Source: CORNELL 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.
1010803
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
NE-1501
Project Start Date
Oct 1, 2016
Project End Date
Sep 30, 2020
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
CORNELL UNIVERSITY
(N/A)
ITHACA,NY 14853
Performing Department
Ecology & Evolutionary Biology
Non Technical Summary
Current conventional, industrialized agriculture is widely considered ecologically and economicallyunsustainable, mainly because it is not suffienctly protecting natural resources (e.g. water, soil etc.) and uses synthetic pesticides who are commonly and increasingly found to negatively affect human and environmetnal health and threatens natural habitats and biodiversity. On the other hand we are dependent on a highly productive agiculture in order to keep pace with an ever-increasing human population. The the public awareness of these problems have made organic agriculture the single fastest-growing sectore of agriculture in the USA and worldwide, and increased the demand for alternative and sustainable ways of pest control.This Multistate Research aims to develop alternative non-pesticidal strategies of pest control, based on chemical ecological principles. With an increased consumer demand for organically grown food and a need for sustainable agriculture to ensure food security, such alternative approaches are timely and welcomed by stakeholders, especially in NY (Northeast IPM Center). We aim to identify pest control strategies that cut across multiple crops and pests. One of the most promising chemical ecology approaches is the manipulation of the chemical information transfer between the pest and the crop plant. Insect pests, in particular, use a complex bouquet of chemical cues when searching for hosts. They will use a search pattern that can be described as an information space that is provided in the context of an information landscape. There are three general ways of manipulating the information transfer between a pest insect and its host plant: a) Change the information available by altering the information space (e.g. plant variety). b) Change the context/information landscape in which the information is provided (e.g. intercropping), c) remove directionality by flooding the environment with chemical information. The general principles have previously been studied by the PI in a native plant system and have been applied in farming technologies, such as "push-pull" (http://www.push-pull.net/)used to control pests on corn in East Africa. That techonlogy had been developed to control insect pests of maize in smallholder farms in East Africa. Our project now aims to develop a standard approach that allows a quick identification of the most efficient informationtransfer-manipulating mechanism for a particular agricultural crop-pest system.Fora study model we will evaluate the information transfer-modifying ways to control two major pests on squash,Cucurbita pepo, the squash bug, and the striped cucumber beetle. Thus the results will allow to identify ways of manipulating of information transfer between organisms efficiently and identify the most efficient manipulation of that information transfer to minimize pest effects on crops and so maximizes quality and quantity of yield. In order to reach our goals we will use chemical analytical methods (HPLC, GC-MS) for the identification of the chemical information traits meditating interactions between crop plant and pests and multifactorial laboratory and field bioassays to establish optimal ways this chemical information to maximize pest control and yield.This research will begin to develop a conceptual tool readily applicable todifferent crop-pest systems in different regions that allows for organic and sustainable control of pest insects. Thereby it will minimize yield losses due to pests while minimizing synthetic pesticide application and may have additional emerging benefits, such as soil health as has been found with the push-pull technology in East Africa.
Animal Health Component
20%
Research Effort Categories
Basic
70%
Applied
20%
Developmental
10%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2151421107050%
2111429107025%
2061429106025%
Knowledge Area
206 - Basic Plant Biology; 211 - Insects, Mites, and Other Arthropods Affecting Plants; 215 - Biological Control of Pests Affecting Plants;

Subject Of Investigation
1429 - Cucurbits, other; 1421 - Cucumber;

Field Of Science
1060 - Biology (whole systems); 1070 - Ecology;
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. 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
Using GC-MS and HPLC, we will analyze plant chemistry of a total of ten squash varieties grown in the region. Chemistry will be linked to host preferences and performance of two major cucumber pests in field experiments. Similar experiments will be established in different regions (NY, NJ) to test for context-dependency of plant chemistry and pest preferences. GC-EAG will be used to identify which components of the chemical information space can actually be perceived by the pests and if the composition of this realized information space affects pest preference. This objective will test if the alteration of the information space affects herbivore host choice and if host choice is correlated with pest herbivore performance on squash varieties.We will compare direct manipulation of the chemical information space with the manipulation of the information landscape (chemical environment) within which the plant cues are perceived by the pests. Initially we will use the most attractive squash varieties (Obj. 1) and plants commonly intercropped with squashes. The pest control effects with these different intercropping systems relative to monocultures will be tested in common garden repeated plot field experiments. Intercrop plants will be chemically profiled and their pest repellence effect will be linked to their chemistry.In both of the above described objectives pollinator visitation and pollination success as well as the occurrence of biocontrol agents (parasitoids and predators) and their effects will be monitored as a functions of crop and companion crop chemistry.

Progress 10/01/16 to 09/30/20

Outputs
Target Audience:For the duration of the project, three undergraduate students, threegraduate students, and one postdoc were involved in this project, conducting plant and insect bioassays and analyzing plant secondary metabolism. Through their involvement, the researchers learned to conduct plant and insect bioassays and to use Gas Chromatograph-Mass Spectrometry (GC-MS) as well as High-Performance Liquid Chromatography (HPLC) for plant secondary chemistry analysis. The skills the researchers learned will help them to be better prepared for their careers. Moreover, results partially or entirely collected with funds from this project have been published in 18 peer-reviewed papers of which 10 derived directly from this project and another 8 benefitted from the infrastructure (analytical machines, field sites, greenhouse space)that this project maintained. Moreover, two book chapters were significantly impacted by the research in this project. In addition, twoadditional publications are currently in preparation. Thus, results from this project have delivered science-based knowledge to people through formal, peer-reviewed publications. Moreover, results include that the lack of Si in soil deprives plants of their ability to appropriately respond to insect herbivores and that there is a serious of environmental factors like Si that similarly affect plant metabolism and so interactions. These factors are now considered (e.g. soil microbial community, plant-plant communication) arecurrently considered or are already applied (Si) for sustainable agricultural applications and a potential alteration of fertilization practices in Cornell greenhouses, respectively. Changes/Problems:We early on broadened the scope of this project from a focus on Si to heavy metals and soil microbial communities affecting plant secondary metabolism. This was done becausethe goal of the original proposal was reached faster than expected and because the original research exposed those two other factors as at least equally important for understanding the environmental conditions that affect plant secondary metabolism and so resistance to pathogens and herbivores. As a consequence, this project resulted in far more publications than expected (18 so far), more efficiently facilitated the analytical infrastructure, and created two new projects that focus on the direct application of the findings from this project and chemical ecological principles in agriculture. What opportunities for training and professional development has the project provided?Three undergraduate students, threegraduate students, and two postdocs have been part of this project (only one of them paid directly from this grant). Through this project, all involved researchersgot intensive new research experience, specifically in planning and conduction plant and insect bioassays and analyzing plant secondary chemistry. Moreover, they were tasked with lab management tasks as well as with data analysis and were advised to independently follow through the entire scientific process. The structure of the project exposed all of the involved students to sustainable agricultural applications and taught them to derive new agricultural practices (e.g. biological pest control through chemical ecology principles) from the basic chemical ecology interaction patterns they revealed. Thus, the project accomplished exactly what the large framework of this Multistate initiative aimed for. How have the results been disseminated to communities of interest?Eighteen papers have already been published in relatively high-impact peer-reviewed journals and are so accessible to the broader community of researchers and stakeholders. Some of those publications (e.g. Kalske et al 2019 Current Biology) have been reported on broadly in the public press, which increased the interactions with stakeholders. In addition, the new projects in NYS and Colombia on functional intercropping, which were directly derived from this project, had us interact directly with farmers and extension personal to define the scope and focus of the new research and identify the key factors thatdetermine the adoption of new chemical ecology technologies by growers. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? (1) The most important results from this project derivefrom experiments with crops (applied aspects) and wild plant species (basic principles) that addressed the context-dependency of plant-induced responses as chemical ecological traits that can be utilized in insect pest control. For example, we found that greenhouse soils commonly (including those commonly used at Cornell) are deprived of silicon (Si). Lacking Si, some plant species, such a cucumber, lose their ability to induce changes to their secondary metabolism, which can significantly deprive them of their ability to induce defenses. So far we found that they lose induce resistance and they cannot induce volatile organic compound emission (involved in the signaling to natural enemies and so mediating indirect resistance and biological pest control). Based on the findings we created a protocol for Si supplementation that is already being usedin greenhouses. Moreover, this finding has done both, it generated the interest in studying the mechanism underlying the apparent linkage between environmentally acquired Si and plant induce responses to herbivory and it has created a broader conceptual scope of this project. From the very beginning of the project, this tempted us to look for more examples in which environmental conditions affect plant endogenous resistance expression. One of those environmental factors is metal contaminations (see publication on As contamination) and another is differences in the soil microbial community. Both of those factors have become major foci ofthis project and resulted in the bulk of the publication resulting from this project. For metal contaminations, like arsenic contaminations, which werefrequently caused by past agricultural activity and persist to this day, we demonstrated that the metals can be taken up into the plant and there replace the plants' own metabolic (chemical) defenses. Inwild plant species, such as goldenrods, the relief of the plants from natural selection by herbivores due to the environmentally acquired resistance trait arsenic, leads to a reduced mean expression of plant endogenous chemical defenses in contaminated plant populations. Similarly, this relief from herbivory caused byAs-contamination selects plants for higher competitive ability and thus potentially higher invasiveness in non-native habitats (publications in preparation). In addition to silicon and heavy metals, we identified rhizosphere microbial communities as major factors influencing plant constitutive and inducible secondary metabolism. Specifically, soil microbial communities of different successional origin (early vs. late succession) had dramatic differential effects on plant secondary metabolism and so on plant defenses against herbivores. Thereby, microbial communities from late-successional soils with relatively higher soil organic matter contents caused higher anti-herbivore resistance in plants than microbial communities of early succession soils (following corn cultivation). The results of this part of the project have already been incorporated into a new project that aims to control pathogens and herbivores of corn through functional intercropping with plants that alter the soil microbial community to the advantage of the crop plant. This provides a sustainable tool for soil protection and organic pest control. (2) All of the factors identified with this project - soil micronutrient Si, heavy metal contamination, and soil microbial community - significantly affect a plant's metabolic properties and so influence all other interactions plants have with their environment. Specifically, we studied the effects of the metabolic changes on herbivores interacting with the plants and derived ways of applying chemical ecology principles in sustainable and biological pest control. The most promising applications derived from this project are Si fertilization and the associated increased induced resistance to herbivores and the manipulation of soil microbial communities through functional intercropping with companion plant species, which in turn affects plant constitutive and induced resistance to pathogens and herbivores. (3) The funds supported the maintenance of chemical analytical infrastructure in the Kessler lab (GC-MS and HPLC) and so facilitated chemical ecology research in the wider Cornell community. Indication for the benefits to the community are the eight collaborative publications that were facilitated by this infrastructure. Moreover, funds from this grant paid grounds and greenhouse services, thus helping to maintain Cornell growth facilities. (4) This project resulted in two new grant proposals that are based on farmer and extension collaborations in NYS and Colombia. In both projects, we try to optimize companion cropping systems to increase soil protection and plant chemical defenses against pathogens and herbivores.

Publications

  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Lim M, McBride MB, Kessler A. 2017. Arsenic Bioaccumulation by Eruca sativa Is Unaffected by Intercropping or Plant Density. Water, Air, Soil Pollution 228:364. doi: 10.1007/s11270-017-3544-9
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Howard, M.M., Kao-Kniffin, J. and Kessler, A., 2020. Shifts in plantmicrobe interactions over community succession and their effects on plant resistance to herbivores. New Phytologist, 226(4), pp.1144-1157.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Zwetsloot, M.J., Kessler, A. and Bauerle, T.L., 2018. Phenolic root exudate and tissue compounds vary widely among temperate forest tree species and have contrasting effects on soil microbial respiration. New Phytologist, 218(2), pp.530-541.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Kessler, A. and Chaut�, A., 2020. The ecological consequences of herbivore-induced plant responses on plantpollinator interactions. Emerging Topics in Life Sciences, 4(1), pp.33-43.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Mutyambai, D.M., Bass, E., Luttermoser, T., Poveda, K., Midega, C.A., Khan, Z.R. and Kessler, A., 2019. More Than Push and Pull? Plant-Soil Feedbacks of Maize Companion Cropping Increase Chemical Plant Defenses Against Herbivores. Frontiers in Ecology and Evolution, 7, p.217.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Morrell, K. and Kessler, A., 2017. Plant communication in a widespread goldenrod: keeping herbivores on the move. Functional Ecology, 31(5), pp.1049-1061.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Uesugi, A., Johnson, R. and Kessler, A., 2019. Context?dependent induction of allelopathy in plants under competition. Oikos, 128(10), pp.1492-1502.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Smeda, J.R., Schilmiller, A.L., Anderson, T., Ben-Mahmoud, S., Ullman, D.E., Chappell, T.M., Kessler, A. and Mutschler, M.A., 2018. Combination of acylglucose QTL reveals additive and epistatic genetic interactions and impacts insect oviposition and virus infection. Molecular breeding, 38(1), pp.1-20.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Howard, M.M., Kalske, A. and Kessler, A., 2018. Eco-evolutionary processes affecting plantherbivore interactions during early community succession. Oecologia, 187(2), pp.547-559.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Kessler, A. and Kalske, A., 2018. Plant secondary metabolite diversity and species interactions. Annual Review of Ecology, Evolution, and Systematics, 49, pp.115-138.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Smeda, J.R., Schilmiller, A.L., Kessler, A. and Mutschler, M.A., 2017. Combination of QTL affecting acylsugar chemistry reveals additive and epistatic genetic interactions to increase acylsugar profile diversity. Molecular Breeding, 37(8), pp.1-18.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Kersch-Becker, M.F., Kessler, A. and Thaler, J.S., 2017. Plant defences limit herbivore population growth by changing predatorprey interactions. Proceedings of the Royal Society B: Biological Sciences, 284(1862), p.20171120.
  • Type: Book Chapters Status: Published Year Published: 2017 Citation: Kessler, A., Plant Defences against Herbivore Attack. eLS, pp.1-11.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Howard, M.M., Mu�oz, C.A., Kao-Kniffin, J. and Kessler, A., 2020. Soil Microbiomes From Fallow Fields Have Species-Specific Effects on Crop Growth and Pest Resistance. Frontiers in Plant Science, 11.
  • Type: Journal Articles Status: Published Year Published: 2020 Citation: Kalske, A. and Kessler, A., 2020. Population?wide shifts in herbivore resistance strategies over succession. Ecology, 101(11), p.e03157.
  • Type: Journal Articles Status: Published Year Published: 2019 Citation: Kalske, A., Shiojiri, K., Uesugi, A., Sakata, Y., Morrell, K. and Kessler, A., 2019. Insect herbivory selects for volatile-mediated plant-plant communication. Current Biology, 29(18), pp.3128-3133.
  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Glaum, P. and Kessler, A., 2017. Functional reduction in pollination through herbivore-induced pollinator limitation and its potential in mutualist communities. Nature communications, 8(1), pp.1-10.
  • Type: Book Chapters Status: Published Year Published: 2017 Citation: Raguso, R.A. and Kessler, A., 2017. Speaking in chemical tongues: decoding the language of plant volatiles. The language of plants: Science, philosophy, literature, pp.27-61.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Wilson, J.K., Woods, H.A. and Kessler, A., 2018. High levels of abiotic noise in volatile organic compounds released by a desert perennial: implications for the evolution and ecology of airborne chemical communication. Oecologia, 188(2), pp.367-379.
  • Type: Journal Articles Status: Published Year Published: 2018 Citation: Kessler, A., 2018. Introduction to a special feature issueNew insights into plant volatiles.New Phytologist


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

Outputs
Target Audience:This past year of the project, one undergraduate student, one graduate student and one postdocwere involved in this project, conducting plant and insect bioassays and analyzing plant secondary metabolism. Through their involvement the researchers learned to conduct plant and insect bioassays and to use Gas Chromatograph-Mass Spectrometry (GC-MS) as well as High Performance Liquid Chromatography (HPLC) for plant secondary chemistry analysis. The skills the researcherslearned will help them to be better prepared for their careers. Moreover, first results from last year's experiments have been published or are currently in revisionin a peer-reviewed journal. Thus, results from this project have delivered science-based knowledge to people through formal, peer-reviewed publications. Moreover, one of the major results, so far is that the lack of Si in soil deprives plants of their ability to appropriately respond to insect herbivores. This finding is currently considered for a potential alteration of fertilization practices in Cornell greenhouses. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?One undergraduate student, one graduate student and one postdochave been part of this project (only one of them paid directly from this grant). Through this project all threeresearchers got intensive new research experience, specifically in planning and conduction plant and insect bioassays and analyzing plant secondary chemistry. Moreover, they were tasked with lab management tasks as well as with data analysis. How have the results been disseminated to communities of interest?One paper has been published and one more is in revision for publication in peer-reviewed journals. We expect more to follow so that the major venue of dissemination of the results of this project will be through sharing the results with the scientific community in the classical way. In addition research in this project resulted in the creation of a protocol for Si fertilization that is currently discussed for use in Cornell greenhouses. What do you plan to do during the next reporting period to accomplish the goals?For the nest period, we will continue a deeper study of the mechanisms underlying the Si- induced response linkage as well as the ecological and biocontrol consequences of it. Moreover, we expand the study to other systems to study the concept of environmentally acquired plant resistance and associated hypothesis.

Impacts
What was accomplished under these goals? In this first year of the project aspects of all four goals have been approached. The most important result thus far derives form experiments that addressed the context dependency of plant induced responses as chemical ecological traits that can be utilized in insect pest control. We found that greenhouse soils commonly used at Cornell are deprived of Si. We found that some plant species, such a cucumber, loose their ability to induce changes to their secondary metabolism, which can significantly deprive them of their ability to induce defenses. So far we found that they lose induce resistance and they cannot induce volatile organic compound emission (involved in the signaling to natural enemies and so mediating indirect resistance and biological pest control). Based on the findings we created a protocol for Si supplementation that is currently considered for use in greenhouses. Moreover, this finding has done both, it generated the interest in studying the mechanism underlying the apparent linkage between environmentally acquired Si and plant induce responses to herbivory and it has created a broader conceptual scope of this project. We started to look for more examples in which environmental condition affect plant endogenous resistance expression. One of those environmental factors are metal contaminations (see publication) and another are differneces in the soil microbial community. Both of those factors have become additional focy of this project.

Publications

  • Type: Journal Articles Status: Published Year Published: 2017 Citation: Lim M, McBride MB, Kessler A. 2017. Arsenic Bioaccumulation by Eruca sativa Is Unaffected by Intercropping or Plant Density. Water, Air, Soil Pollution 228:364. doi: 10.1007/s11270-017-3544-9