citation:
Mason, C.J., A.M. Campbell, E.D. Scully and K. Hoover. 2017. Bacterial and fungal midgut community dynamics and transfer between mother and brood in an invasive xylophage. Microbial Ecology, (in review).
- Type:
Book Chapters
Status:
Published
Year Published:
2017
Citation:
Ment, D., Shikano, I. & Glazer, I. (2017) The Abiotic Environment, In: Hajek, A.E. & Shapiro-Ilan, D. (Eds.), Ecology of Invertebrate Diseases. Wiley. (ISBN: 978-1-119-25607-6)
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Shikano, I. (2017) Evolutionary ecology of multitrophic interactions between plants, insect herbivores and entomopathogens. Journal of Chemical Ecology 43:586-598.
- Type:
Journal Articles
Status:
Published
Year Published:
2017
Citation:
Shikano, I., Rosa, C., Tan, C-W. & Felton, G.W. (2017) Tritrophic interactions: microbe-mediated plant effects on insect herbivores. Annual Review of Phytopathology 55:313-331
|
Progress 10/01/15 to 09/30/16
Outputs
Target Audience:The USDA-APHIS, USDA-Forest Service, and state agricultural agencies will benefit from our studies on ALB and Asian gypsy moth. The USDA, chemical ecologist, and crop managers will benefit from studies on plant-insect-symbiont interactions, and effects of plant defenses on performance of baculoviruses. Changes/Problems:Due to the significant losses in the S. camptodromus colony, the remaining beetles will be confined this fall to hemlocks infested with hemlock woolly adelgid in the hoop house that was established with planted hemlocks trees several years ago. These trees are well infested and as soon as egg laying by the adelgids begins, we will put the remaining beetles in this location to determine if mass rearing is possible. This was a goal of our project and although the funding cycle has expired, we would like to see if we can revive the predator colony using this approach. A newinvasive species, the Spotted Lanternfly, Lycorma delicatula, was detected in Pennsylvania in September2014. This insect is known to use cultivated grape, fruit trees, and hardwood species, andhas thepotential to cause serious economic damage to these industries. The Spotted Lanternfly directly damages plants viaphloem feeding, but also incurs serious secondary damage due to sooty mold that builds up on the insects' sugary excretions, blocking plant photosynthesis.As such, there is need to extend the current project to include research on this insect, in order to understand insect-plant-microbe interactions and to potentially improve control of this insect. What opportunities for training and professional development has the project provided?In the Hoover lab, 4 graduate students and 2 postdocs were trained on this project. These individuals have also attended and given presentations at scientific conferences (including an international conference), and attended grant writing workshops, and teaching workshops. One postdoc wrote and received a prestigious grant from the Canadian government that covers most of his salary for two years. One graduate student received extensive training from US Forest Service personnel in how to use modeling software. In the Schilder lab, three graduate students in Biology and Entomology, respectively (as well as four undergraduate students) received training on these projects. In the Felton lab, two graduate students were trained on this project as part of their dissertation research. How have the results been disseminated to communities of interest?Results have been published in peer-reviewed journals and presented at scientific meetings. Results related to management of ALB have been conveyed to appropriate USDA-APHIS personnel. Results on the effects of temperature on development of Asian gypsy moth have also been conveyed to USDA-APHIS and US Forest Service to assist with monitoring for introductions of this pest in the U.S. What do you plan to do during the next reporting period to accomplish the goals?A new collaboration is starting up with Rick Lindroth at University of Wisconsin to determine how ALB is metabolizing salicinoids in different regions of the gut to determine why the anterior midgut is the most impacted region of the gut and the mechanisms of toxicity to ALB. Next summer we will go to Inner Mongolia where there is a population of ALB that is attacking poplar plantations to continue the study of potential geographic differences in ALB susceptibility to salicinoids. My graduate student will also travel to this region next summer to collect samples of ALB eggs and larvae to determine if F. solani is associated with these populations as well. An extensive phylogenetic analysis will tell us about the radiation of F. solani among geographic populations of ALB in the native and introduced range. Comparative genomics will be performed on F. solani isolates from N. America in comparison with isolates from ambrosia beetles and other insects in collaboration with Kerry O'Donnell at the USDA. We will also determine if there are geographic differences in poplar defenses against ALB based on differences in metabolism or in salicinoid content as a result of differences in poplar genotypes planted in different regions of China. The hypothesis that a major function of the ALB fungal symbiont is to degrade lignin in the oviposition site to enable the newly hatched larva to enter the host tree are planned in collaboration with Tim Filley at Purdue and Ming Tien at PSU. RNAi approaches will continue as a means of control for ALB in collaboration with Reddy Palli at University of Kentucky and Cristina Rosa at PSU. Phenology modeling/mapping for Asian gypsy moth is underway in collaboration with Talbot Trotter and Melody Keena of the US Forest Service using our temperature data and USDA-APHIS' trapping data from Japan. The model will allow managers to predict the timing of treatment of second instars and trap deployment for monitoring in North America. Studies on the effects of starvation (as occurs during insect outbreaks) in overcoming developmental resistance in caterpillars to baculovirus infection are planned. Validation of the roles of identified candidate genes in controlling flight muscle function in the dragonfly system, as well as extending these findings in the hawkmoth (M. sexta) system as proof of concept; i.e. this species lends itself more readily for gene manipulation than dragonflies or crickets. Further studies on the role of herbivore-associated microbiota in mediating plant responses to herbivory is underway. Particualr focus is on the bacteria and viruses associated with insect herbivores and their natural enemies.
Impacts
What was accomplished under these goals?
We traveled to China this past summer to determine if there could be geographic differences in Chinese populations of ALB that permit them to use poplar as a host, suggesting that they can detoxify salicinoids while the introduced population cannot. At two field sites near Beijing and Zhejiang Province we found that ALB would not feed on and was not attacking poplar (Populus nigra and P. deltoides hybrids), but they did feed on willow (Salix alba and a S. alba hybrid). Willows are also known to contact salicinoids and are attacked in both China and the introduced range in North America and Europe. Twig samples from these poplars and willow trees were shipped to our collaborators at the University of Georgia for chemical analysis. Results showed that these poplars were very high in salicin and salicortin, while willows were much lower in these salicinoids. Application of salicinoid extracts on maple branches confirmed that ALB live trapped in China would not feed on these compounds. Results to date continue to be consistent with our hypothesis that salicinoids are feeding deterrents to ALB, but if the concentration is low enough they will feed but after a few weeks will suffer a premature death. Autopsies continue to show that the anterior midgut is destroyed and egg loads are significantly depleted in females. The physiological conditions of the ALB gut and how these conditions may influence the microbial composition across gut regions were examined. We measured oxygen tension, pH, and redox potential along the length of the ALB larval gut from two North American field populations. We then analyzed and compared bacterial and fungal gut communities of ALB from these two populations within individual hosts along the length of the gut. The ALB midgut lumen was anoxic, with a pH gradient from 5.5 to 9, moving anterior to posterior. Redox potential was higher in the anterior midgut compared to posterior regions. We observed no differences in gut physiological conditions between the two populations. The two beetle populations harbored diverse assemblages of bacteria and fungi, which differed between the geographic locations. However, the composition of the ALB gut microbiota did not differ among gut regions despite physiological differences within a given host. Unlike other insect systems that have distinct gut compartmentalization and corresponding microbial assemblages, the ALB gut lacks such morphological modifications, which may explain why discrete regional microbial community structures were not found along the digestive system. In the summer of 2016 at two field locations in China, ALB eggs were collected and oviposition sites sampled for the fungal symbiont Fusarium solani. By culturing and sequencing, we found that F. solani is also present in larval guts, egg surfaces, and oviposition sites in this region of China. Phylogenetic analyses are underway. Attempts to silence the chitin synthase gene in ALB larvae failed to produce a detectable phenotype despite evidence that dsRNA was present at sufficient levels in the larvae. The ALB genome has been sequenced and the community annotation project for this genome is in review for publication. Bioassays with ALB males showed that the palps on the maxilla and labium are responsible for detection of the female-produced trail sex pheromone. Surgical removal of the last four antennal segments (the region where most of the olfactory receptors are located) and/or the palps showed that males could not detect or follow the trail sex pheromone if the palps were removed, but could still follow the trail with removal of antennal segments. Trapping studies with collaborators at Beijing Forestry University over the past three years have been completed and show that the lure combination of the ALB male-produced long range pheromone (4-(n-heptyloxy)butan-1-ol and 4-(nheptyloxy)butanal) and three plant volatiles ((-)-linalool, trans-caryophyllene, and (Z)-3-hexen-1-ol) caught signi?cantly more ALB and Anoplophora chinensis (citrus longhorned borer or CLB) than controls in China. This lure combination can therefore be used for trapping both species. Both are considered serious invasive species with very broad host ranges. Six different strains of Asian gypsy moth were reared at five different temperatures on artificial diet in quarantine. At temperatures of 10 C or 30 degrees C, development did not occur and the insects ultimately died. A subset of larvae from the 25 degrees C temperature were moved to 30 C for pupation and many of these pupae produced abnormal adults; the females that survived this treatment had significantly reduced fitness (low fecundity and fertility). The temperatures of 20 and 25 °C appeared to be optimum for survivorship to the adult and pupal stages. There were significant differences in development time and survival as a function of temperature. Strains from geographically warmer regions performed better at warmer temperatures while those from cooler climates performed better at low temperatures. Levels of Spodoptera frugiperda (fall armyworm or FAW) mortality inflicted by S. frugiperda multiple nucleopolyhedrovirus (SfMNPV) did not vary among soybean 8 genotypes when the virus was ingested with non-induced foliage. Ingestion of the virus on induced foliage reduced FAW mortality, relative to mortality on non-induced foliage, on some but not all soybean genotypes. Baculovirus efficacy was lower when ingested with foliage that contained higher phenolic content and defensive properties that reduced FAW weight gain and leaf utilization. However, soybean genotypes that defended the plant by reducing FAW feeding rate and strongly deterred feeding upon JA-induction did not reduce baculovirus efficacy. We also found that induction of the JA-signaling pathway in soybean can overcome intrastadial developmental resistance in the FAW to the baculovirus SfNPV. We continued work on defining the set of genes involved in flight muscle functional plasticity in insects, which will lead to the development of conditional RNAi or knockout/down targets that can be used in (m)any pest insect species to prevent dispersal; a key factor in pest impact. The earlier reported cricket system has been abandonded, instead, two graduate students are working on flight muscle plasticity in two flying insect systems; (hemimetabolous) libellulid dragonflies and (holometabolous) Manduca sexta hawkmoths. In both these insect systems, alternative splicing of the sarcomere gene Troponin T appears to control flight muscle functional plasticity and ability to support body weight in flight. Our longer term goals are to elucidate the upstream mechanisms that control this process in insects, so that we can initiate suppression approaches (i.e. control the process of troponin T alternative splicing and affect flight performance in vivo). In the dragonfly system, through genome-wide SNP association mapping we have identified several candidate genes controlling tracheal development and flight muscle fuel mobilization as additional targets for such approaches.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2016
Citation:
Mason, C., Scully, E., Rosa, C.R., Long, D., McCarthy, E. and K. Hoover. 2016. Contrasting diets reveal metabolic plasticity in the tree-killing beetle, Anoplophora glabripennis (Cerambycidae: Lamiinae). Scientific Reports 6:33813 | DOI: 10.1038/srep33813.
- Type:
Journal Articles
Status:
Accepted
Year Published:
2016
Citation:
Graves, F., T. Baker, A. Zhang, M.A. Keena, and K. Hoover. 2016. Sensory aspects of trail-following behaviors in the Asian longhorned beetle, Anoplophora glabripennis. J Insect Behavior, (in press).
- Type:
Journal Articles
Status:
Published
Year Published:
2016
Citation:
Herr, J.R., E.D. Scully, S.M. Geib, J.E. Carlson, and D.M. Geiser. 2016. Genome sequence of Fusarium Isolate MYA-4552 from the midgut of Anoplophora glabripennis, an invasive, wood-boring beetle. Genome Announcements 4(4) e00544-16.
- Type:
Journal Articles
Status:
Published
Year Published:
2016
Citation:
Wang, J., et al. (2016). Herbivore oral secreted bacteria trigger distinct defense responses in preferred and non-preferred host plants. Journal of Chemical Ecology 42(6):463-474.
- Type:
Journal Articles
Status:
Under Review
Year Published:
2016
Citation:
Mason, C.J., D. Long, E.M. McCarthy, C. Rosa, E.D. Scully and K. Mason, C.J., D. Long, E.M. McCarthy, C. Rosa, E.D. Scully and K. Hoover. 2016. Influence of population source and gut physiological conditions on fungal and bacterial communities in a tree-killing, xylophagous insect. Applied Environmental Microbiology, (in review).
- Type:
Journal Articles
Status:
Under Review
Year Published:
2016
Citation:
Acevedo, F.E., M. Peiffer, C.W. Tan, B.A. Stanley, A. Stanley, K. Acevedo, F.E., M. Peiffer, C.W. Tan, B.A. Stanley, A. Stanley, K. Hoover, C. Rosa, D. Luthe and G.W. Felton. 2016. Fall armyworm-associated gut bacteria modulate plant defense responses. Mol. Plant-Microbe Interactions, (in review).
- Type:
Journal Articles
Status:
Published
Year Published:
2016
Citation:
RJ Schilder (2016). (How) do animals know how much they weigh?. Journal of Experimental Biology 219 (9), 1275-1282. (invited review)
- Type:
Journal Articles
Status:
Published
Year Published:
2016
Citation:
S Bybee, A C�rdoba-Aguilar, M. Catherine Duryea, R Futahashi, B Hansson, M. Olalla Lorenzo-Carballa, R Schilder, R Stoks, A Suvorov, E I Svensson, J Swaegers, Y Takahashi, P C Watts and M Wellenreuther (2016). Odonata (dragonflies and damselflies) as a bridge between ecology and evolutionary genomics. Frontiers in Zoology 13, 46.
- Type:
Journal Articles
Status:
Accepted
Year Published:
2016
Citation:
O Evangelista, AM Sakakibara, JR Cryan and JM Urban. A phylogeny of the treehopper subfamily Heternotinae reveals convergent pronotal traits (Hemiptera: Auchenorrhyncha: Membracidae). Systematic Entomology, (in press).
- Type:
Journal Articles
Status:
Under Review
Year Published:
2016
Citation:
JL Stevens, RR Dunn, JM Urban. Rhizosphere bacterial recruitment by the common dandelion (Taraxacum officinale) from diverse soils. PlosOne, (under review).
- Type:
Journal Articles
Status:
Published
Year Published:
2016
Citation:
Swayamjit Ray, Patrick CMS Alves, Imtiaz Ahmad, Iffa Gaffoor, Flor E Acevedo, Michelle Peiffer, Shan Jin, Yang Han, Samina Shakeel, Gary W Felton, Dawn S Luthe. Turnabout is fair play: Herbivory-induced plant chitinases excreted in fall armyworm frass suppress herbivore defenses in maize. Plant Physiology 171:694-706.
- Type:
Journal Articles
Status:
Published
Year Published:
2016
Citation:
Swayamjit Ray, Saumik Basu, Loren J Rivera-Vega, Flor E Acevedo, Joe Louis, Gary W Felton, Dawn S Luthe. 2016. Lessons from the far end: caterpillar frass-induced defenses in maize, rice, cabbage, and tomato. Journal of Chemical Ecology 1-12 (published online).
|
Progress 12/01/14 to 09/30/15
Outputs
Target Audience:The USDA-APHIS, USDA-Forest Service, and state ag agencies will benefit from our findings on mechanisms of resistance against Asian longhorned beetle (ALB) in poplar species, which is apparent in the US, and development of gene silencing methods that have the potential to kill ALB larvae and adults that feed on genetically engineered trees (a long-term goal). These same agencies, including Pennsylvania Department of Agriculture, national park managers, and the general public will benefit from our efforts to develop mass rearing procedures for a biological control agent of hemlock woolly adelgid. Saving hemlock trees is important to, and falls under the purview of, federal, state, and local government agencies as well as individual homeowners. The scientific community as well as ALB managers will benefit from the studies on mechanisms of plant resistance against ALB and impacts on its gut microbial community. The USDA, chemical ecology scientists, and crop managers will benefit from research on crop pests and plant-biotic interactions. Several graduate students from underrepresented groups were trained on these projects. Changes/Problems:
Nothing Reported
What opportunities for training and professional development has the project provided?Eight graduate students and two postdocs received training on these projects. Professional development was provided as opportunities to write grant proposals and attend/present their research at professional meetings. How have the results been disseminated to communities of interest?Results were disseminated as publications, presentations at scientific meetings, and as reports to government and state agencies with a vested interest in the results. What do you plan to do during the next reporting period to accomplish the goals?Comparative metabolomics will be conducted to further characterize differences in not just phenolic glycoside content, but other plant seconary metabolites in Chinese poplar vs. eastern cottonwood. In addition, we plan to further characterize differences in PG content among different poplar genotypes to determine which genotype of cottonwood is best suited to this study. Mechanisms of resistance in adult ALB will be pursued from both a physiological and morphological perspective. RNAi studies for genes that can be silenced with fatal results in ALB larvae will continue adding a new gene that has less redundancy now that the ALB genome has been sequenced (but not yet published). To continue mass rearing studies we will work to increase the infestation level of hemlock woolly adelgids in our hoophouse and release predator larvae in the late winter. If the USDA NAPPO is approved, mass rearing procedures will also be evaluated in the field at Cornell University. Longitudinal transcriptomics during (naturally occurring) flight muscle degeneration in the cricket species (gryllus firmus) to identify more proximate gene targets controlling this phenotype switch; develop RNAi methods in this system first, test them in other species once successful.
Impacts
What was accomplished under these goals?
Resistance mechanisms in Chinese poplar to ALB were found to occur primarily against adults during feeding on poplar branches, regardless of plant genotype. In choice experiments, adults avoid feeding on poplar and in no choice experiments died prematurely. Upon dissection the anterior midgut of these beetles had been destroyed. Levels of phenolic glycosides salicortin and tremuloidin were found particularly high in Chinese poplar (Populus tomentosa) in comparison with native Eastern cottonwood (Populus deltoides). Application of extracted phenolic glycosides to maple branches produced similar early mortality and the same mechanism of death in adults. Eggs deposited into poplar trees rarely eclosed to larvae and those oviposited into Chinese poplar failed to hatch at all. Addition of extracted phenolics retarded larval develop of ALB in a dose dependent manner and also deter feeding. Work is ongoing on silencing the beetle gene chitin synthase. Mass rearing procedures for Scymnus camptodromus for control of hemlock woolly adelgid are still in progress in a hoop house at the field site on Penn State property. Experiments were completed in the last year to finalize host range studies of the predator and a NAPPO application was filed to allow field release of the predator once mass rearing procedures are in place. Among several projects, my lab is working on defining the set of genes involved in controlled flight muscle degeneration in insects, which will lead to the development of conditional RNAi or knockout/down targets that can be used in (m)any pest insect species to prevent dispersal; a key factor in pest impact. A graduate student is currently developing the infrastructure for this project. We have confirmed that bacteria play an important role for suppression of defenses for both Spodoptera frugiperda and Helicoverpa zea. This has been replicated with two years of field data. Our preliminary evidence indicates that gut bacteria also aid in suppression of plant defenses in Trichoplusia ni. We have identified suppressing bacteria from the gut and oral secretions of S. frugiperda. Pantoea ananatis consistently suppresses defenses when reintroduced into larvae. We have consistently ound this bacterium in the oral secretions and guts of larvae collected at our research site at Rock Springs, PA. Re-introduction of a specific Raoultella from H. zea causes suppression of defenses during larval feeding. We are still identifying further gut bacteria involved in suppression. We have found that specific bacteria affect the production of salivary HAMPs and effectors. In addition to the preliminary data in our proposal, we have since found that recombinant salivary phospholipase C (PLC) from H. zea elicits jasmonate regulated defenses in maize such as maize proteinase inhibitor and ribosome inactivating protein. This is in contrast to tomato where PLC suppresses defenses. We will determine if bacteria play a role in mediating PLC activity and expression. Induced defenses in soybean were found to reduce larval growth and viral-induced mortality in fall armyworm.
Publications
- Type:
Journal Articles
Status:
Published
Year Published:
2014
Citation:
Scully, ED, Geib, SM, Carlson, JE, Tien, M, and Hoover, K. 2014. Functional genomics and microbiome profiling of the Asian longhorned beetle (Anoplophora glabripennis) reveal new insights into the digestive physiology and nutritional ecology of wood feeding beetles. BMC Genomics, 15:1096, DOI: 10.1186/1471-2164-15-1096.
- Type:
Journal Articles
Status:
Published
Year Published:
2014
Citation:
Meng, P., R.T. Trotter, M.A. Keena, T. Baker, S. Yan, E. Schwartzberg, and K. Hoover. 2014. Effects of pheromone and plant volatile release rates and ratios on trapping Anoplophora glabripennis in China. Environ. Entomol., 43(5):1379-1388
- Type:
Journal Articles
Status:
Published
Year Published:
2015
Citation:
Limbu, S., M.A. Keena, D. Long, N. Ostiguy and K. Hoover. 2015. Scymnus camptodromus larval development and predation of hemlock woolly adelgid (Hemiptera: Adelgidae). Environ. Entomol. 44:81-89.
- Type:
Journal Articles
Status:
Published
Year Published:
2014
Citation:
Hoover, K., M. Keena, M. Nehme, S. Wang, P. Meng and A. Zhang. 2014. Sex-specific trail pheromone mediates complex mate finding behavior in Anoplophora glabripennis. J Chem Ecol. 40:169-180.
- Type:
Journal Articles
Status:
Awaiting Publication
Year Published:
2015
Citation:
Ayayee, P., T. Larsen, C. Rosa, G. Felton, G. Ferry, and K. Hoover. 2015. Essential amino acid provisioning by gut microbes of a wood feeding cerambycid. Environ. Entomol., in press.
- Type:
Journal Articles
Status:
Published
Year Published:
2015
Citation:
Acevedo FE, Rivera-Vega LJ, Chung SH, Ray S, Felton GW: Cues from chewing insectsthe intersection of DAMPs, HAMPs, MAMPs and effectors. Current Opinion in Plant Biology 2015, 26:80-86.
- Type:
Journal Articles
Status:
Published
Year Published:
2015
Citation:
Louis J, Basu S, Varsani S, Castano-Duque L, Jiang V, Williams WP, Felton GW, Luthe DS: Ethylene contributes to maize insect resistance1-mediated maize defense against the phloem sap-sucking corn leaf aphid. Plant Physiology 2015, 169:313-324.
- Type:
Journal Articles
Status:
Published
Year Published:
2015
Citation:
Limbu, S., K. Cassidy, P. Tobin, M. Keena, and K. Hoover. 2015. Host specificity of Scymnus camptodromus for biological control of hemlock woolly adelgid. Environ. Entomol. 44:81-89.
- Type:
Journal Articles
Status:
Published
Year Published:
2015
Citation:
Meng, P., K. Hoover and M.A. Keena. 2015. Detection and management of Anoplophora glabripennis in the United States. J Integrated Pest Management, 6(1):4, DOI: 10.1093/jipm/pmv003.
- Type:
Journal Articles
Status:
Awaiting Publication
Year Published:
2015
Citation:
Kung, W., K. Hoover and R.T. Trotter. 2015. Long term effects of imidacloprid on canopy arthropod biodiversity on eastern hemlock in New England. Northeastern Naturalist, in press.
- Type:
Journal Articles
Status:
Published
Year Published:
2015
Citation:
Ray S, Gaffor I, Acevedo FE, Helms A, Chuang W-P, Tooker J, Felton GW, Luthe DS: Maize plants recognize herbivore-associated cues from caterpillar frass. Journal of Chemical Ecology 2015, 41:781-792.
- Type:
Journal Articles
Status:
Published
Year Published:
2015
Citation:
Coble J., R. J. Schilder, A. Berg, M. Drummond, B. B. Rasmussen, S. R. Kimball (2015). Influence of ageing and essential amino acids on quantitative patterns of troponin T alternative splicing in human skeletal muscle. Applied Physiology, Nutrition, and Metabolism. 10.1139/apnm-2014-0568
- Type:
Journal Articles
Status:
Published
Year Published:
2015
Citation:
Ravi S., Schilder R., Kimball S. (2015). Role of Pre-mRNA Splicing in Nutrient-Induced Alterations in Gene Expression and Metabolism. Journal of Nutrition. Mar 11. pii: jn203216.
- Type:
Journal Articles
Status:
Published
Year Published:
2014
Citation:
Zera, A J, C. Wehrkamp, R. Schilder, C. Black, and P. Gribben (2014). Purification and Characterization of 6-Phosphogluconate Dehydrogenase From the Wing-Polymorphic Cricket, Gryllus Firmus, and Assessment of Causes of Morph-Differences in Enzyme Activity. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology. doi:10.1016/j.cbpb.2014.04.001.
- Type:
Journal Articles
Status:
Published
Year Published:
2014
Citation:
N. N. Vellichirammal, A. J. Zera, R. J. Schilder, C. Wehrkamp, J-J. M. Riethoven, J. A. Brisson (2014). De novo transcriptome assembly and morph-specific gene expression profiling of the wing polymorphic cricket Gryllus firmus. PLoS ONE DOI: 10.1371/journal.pone.0082129.
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