Source: PENNSYLVANIA STATE UNIVERSITY submitted to NRP
HARNESSING CHEMICAL ECOLOGY TO ADDRESS AGRICULTURAL PEST AND POLLINATOR PRIORITIES
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
HATCH
Reporting Frequency
Annual
Accession No.
1007907
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
NE-1501
Project Start Date
Oct 1, 2015
Project End Date
Sep 30, 2020
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
PENNSYLVANIA STATE UNIVERSITY
208 MUELLER LABORATORY
UNIVERSITY PARK,PA 16802
Performing Department
Entomology
Non Technical Summary
The research will involve the use of chemical elicitors of plant resistance such as jasmonic acid and silica to induce plant resistance to pest insects. The application of these elicitors are being tested as seed treatments that will mitigate costs and application requirements. The elicitors will be tested in greenhouse and field based experiments where resistance will be measured as well as plant yields. Work on non-target effects of popular pest management tacticswill involvecharacterizingeffects of pesticides on pollinators, herbivores, and natural enemies of pests including unexpected routes of exposure and consequences of over-reliance on pesticides on non-target community members that arerelevant to pest control and pollination.
Animal Health Component
50%
Research Effort Categories
Basic
50%
Applied
50%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2111461113020%
2111460113040%
7211820113040%
Knowledge Area
211 - Insects, Mites, and Other Arthropods Affecting Plants; 721 - Insects and Other Pests Affecting Humans;

Subject Of Investigation
1460 - Tomato; 1461 - Peppers; 1820 - Soybean;

Field Of Science
1130 - Entomology and acarology;
Goals / Objectives
Develop chemical ecology tools and information to support sustainable agriculture by reducing damage by pests in crops such as potatoes, brassicas, cucurbits, apples, blueberries, and sweet corn, while maintaining pollinator health in agricultural systems. Define variability of chemically mediated interactions between pests, crops, and beneficial organisms in terms of plant chemistry, species interactions and landscape factors in the Northeast. Characterize the non-target effects of pesticides on pollinators and natural enemies of pests. Establish a chemical ecology analytical facility for the Northeast to allow researchers ready access to equipment and technical expertise. Extension to facilitate adoption and awareness of science-based chemical ecology tools to support sustainable production.
Project Methods
Our projects involve both a field and laboratory component and will focus on tomatoes, peppers, maize, and soybeans among others. Field work will involved community characterization andanalyses to understand the influence of potential management tactics on pest and natural enemy communities.Chemical analyses, typically including liquid and gas chromatography, mass spectrometry, or spectrophotometry will be employed in the research projects.

Progress 10/01/15 to 09/30/20

Outputs
Target Audience:Entomologists, plant scientists, extension professionals, farmers, other agricultural professionals Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Four graduate students who have participated in these projects have graduated with Ph.D.s and are employed in academic positions (postdoctoral, faculty). Four postdoctoral scientists have participated and one is now employed in a faculty position. How have the results been disseminated to communities of interest?Presentations by faculty, postdocs, and graduate students have been presented at the Entomological Society of America, Ecological Society, and International Society of Chemical Ecology annual meetings. 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. Tooker/Felton/Tumlinson/Baker - We studied maize (cvB73) and teosinte (Zea mays ssp. parviglumis) to determine if they can detect the pheromones of fall armyworm (FAW). We exposed plants to FAW pheromones or the pheromones of sunflower head moth (SHM; Homeosoma electellum), an unassociated lepidopteran that acted as a chemical control. Following pheromone exposure, we allowed FAW caterpillars to feed on exposed and unexposed plants. We found feeding damage was reduced on maize plants that were exposed to FAW and SHM pheromone emissions and teosinte plants that were exposed to only FAW pheromone emissions. Salivary glucose oxidase (GOX)in larval Helicoverpa zeahas been hypothesized to benefit H. zea by modulating direct defense responses of plants.Using six different plants in Solanaceae, including tomato (Solanum lycopersicum cv. Better Boy and S. lycopersicum var. cerasiforme), bell pepper, habanero pepper, tomatillo, and tobacco (N. benthamiana), we tested the impact of GOX on induction of two common defense proteins, trypsin protease inhibitors (TPI) and polyphenol oxidases (PPO), and on relative growth rate of H. zea. GOX specifically induced TPI activity in tomato and habanero pepper, and level of defense protein depended on leaf location. Changes in performance in tomato and habanero pepper matched the induction of TPI. Our findings indicate that GOX induces similar defense responses in some Solanacean plants, but largely depends on species/genotype of plant. Crop domestication and selective breeding have altered plant defense mechanisms, influencing insect-plant interactions.In ourstudies, the inducibility of several plant defense mechanisms (e.g., defensive chemicals, trichomes, plant volatiles) were investigated, and the performance and preference of the herbivore H.zea were measured in three different tomato genotypes; a) wild tomato, Solanum pimpinellifolium L. (accession LA 2093), b) cherry tomato, S. lycopersicum L. var. cerasiforme (accession Matts Wild Cherry), and c) cultivated tomato, S. lycopersicum L. var. Better Boy). Enhanced inducibility of defensive chemicals, trichomes, and plant volatiles in the cultivated tomato, and a higher level of constitutive plant resistance against herbivory in the wild genotype was observed. When comparing the responses of damaged vs. undamaged leaves, the percent reduction in larval growth was higher on damaged leaves from cultivated tomato, suggesting a higher induced resistance compared to other two genotypes. While all tomato genotypes exhibited increased volatile organic compound (VOCs) emissions in response to herbivory, the cultivated variety responded with generally higher levels of VOCs. Differences in VOC patterns may have influenced the ovipositional preferences, as H. zea female moths significantly preferred laying eggs on the cultivated versus the wild tomato genotypes. Goal 2. Ali/Felton/Acevedo/Hermann - Ongoing studies have focused on how the insect pest's microbiome may influence plant resistance and plant defenses. Specific manipulation of the microbiome could offer new approaches for insect control. For instance, many plant defenses target the insect digestive system, with some altering the protective peritrophic matrix (PM) and causing increased permeability. The PM is responsible for multiple digestive functions, including reducing infections from potential pathogenic microbes. In our study, we developed axenic and gnotobiotic methods for FAWand tested how particular members present in the gut community influence interactions with plant defenses that can alter PM permeability. Axenic insects grew more but displayed lower immune-based responses compared with those possessing Enterococcus, Klebsiella, and Enterobacter isolates from field-collected larvae. Our results strongly suggest 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 indirectmicrobe-mediated assaults by maize defenses on FAWon the insect digestive and immune system reduced growth and elevated mortality in these insects. In other studies, we have found that the microbiome has a strong influence on the ability of insect pests to trigger induced resistance in plants. We identified five secreted fungi from black cutwormincluding Aspergillus parasiticus, Aspergillus niger, Geotrichum candidum, Fusarium subglutinans, and Mucor circinelloides f. lusitanicus. We found that caterpillars inoculated with F. subglutinans or M. circinelloides f. lusitanicus induced higher defense responses in plants, but with different patterns between different plants. These herbivore-induced defense responses reduced the growth of caterpillars. However, direct application of fungi to mechanically wounded tomato did not induce JA-related defense responses. Our finding suggests that insect-associated fungi could influence plant-insect interactions by indirectly mediating plant defense responses, and directly affecting caterpillar performance on host plants. Other research is demonstrating how other organisms in the environment may influence the outcome of plant resistance to insect pests. Here, we investigated plant and insect responses to chemical cues from below ground natural enemies and explored the ecological significance of these cues for multitrophic interactions. More specifically, we examined the influence of odors emitted by entomopathogenic nematodes (EPNs), a natural enemy of insect herbivores, on the performance and behavior of their insect prey and the defense responses of nearby plants.Our findings revealed that EPN-infected insect cadavers emit a characteristic blend of volatile compounds with bioactivity in plants and insects. EPN chemical cues influenced both performance and preference of a specialist herbivore, Colorado potato beetle (CPB, Leptinotarsa decemlineata), feeding on its host plant, potato (Solanum tuberosum). CPB larvae consumed less leaf tissue and gained less mass feeding on plants exposed to EPN cues compared to control plants. Female CPBs laid fewer eggs on plants with EPN cues than on controls, indicating deterrence by EPN cues or EPN-altered plant defenses. Goal 3. Tooker/Amsalem - Research using the abundant native pollinator Bombus impatiens and neonicitinoid imidacloprid demonstrate that environmentally realistic chronic exposure to sublethal amounts of imidacloprid in females reduced mating attempts by males toward queens. Preliminary results show that imidacloprid exposure interferes with production and perception of female sex pheromones that mediate mating behavior in queens. In the reciprocal experiment with imidacloprid chronically fed males, we found no preference by queens towards exposed and non-exposed males in either behavioral assays or in antennal responses of queens to male sex pheromones. Understanding how pesticide exposure affects insect mating will inform pesticide use and guide development ofremedies. Insecticides use in field crops has grown increasingly prophylactic, posing unnecessary risk to arthropod decomposers. Decomposers (including millipedes, soil mites, and Collembola)act as alternative prey for generalist predators, facilitate crop-residue breakdown, and can influence nutrient cycling. We conducted a three-year field experiment in no-till corn and soybean fields to assess how neonicotinoid seed coatings or broadcast applications of a pyrethroid insecticide affect arthropod decomposers and litter decomposition. Both insecticides reduced densities of arthropod decomposers and decomposition of plant litter. Neonicotinoid seed coatings reduced collembolan and millipede densities, while pyrethroid significantly reduced soil mite and millipede densities. Widespread use of prophylactic insecticides is likely to have concerning negative effects on the availability of alternative prey, plant residue breakdown, and nutrient cycling in field crops.

Publications

  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Mason, C. J., Jones, A. G., & Felton, G. W. (2019). Co-option of microbial associates by insects and their impact on plantfolivore interactions. Plant, Cell & Environment, 42(3), 1078-1086.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Mason, C. J., St. Clair, A., Peiffer, M., Gomez, E., Jones, A. G., Felton, G. W., & Hoover, K. (2020). Diet influences proliferation and stability of gut bacterial populations in herbivorous lepidopteran larvae. Plos one, 15(3), e0229848.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Tan, C. W., Peiffer, M. L., Ali, J. G., Luthe, D. S., & Felton, G. W. (2020). Top-down effects from parasitoids may mediate plant defence and plant fitness. Functional Ecology, 34(9), 1767-1778.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Lin, P. A., Peiffer, M., & Felton, G. W. (2020). Induction of defensive proteins in Solanaceae by salivary glucose oxidase of Helicoverpa zea caterpillars and consequences for larval performance. Arthropod-Plant Interactions, 1-9.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Chen, X., Peiffer, M., Tan, C. W., & Felton, G. W. (2020). Fungi from the black cutworm Agrotis ipsilon oral secretions mediate plantinsect interactions. Arthropod-Plant Interactions, 1-10.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Paudel Timilsena, B., Seidl-Adams, I., & Tumlinson, J. H. (2020). Herbivore-specific plant volatiles prime neighboring plants for nonspecific defense responses. Plant, Cell & Environment, 43(3), 787-800.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Grettenberger, I. M., & Tooker, J. F. (2020). Cultivar mixtures of soybeans have inconsistent effects on herbivore and natural-enemy populations. Agriculture, Ecosystems & Environment, 292, 106835.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Frank, S. D., & Tooker, J. F. (2020). Opinion: Neonicotinoids pose undocumented threats to food webs. Proceedings of the National Academy of Sciences, 117(37), 22609-22613.


Progress 10/01/18 to 09/30/19

Outputs
Target Audience:Entomologists, plant scientist, extension professional, farmers, other agricultural professionals.Research has been presented to scientists and media professionals at multiple scientific meetings including the InternationalSociety of Chemical Ecology,Entomological Society of America, among others. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?A total of 7graduate students are being trained as part of this project. Additionally, one postdoctoral scholar is being mentored as part of the project. Students have presented their findings at the Annual Meeting of Ento Soc and the International Society of Chemical Ecology. How have the results been disseminated to communities of interest?We have presented our science to entomologists and other colleagues at the Joint Annual Meeting of the Entomological Society of America and Entomological Society of Canada, the International Society of Chemical Ecology, and the Phytobiome Meeting (Penn State). What do you plan to do during the next reporting period to accomplish the goals?These are all ongoing projects that will continue under Goals 1 to 3.

Impacts
What was accomplished under these goals? Goal 1: We continue to develop basic knowledge that can be used to build pest management programs that rely less on synthetic insecticides. In a collaborative study with Purdue University, we have recently completed collecting data for a project on the influence of plant phylogenetic relationships, and associated chemical defenses, among plant species on the pest complex that develop on them. We have appear to have found that crops neighboring crop species of different evolutionary divergent times can influence the pest complex that develops on focal plants, and that this effect is strongest toward the end of the season. We have found that the species of cover crop farmers choose has legacy effects on the subsequent corn crop's resistance to the European corn borer, and that this legacy is mediated by soil fertility and/or mycorrhizal colonization. The goal of this proposal is to discover mechanisms that control the cascade of interactions linking cover crops, soil fertility, and corn pest management. We are studying how cover crop-induced changes in corn mycorrhizal colonization and soil nutrients affect constitutive and induced corn defenses against a variety of herbivores; whether the effect of mycorrhizae on corn defense are simply caused by increased nutrient uptake; What effects do cover crop species have on attraction or repellence of corn pests? And how do plants in a field setting respond to herbivore cues when grown after different cover crop species? In greenhouse and field experiments we will evaluate how three cover crop species affect crop plant resistance. We will monitor mycorrhizal colonization, corn metabolic responses, corn resistance to both above- and belowground pests, and pest behavior. This foundational knowledge will advance the prospect that farmers could intentionally select cover crops to effect corn defense against a suite of herbivores. Goal 2: We demonstrated that Green Leaf Volatiles (GLV) emitted by damaged plants are suppressed by caterpillars, thus altering the plant distress signals and interrupting plant communication with beneficial insects and other organisms and suppressing plant defenses. Caterpillars have at least 3 different types of effectors . Two are enzymes, one of which blocks production of the main product of GLV biosynthesis, and the other isomerizes this product. The third effector which we discovered is a small, non protein molecule that reacts with the main GLV product, thus suppressing all subsequent biosynthesis. Caterpillars of different species employ different combinations of these effectors. In other projects we are determining how the insect microbiome can be manipulated to enhance plant resistance. The application of plant beneficial bacteria to improve agricultural production and soil quality has long been of interest. Thus, these insect-associated microbiota have the potential to be developed into effective bio-fertilizers. The bacterium, Enterobacter ludwigii, was isolated from the regurgitant of field-collected tomato fruitworm, Helicoverpa zea. The bacterium can be secreted by the insect onto tomato seeds during fruit feeding and is also commonly found in the soil. When E. ludwigii was applied to germinated tomato seeds, the plants exhibited faster root, shoot and hypocotyl growth, and produced more fruits and seeds than untreated control plants. The plants treated with bacteria exhibited the same activity levels of two key enzymes involved in anti-herbivore defenses, polyphenol oxidase and peroxidase, and induced the same levels of mortality and growth inhibition in H. zea larvae as untreated plants. Thus, our results demonstrate that the application of E. ludwigii to seeds can promote tomato plant growth and yield without compromising anti-herbivore defenses. In another project were are investigating the role of the gut microbiome in enhancing plant defenses in maize and other systems.Many plant defenses target the insect digestive system, with some altering the protective peritrophic matrix (PM) and causing increased permeability. The PM is responsible for multiple digestive functions, including reducing infections from potential pathogenic microbes. In our study, we developed axenic and gnotobiotic methods for fall armyworm (Spodoptera frugiperda) and tested how particular members present in the gut community influence interactions with plant defenses that can alter PM permeability. We observed interactions between gut bacteria with plant resistance. Axenic insects grew more but displayed lower immune-based responses compared with those possessing Enterococcus, Klebsiella, and Enterobacter 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. Our results strongly suggest 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 in these insects. These results imply that plant-insect interactions should be considered in the context of potential mediation by the insect gut microbiome. In a separate project, we continue to study the capacity of plants to "smell" volatile cues associated with their herbivores. We have developed tall goldenrod (Solidago altissima) as a model system because we found that this species can perceive the putative sex pheromone of its specialist herbivore,Eurosta solidaginis, and then alter its defensive status.We have recently determined that the defensive response mounted byS. altissimaprovides protection against feeding byE. solidaginis, the gall-inducing fly that releases the putative pheromone. Building on our work in this system, we established a collaboration with a USDA colleague to see if we can harness this same phenomenon in an applied system to improve pest control. The preliminary data from cranberry, which is attacked by three native lepidopteran species, suggest that cranberry can also detect the pheromones of these pests. Goal 3: Monarchs, migrations and milkweed: We have initiated a pollinator health conservation project linking variation in milkweed defense biochemistry to variation in larval and resulting adult monarch butterfly fitness traits (NSF $897,841 funded May 2018). We are quantifying variation in plant toxicity traits within and across milkweed species using state-of-the-art methods in chemical ecology to determine how plant defense affects larval growth and subsequent adult fecundity, in reproductively active monarch butterfly cohorts. Using a combination of respirometry, flight kinematic analyses, and studies of lipid metabolism, we are examining how milkweed toxicity experienced during larval stages affects adult flight performance and energetics in migratory monarchs and will link these effects to expression of microRNAs controlling traits associated with migratory phenotypes. This project adds a novel perspective to typical chemical ecology practices to studying plant-herbivore interactions by examining physiological consequences of trophic interactions across the entire ontogeny of an herbivorous insect. The project substantially advances the knowledge of the basic biology of the iconic milkweed-monarch butterfly system, a model migratory insect with a complex ecology. In addition, considering the general relevance of how variable environments (including host plant quality) and larval experience affect the biology of flying adult insects, our work is of broad significance to agricultural and vector-borne disease dynamics research. It also provides pertinent information to habitat restoration efforts to offset population declines in beneficial insects.

Publications

  • Type: Journal Articles Status: Published Year Published: 2019 Citation: AC Jones, I Seidl-Adams, J Engelberth, CT Hunter, H Alborn, Tumlinson, JH. 2019. Herbivorous Caterpillars Can Utilize Three Mechanisms to Alter Green Leaf Volatile Emission. Environmental entomology 48 (2), 419-425
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Cofer, T. M., Seidl-Adams, I., & Tumlinson, J. H. (2018). From acetoin to (Z)-3-hexen-1-ol: the diversity of volatile organic compounds that induce plant responses. Journal of agricultural and food chemistry, 66(43), 11197-11208.
  • Type: Journal Articles Status: Accepted Year Published: 2018 Citation: Beck, John J., Hans T. Alborn, Anna K. Block, Shawn A. Christensen, Charles T. Hunter, Caitlin C. Rering, Irmgard Seidl-Adams, Charles J. Stuhl, Baldwyn Torto, and James H. Tumlinson. "Interactions among plants, insects, and microbes: elucidation of inter-organismal chemical communications in agricultural ecology." Journal of agricultural and food chemistry 66, no. 26 (2018): 6663-6674.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Castano-Duque, Lina, Anjel Helms, Jared Gregory Ali, and Dawn S. Luthe. "Plant Bio-Wars: Maize Protein Networks Reveal Tissue-Specific Defense Strategies in Response to a Root Herbivore." Journal of chemical ecology 44, no. 7-8 (2018): 727-745.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Davidson Lowe, Elizabeth, Zsofia Szendrei, and Jared G. Ali. "Asymmetric effects of a leaf?chewing herbivore on aphid population growth." Ecological entomology 44, no. 1 (2019): 81-92.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Malik, R. J., Ali, J. G., & Bever, J. D. (2018). Mycorrhizal composition influences plant anatomical defense and impacts herbivore growth and survival in a life-stage dependent manner. Pedobiologia, 66, 29-35.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Paudel, Sulav, Po-An Lin, Majid R. Foolad, Jared G. Ali, Edwin G. Rajotte, and Gary W. Felton. "Induced Plant Defenses Against Herbivory in Cultivated and Wild Tomato." Journal of chemical ecology 45, no. 8 (2019): 693-707.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Mason, Charles J., Swayamjit Ray, Ikkei Shikano, Michelle Peiffer, Asher G. Jones, Dawn S. Luthe, Kelli Hoover, and Gary W. Felton. "Plant defenses interact with insect enteric bacteria by initiating a leaky gut syndrome." Proceedings of the National Academy of Sciences 116, no. 32 (2019): 15991-15996.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Pan, Qinjian, Ikkei Shikano, Kelli Hoover, Tong-Xian Liu, and Gary W. Felton. "Pathogen-Mediated Tritrophic Interactions: Baculovirus-Challenged Caterpillars Induce Higher Plant Defenses than Healthy Caterpillars." Journal of chemical ecology (2019): 1-10.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Jones, Asher G., Charles J. Mason, Gary W. Felton, and Kelli Hoover. "Host plant and population source drive diversity of microbial gut communities in two polyphagous insects." Scientific reports 9, no. 1 (2019): 2792.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: FE Acevedo, P Smith, M Peiffer, A Helms, J Tooker, GW Felton (2019) Phytohormones in fall armyworm saliva modulate defense responses in plants. Journal of Chemical Ecology, 1-12
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Helms, A. M., S. Ray, N. Matulis, Nina, M. Kuzemchak, W. Grisales, J. F. Tooker, and J. Ali. Chemical cues linked to risk: Cues from below?ground natural enemies enhance plant defences and influence herbivore behaviour and performance. Functional Ecology 33: 798-808.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Yip, E., R. P. Sowers, A. M. Helms, M. C. Mescher, C. M. De Moraes, and J. F. Tooker. Tradeoffs between defenses against different specialist herbivores in goldenrod (Solidago altissima). Invited manuscript. Arthropod-Plant Interactions 13: 279-287.
  • Type: Journal Articles Status: Accepted Year Published: 2019 Citation: Yip, E.; J. F. Tooker, M. C. Mescher, C. M. De Moraes. 2019. Costs of plant defense priming: Exposure to volatile cues from a specialist herbivore alters growth in tall goldenrod, implications for plant fitness. BMC Plant Biology 19: 209
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Pan, Qinjian, Ikkei Shikano, Kelli Hoover, Tong-Xian Liu, and Gary W. Felton. "Enterobacter ludwigii, isolated from the gut microbiota of Helicoverpa zea, promotes tomato plant growth and yield without compromising anti-herbivore defenses." Arthropod-Plant Interactions 13, no. 2 (2019): 271-278.


Progress 10/01/17 to 09/30/18

Outputs
Target Audience:Entomologists, plant scientist, extension professional, farmers, other agricultural professionals Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Two graduate students completed their Ph.D. degrees during this period. How have the results been disseminated to communities of interest?Yes, at scientific and grower meetings. What do you plan to do during the next reporting period to accomplish the goals?These are multifacted projects and work is in progress under all the studies cite under "Accomplishment of Goals". For example, in greenhouse and field experiments we will evaluate how three cover crop species affect crop plant resistance. We will monitor mycorrhizal colonization, corn metabolic responses, corn resistance to both above- and belowground pests, and pest behavior. This foundational knowledge will advance the prospect that farmers could intentionally select cover crops to effect corn defense against a suite of herbivores. We will continue to characterize pest microbiomes and identify specific fungal and bacterial components that can be used to elicit plant resistance and/or promote plant growth and productivity. The Allium leafminer (ALM), Phytomyza gymnostoma (Diptera: Agromyzidae), an invasive species first recorded in the Western Hemisphere in December, 2015. ALM attacks high-value crops in the Allium genus such as onion, garlic, leek, scallions, shallots, and chives; it also threatens an emerging agroforestry crop, and could pose a threat to an endangered Allium. High ALM infestations have occurred in onion and leek fields with as many as 20 pupae per plant, and 100% of plants infested. In PA and NY, some growers have had total losses to their leek crop from ALM.Our work will (1) Identify ALM fly-free periods during the season through studies of phenology and delivery of monitoring programs, (2) Determine the behavioral response of ALM to variation in host species, host growth stages, and plant volatiles, and quantify the within-field distribution of ALM infestations, (3) Enable future opportunities for biological control through baseline natural enemy surveys, building on our finding of parasitism in U.S. populations, and (4) Improve the use of conventional and organic insecticides to manage ALM through efficacy trials, while minimizing flare ups of insecticide-resistant onion thrips. Results will be communicated to stakeholders via an experienced network of extension educators.

Impacts
What was accomplished under these goals? 1.Cover crops legacy effects on plant resistance to herbivores: We have found that the species of cover crop farmers choose has legacy effects on the subsequent corn crop's resistance to the European corn borer, and that this legacy is mediated by soil fertility and/or mycorrhizal colonization. We are studying how cover crop-induced changes in corn mycorrhizal colonization and soil nutrients affect constitutive and induced corn defenses against a variety of herbivores; whether the effect of mycorrhizae on corn defense are simply caused by increased nutrient uptake. A recent and exciting discovery is that plants perceive and respond to chemical cues, often detecting herbivore-associated cues as a warning to prepare for future attack. Finding novel ways to harness these natural cues for enhancing crop protection represents a new frontier in agroecology. Biological control by beneficial entomopathogenic nematodes (EPNs) is one strategy that offers a promising alternative for controlling soil-dwelling insect pests. We have found that EPN-infested insect cadavers emit volatile compounds, and these indirect chemical cues have performance reducing effects on herbivore pests. In this project, we are investigating the influence of EPN chemical cues on plants and insect herbivores, as both cases would have important consequences for protecting plants against herbivore pests. For example, if plants detect EPN odors as a warning cue that EPN-herbivore hosts are present and likely to attack, they can enhance their anti-herbivore defenses to reduce future damage. If insect herbivores perceive and avoid odors from their EPN natural enemies, they will likely avoid nearby plant roots where EPN are present, resulting in a further reduction of herbivore damage. We continue to develop basic knowledge and principles that can be used to build pest management programs that rely less heavily on synthetic insecticides. In a collaborative study with Purdue University (funded by the NIFA AFRI Agroecosystem program), we are learning that plant phylogenetic (and presumably chemical) relationships among plant species can influence the pest complex that develop on them. In particular, when we surround a focal row of cucurbits with crop species of different evolutionary divergent times from cucurbits, the abundance of spotted and striped cucumber beetles on the focal curcurbits decreased as the evolutionary relatedness of neighboring plants decreased; that is, when squash was surrounded by grasses, squash had fewer cucumber beetles than when surrounded by crop species more closely related to cucurbits. Notably, natural enemies did not respond similarly to our evolutionary-divergence related plantings. We repeated this experiment in summer of 2018, but the data are still being collected. In a separate project we are characterizing the bacterial and fungal communities of several lepidopteran pests including the corn earworm, fall armyworm, and black cutworm. Some of the associated bacteria and fungi cause these pests to elicit more potent induced defenses in their crop host plants. Moreover, we have found that some of these microbes may have plant growth promoting properties.The bacterium, Enterobacter ludwigii, was isolated from the regurgitant of field-collected tomato fruitworm, Helicoverpa zea. The bacterium can be secreted by the insect onto tomato seeds during fruit feeding and is also commonly found in the soil. We applied E. ludwigii to germinated tomato seeds and measured tomato plant growth and productivity under controlled greenhouse conditions. Since there are often trade-offs between plant growth and plant defenses, we examined whether the E. ludwigii-mediated faster growth corresponds with weaker anti-herbivore defenses. When E. ludwigii was applied to germinated tomato seeds, the plants exhibited faster root, shoot and hypocotyl growth, and produced more fruits and seeds than untreated control plants. The plants treated with bacteria exhibited the same activity levels of two key enzymes involved in anti-herbivore defenses, polyphenol oxidase and peroxidase, and induced the same levels of mortality and growth inhibition in H. zea larvae as untreated plants. Thus, our results demonstrate that the application of E. ludwigii to seeds can promote tomato plant growth and yield without compromising anti-herbivore defenses. 2.Monarchs, migrations and milkweed: We have initiated a pollinator health conservation project linking variation in milkweed defense biochemistry to variation in larval and resulting adult monarch butterfly fitness traits (NSF $897,841 funded May 2018). We are quantifying variation in plant toxicity traits within and across milkweed species using state-of-the-art methods in chemical ecology to determine how plant defense affects larval growth and subsequent adult fecundity, in reproductively active monarch butterfly cohorts. Using a combination of respirometry, flight kinematic analyses, and studies of lipid metabolism, we are examining how milkweed toxicity experienced during larval stages affects adult flight performance and energetics in migratory monarchs and will link these effects to expression of microRNAs controlling traits associated with migratory phenotypes. This project adds a novel perspective to typical chemical ecology practices to studying plant-herbivore interactions by examining physiological consequences of trophic interactions across the entire ontogeny of an herbivorous insect. The project substantially advances the knowledge of the basic biology of the iconic milkweed-monarch butterfly system, a model migratory insect with a complex ecology. In addition, considering the general relevance of how variable environments (including host plant quality) and larval experience affect the biology of flying adult insects, our work is of broad significance to agricultural and vector-borne disease dynamics research. It also provides pertinent information to habitat restoration efforts to offset population declines in beneficial insects. In a separate project, we are continuing to study the capacity of plants to "smell" volatile cues associated with their herbivores. We continue to develop tall goldenrod (Solidago altissima) as a model system because we found that this species can perceive the putative sex pheromone of its specialist herbivore, Eurosta solidaginis, and then alter its defensive status. As we previously reported, when S. altissima responds, it increases its defensive responses rendering it less palatable to herbivore species. Our most recent set of experiments has revealed that the defensive response mounted by S. altissima provides protection against E. solidaginis, the gall-inducing fly that releases the putative pheromone. This detail was unknown but expected because the main evolutionary reason that S. altissima should have a capacity to detect and respond to the pheromone to E. solidaginis would be because a successful attack from E. solidaginis reduces the fitness of S. altissima. Our results support the co-evolutionary relationship between S. altissima and E. solidaginis by providing evidence that the plant species gains a benefit by inducing defenses useful against the fly after being exposed to the putative sex pheromone of the fly. Building on our work in this system, we have established a collaboration with a USDA colleague based in Madison, Wisconsin who has collected some preliminary data suggesting that cranberry can detect the pheromone of its coevolved lepidopteran species that are major pests of this native crop species. The preliminary data are very similar to our results with S. altissima and E. solidaginis. We used the preliminary data as part of a research proposal to the Foundational Program of USDA NIFA.

Publications

  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Abbot, P., J. F. Tooker, and S. Lawson. 2018. Chemical ecology and sociality in aphids: opportunities and directions. Journal of Chemical Ecology, 44: 770-784.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Vaudo, A. D., L. M. Farrell, H. M. Patch, C. M. Grozinger, and J. F. Tooker. 2018. Consistent pollen nutritional intake drives bumble bee (Bombus impatiens) colony growth and reproduction across different habitats. Ecology and Evolution 00:112 doi.org/10.1002/ece3.4115
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Harth, J. E., A. M. Helms, M. E. Ferrari, J. F. Tooker, A. G. Stephenson. 2018. Viral infection limits establishment and severity of a powdery mildew in wild populations of Cucurbita pepo. Frontiers in Plant Science 9: 792. doi: 10.3389/fpls.2018.00792.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Acevedo, F. E., Peiffer, M. , Ray, S. , Meagher, R. , Luthe, D. S. and Felton, G. W. (2018), Intraspecific differences in plant defense induction by fall armyworm strains. New Phytol, 218: 310-321. doi:10.1111/nph.14981
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Loren J. Rivera-Vega, Bruce A. Stanley, Anne Stanley, Gary W. Felton, Proteomic analysis of labial saliva of the generalist cabbage looper (Trichoplusia ni) and its role in interactions with host plants,Journal of Insect Physiology, Volume 107,2018,Pages 97-103,
  • 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: Castano-Duque, L., Helms, A., Ali, J. G., & Luthe, D. S. (2018). Plant Bio-Wars: Maize Protein Networks Reveal Tissue-Specific Defense Strategies in Response to a Root Herbivore. Journal of chemical ecology, 1-19
  • Type: Journal Articles Status: Accepted Year Published: 2018 Citation: Davidson-Lowe, E., Szendrei, Z., & Ali, J. G. (2018). Asymmetric effects of a leaf?chewing herbivore on aphid population growth. Ecological Entomology.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Malik, R. J., Ali, J. G., & Bever, J. D. (2018). Mycorrhizal composition influences plant anatomical defense and impacts herbivore growth and survival in a life-stage dependent manner. Pedobiologia, 66, 29-35.


Progress 10/01/16 to 09/30/17

Outputs
Target Audience:Entomologists, plant scientist, extension professional, farmers, other agricultural professionals. Research has been presented to scientists and media professionals at multiple scientific meetings including the International Society of Chemical Ecology, AAAS, Entomological Society of America, among others. Research on elicitors was presented at a Penn State Extension meeting for those in the green industry including commercial growers and educators. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?Five graduate students are conducting experiments and gaining knowledge about the natural chemical defenses that plants employ to fend off insect herbivores. In addition, 5 undergraduate students have assisted with experiments in the lab and thus gained research experience. Further, through Penn States SROP a student from Virginia State University gained research experience. How have the results been disseminated to communities of interest?Findings have been published in refereed journals, been presented at national/international meetings, and presented to extension educators and growers. What do you plan to do during the next reporting period to accomplish the goals?Work will continue in identifying elicitors of plant defensive responses. Experiments will focus on understanding the influence of plant phylogenetic (and plant chemistry) relationships on pest and natural enemy populations in vegetable production and on understanding the role of pheromone perception by plants and the ecological influence of this sort of eavesdropping by plants.

Impacts
What was accomplished under these goals? 1: Our efforts on this project are working toward developing fundamental knowledge and principles that can be applied in environmentally safe pest management programs. This regional project facilitated interactions with a colleague at Purdue that resulted in a USDA grant proposal to the NIFA AFRI Agroecosystem program, which funded our work to understand the influence of plant phylogenetic (and chemical) relationships on pest outbreaks in vegetable production. During the 2017, growing season we had a large field experiment in the ground to test how phylogentic relationships influence associational resistance against herbivores. The data from this experiment are still being gathered and analyzed. In addition, our group at Penn State continues to study the ability of plants are to detect cues associated with their herbivores. We are working with tall goldenrod (Solidago altissima), which we have found can perceive and respond to the putative sex pheromone of its specialist herbivore, Eurosta solidaginis. When S. altissima responds, it increases its defensive responses rendering it less palatable to herbivore species. Recently, we have determined the distance over which this pheromone exposure operates (< 1 meter) and the duration of the effect (~1 week), as well as component of the fly emission that detected by the plants. 2: Plants defend against insect herbivores by emitting volatile organic compounds (odors) that attract natural enemies of the herbivores. An increase in carbon dioxide, as a result of climate change, diminishes release of these defensive odors by plants, thus decreasing their natural ability to recruit natural enemies of attacking insects. It was discovered that herbivore-associated bacteria have an important role in mediating induced plant reisstance. We have found that certain gut bacteria can be re-introduced to caterpillars, which cause an increase in their salivary elicitors thus driving increases in induced plant defenses. This was a proof of concept for developing a new tactic for management of important caterpilalr pests.

Publications

  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Block, A., Vaughan, M. M., Christensen, S. A., Alborn, H. T., and Tumlinson, J. H. (2017) Elevated Carbon Dioxide Reduces Emission of Herbivore Induced Volatiles in Zea mays. Plant, Cell & Environment, doi: 10.1111/pce.12976.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Rigsby, CM, McCartney, NB, Herms, DA, Tumlinson, JH, and Cipollini, D (2017) Variation in the Volatile Profiles of Black and Manchurian Ash in Relation to Emerald Ash Borer Oviposition Preferences. J Chem Ecol. 43:831842.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Helms, A. M., C. M. De Moraes, A. Tr�ger, H. T. Alborn, W. Francke, J. F. Tooker, M. C. Mescher. Identification of an insect-produced olfactory cue that primes plant defenses. Nature Communications 8:337. doi:10.1038/s41467-017-00335-8
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Yip, E., C. M. De Moraes, M. C. Mescher, J. F. Tooker. 2017. The volatile emission of a specialist herbivore alters patterns of plant defence, growth and flower production in a field population of goldenrod (Solidago altissima). Functional Ecology 31:10621070.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: LJ Rivera-Vega, DA Galbraith, CM Grozinger, GW Felton. 2017. Host plant driven transcriptome plasticity in the salivary glands of the cabbage looper (Trichoplusia ni. PLoS One https://doi.org/10.1371/journal.pone.0182636.


Progress 10/01/15 to 09/30/16

Outputs
Target Audience:Main target audience was the scientific community where information has been shared via seminars, public talks, and journal publications. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?One Ph.D. graduate student (Flor Acevedo) has been conducting research directly related to this project. How have the results been disseminated to communities of interest?Yes, several invited presentations have been given at the International Congress of Entomology/Entomological Society of America meeting in 2016. What do you plan to do during the next reporting period to accomplish the goals?The Tumlinson lab is focusing on the volatile compounds and their role in plant priming. The Felton lab will be focusing on microbial regulation of plant induced responses to herbivores. The Tooker Lab is studying the flow of synthetic plant secondary metabolites (i.e., systemic neonicotinoid insecticides) through an invertebrate food web, and are studying the non-target effects of these ubiquitous agricultural compounds. We also are exploring the nutritional value of plant floral resources to understand their influence on pollinator health and performance. In the Ali lab work will privide progress toward understanding various plant effectors and cues that either increase plant resistance or susceptibility. These factors include cues from caterpillars that increased aphid growth rate and changed plant volatiles in corn, belowground cues from beneficial nematodes that increased resistance to insect pest on potato aboveground, and we have characterized cues from domesticated and wild carrot that influence the behavior of plant parasitic nematodes.

Impacts
What was accomplished under these goals? 1. In the last year, efforts by the Tooker lab have emphasized developing fundamental knowledge and principles that can be applied in environmentally safe pest management programs. This regional project facilitated interactions with a colleague at Purdue that resulted in a USDA grant proposal to the NIFA AFRI Agroecosystem program, which funded our work to understand the influence of plant phylogenetic (and chemical) relationships on pest outbreaks in vegetable production. More effective and sustainable approaches to managing and controlling herbivorous insect pests will be developed based on knowledge of the fundamental mechanisms of insect herbivores interactions with their host plants, including the mechanisms by which plants defend against insects. Stomata are tiny pores in the epidermis of the leaf and stem that control gas exchange between the plant and environment. The critical role of stomata in the uptake of CO2 and release of water via transpiration is well documented in the literature. Predicted climate changes include a rise in average temperature, rising atmospheric CO2 levels, extreme weather conditions, i.e. drought and flooding. Stomata play a crucial role in the plants' responses to these climatic challenges and all of these conditions influence the number of stomata initiated and the status of the aperture. We hypothesize that maize stomata play a critical role in the regulation of voc production and emission; in particular, reduced stomatal conductance will reduce the emission of voc and significantly impact crop plant defenses against pathogens and insect herbivores. The biosynthesis of herbivore-induced sesquiterpenes (volatile organic compounds that attract natural enemies of the herbivores) is regulated by farnesyl diphosphate synthases in maize. These chemical signals are produced by cells inside the leaf and emitted via the stomata. The opening and closing of stomata regulates release of these semiochemicals. 2. Insect symbionts modulating plant defenses have been observed in beetles and piercing-sucking insects, but the role of caterpillar-associated bacteria in regulating plant-induced defenses has not been adequately examined. We identified bacteria from the regurgitant of field-collected Helicoverpa zea (H. zea) larvae using 16S rRNA gene sequencing and MALDI-TOF mass spectrometry. A combination of biochemical, molecular, and confocal-electron microscopy methods were used to determine the role of caterpillar-associated bacteria in mediating defenses in Solanum lycopersicum (tomato). Lab-reared H. zea inoculated with one of the bacteria identified in field-collected H. zea, Enterobacter ludwigii (E. ludwigii) induced expression of the tomato defense-related enzyme polyphenol oxidase and genes regulated by jasmonic acid, whereas the salicylic acid responsive pathogenesis-related gene was suppressed. Additionally, saliva and its main component glucose oxidase from inoculated caterpillars played an important role in elevating tomato anti-herbivore defenses. However, there was little detectable amount of regurgitant and bacteria on H. zea- damaged tomato leaves. Our results suggest that H. zea-associated bacteria indirectly mediated the interaction of plant-insect by triggering salivary elicitors. These findings provide a proof-of-concept that introducing gut bacteria to a herbivore may provide a novel approach to pest management through indirect induction of plant resistance. The Tooker group at Penn State continues to explore their line of inquiry that revealed that plants are capable of detecting volatile cues associated with their herbivores. We continue to study this system of tall goldenrod (Solidago altissima) which can perceive and responds alter its physiology in response to the putative sex pheromone of its specialist herbivore, Eurosta solidaginis. We also found that decreases in herbivory associated with exposure to the pheromone are indeed associated with changes in plant physiology, which alters the community of insects associated with exposed plants. Recent work is determining the distance over which this pheromone exposure operates and the duration of the effect.

Publications

  • Type: Journal Articles Status: Under Review Year Published: 2016 Citation: Jie Wang, Michelle Peiffer, Cristina Rosa, Kelli Hoover, Rensen Zeng1, Gary W. Felton. 2016. Helicoverpa zea gut-associated bacteria indirectly induce defenses in tomato through mediating salivary elicitor(s. New Phytologist.
  • Type: Journal Articles Status: Under Review Year Published: 2016 Citation: Flor E. Acevedo, Michelle Peiffer, Ching-Wen Tan, Anne Stanley, Bruce Stanley, Kelli Hoover, Cristina Rosa, Dawn Luthe, and Gary Felton. 2016. Fall armyworm-associated gut bacteria modulate plant defense responses. Molecular Plant Microbe Interactions.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: 6. Seidl-Adams, I., Richter, A., Boomer, KB, Yoshinaga, N., Degenhardt, J., and Tumlinson, J. H. 2015. Emission of herbivore elicitor-induced sesquiterpenes is regulated by stomatal aperture in maize (Zea mays) seedlings). Plant Cell and Environ. 38:23-34.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Richter, A., Seidl-Adams, I., Ko�llner, T.G., Schaff, C., Tumlinson, J.H., Degenhardt, J. 2015. A small, differentially regulated family of farnesyl diphosphate synthases in maize (Zea mays) provides farnesyl diphosphate for the biosynthesis of herbivore-induced sesquiterpenes. Planta 241:13511361.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Vaudo, A. D., J. F. Tooker, C. M. Grozinger, and H. M. Patch. 2015. Bee nutrition and floral resource restoration. Current Opinion in Insect Science 10:133141.
  • Type: Journal Articles Status: Published Year Published: 2015 Citation: Ray, S., I. Gaffor, F. Acevedo, A. M. Helms, W.-P. Chuang, J.F. Tooker, G. W. Felton, D. S. Luthe. 2015. Maize plants recognize herbivore-associated cues from caterpillar frass. Journal of Chemical Ecology 41:781792
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Bohnenblust, E. W., A. D. Vaudo, J. F. Egan, D. A. Mortensen, and J. F. Tooker. 2016. Effects of the herbicide dicamba on non-target plants and pollinator visitation. Environmental Toxicology and Chemistry 35:144151.
  • Type: Journal Articles Status: Published Year Published: 2016 Citation: Grettenberger, I. M. and J. F. Tooker. 2016. Inter-varietal interactions among plants in genotypically diverse mixtures tend to decrease herbivore performance Oecologia 182:189-202.
  • Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Vaudo, A. D., H. M. Patch, D. A. Mortensen, J. F. Tooker, C. M. Grozinger. Macronutrient ratios in pollen shape bumble bee (Bombus impatiens) foraging strategies and floral preferences. Proceedings of National Academy of Science USA 113:E4035-42.
  • Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Ali, J.G. and A.A. Agrawal. (In press) Trade-offs and tritrophic consequences of host shifts in highly specialized root herbivores. Functional Ecology.
  • Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Hufnagel, M., Schilmiller, A., Ali, J., Szendrei, Z. (In press) Choosy mothers pick challenging plants: Maternal preference and larval performance of a specialist herbivore are not linked. Ecological Entomology.
  • Type: Journal Articles Status: Accepted Year Published: 2016 Citation: Morrison III, W. R., Ingrao, A., Ali, J., & Szendrei, Z. (2016). Identification of plant semiochemicals and evaluation of their interactions with early spring insect pests of asparagus. Journal of Plant Interactions, 11(1), 11-19.
  • Type: Book Chapters Status: Published Year Published: 2015 Citation: Ali, J. G., & Davidson-Lowe, E. (2015). Plant Cues and Factors In?uencing the Behaviour of Bene?cial Nematodes as a Belowground Indirect Defense. In H. Bais & J. Sherrier (Eds.), Plant Microbe Interactions (pp. 191214).