Source: MICHIGAN STATE UNIV submitted to NRP
EVALUATION OF DEFENSE DIVERSITY IN TOMATO AND ITS DEPLOYMENT FOR MANAGING INSECT PESTS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
1015506
Grant No.
2018-67013-28065
Cumulative Award Amt.
$499,855.00
Proposal No.
2017-08228
Multistate No.
(N/A)
Project Start Date
Apr 1, 2018
Project End Date
Mar 31, 2023
Grant Year
2018
Program Code
[A1112]- Pests and Beneficial Species in Agricultural Production Systems
Recipient Organization
MICHIGAN STATE UNIV
(N/A)
EAST LANSING,MI 48824
Performing Department
ENTOMOLOGY
Non Technical Summary
Herbivore-resistant crop varieties should be the cornerstone of sustainable pest management programs. Some crop species are known to have a diversity of phenotypes that each confer a unique defensive trait against herbivores. Recent studies suggest that deployment of a diversity of defensive phenotypes may be a more effective pest management strategy than deploying a single phenotype that confers a single defensive trait. Moreover, the efficacy of deploying crops with intraspecific defense trait diversity for pest control may be further enhanced by increased mortality from natural enemies. The goal of this project is to uncover the consequences of intra-crop defense diversity in tomato (Solanum lycopersicum) in order to improve management of two economically important agricultural pests: cabbage looper (Trichoplusia ni) and green peach aphid (Myzus persicae). This goal will be addressed by measuring the effects that multiple genetic lines of tomato, each conferring unique resistance via glycoalkaloids, terpenes, or acyl sugars, have on pest performance, movement, population dynamics, and interactions with natural enemies. Experiments will be conducted in the lab to uncover the physiological effects of defense diversity, and in the field to measure pest movement and population dynamics and effects on tomato crop health. Additionally, field studies will identify how defense trait diversity influences interactions between pests and natural enemies by combining treatments with important biocontrol predators. This project will advance the goals of the program area priority by leading to the development of intra-crop defense diversity as an innovative, environmentally-sound, and cost-effective strategy for managing agriculturally important pests.
Animal Health Component
(N/A)
Research Effort Categories
Basic
100%
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
21114601070100%
Knowledge Area
211 - Insects, Mites, and Other Arthropods Affecting Plants;

Subject Of Investigation
1460 - Tomato;

Field Of Science
1070 - Ecology;
Goals / Objectives
Our proposal has five objectives. Objectives 1-4 test the physiology, movement, population dynamics, and enemies hypotheses, scaling from laboratory bioassays to large field experiments. In these objectives, we use M82 and the three introgression lines discussed above (IL1-1, IL1-3, and IL10-3) to ask how the effects of each of the focal resistance trait axes--glycoalkaloids, acyl sugars, and terpenes--differ for each of the hypotheses, and how diversity along multiple axes simultaneously changes the consequences of diversity for physiology, movement, population dynamics, and interactions with natural enemies. Objective 5 continues the development of the M82 × pennellii introgression lines as a model system for studying the consequences of intra-crop diversity for insects. In this objective, we phenotype each IL for its internal leaf chemistry, a key component of the plant resistance phenotype that remains to be characterized.Objective 1: Understand the effects of intra-crop defense diversity on pest physiology and responses to predators. We will test the Physiology Hypothesis by rearing cabbage loopers and green peach aphids in the lab on single lines (of M82, IL1-1, IL1-3, and IL10-3) or on mixtures of these lines representing different types and amounts of trait diversity. We will measure insect physiology and performance in each plant diversity treatment. We will test the second part of the Physiology Hypothesis--that plant defense diversity reduces the physiological ability of herbivores to defend against predators--by challenging the pests with predators used in biological control and measuring rates of successful predation. These lab experiments will reveal the potential effects of defense diversity when individual herbivores consume diverse plant defenses.Objective 2: Understand the effects of intra-crop defense diversity on pest movement. We will test the Movement Hypothesis by planting M82 and the three ILs in monocultures and polycultures in open plots in the field and tracking colonization by the entire insect herbivore community, including cabbage loopers and green peach aphids, both of which are present at the field site (MSU Kellogg Biological Station). The polycultures will represent different types and amounts of trait diversity, allowing us to reveal the relationship between herbivore immigration and intra-crop diversity.Objective 3: Understand the effects of intra-crop defense diversity on pest population dynamics and predator-prey interactions. We will test the Population Dynamics Hypothesis by tracking population dynamics of cabbage loopers and green peach aphids for multiple generations in large field cages with monocultures and polycultures of M82 and the three ILs, as above. Measurements of pest survival, fecundity, and density will allow us to model population dynamics in the presence and absence of plant defense diversity, indicating the total effect of defense diversity on pest control.Objective 4: Understand the effects of intra-crop defense diversity on recruitment of natural enemies. We will test the Enemies Hypothesis by tethering cabbage loopers or bagging aphids in field plots of monocultures and polycultures of M82 and the three ILs and tracking predation events and colonization by natural enemies.Objective 5: Characterize the internal insect-resistance traits of M82 and all 76 ILs. The chemistry of resistance traits in the IL trichomes and epidermal cells has been extensively characterized both in terms of volatile and non-volatile components (Schilmiller et al. 2010). The final objective of this proposal is to continue the development of the M82 × pennellii introgression lines as a model system for studying the consequences of intra-crop diversity for insects. We will do this by phenotyping each IL for its internal leaf chemistry, a key component of the plant resistance phenotype that remains to be characterized. This will include glycoalkaloids, phenolics, protease inhibitors, nutrient content, leaf water content, and leaf toughness. Finally, we will assay each IL individually with cabbage loopers and green peach aphids to link plant phenotypes to pest performance.
Project Methods
Introgression LinesObjectives 1-4 rely on M82, IL1-1, IL1-3, and IL10-3 of the tomato cv. M82 × Solanum pennellii introgression line system, as discussed above. We chose IL1-1 from among the 76 ILs because it displays a differing glycoalkaloid resistance phenotype from M82, and is similar to M82 in other resistance traits. Glycoalkaloids are a key class of secondary metabolites for resistance against insect pests in tomato and other solanaceous plants (Tingey 1984, Friedman 2002). In particular, IL1-1 has several unique glycoalkaloids, including two isomers of dehydrotomatine, didehydrotomatine, and hydroxytomatine (Schilmiller et al. 2010). IL1-1 has lower abundances of tomatine and other glycoalkoids common in M82. We chose IL1-3 because it has a different profile of acyl sugars, many of which lack acetyl groups relative to M82. Acyl sugars are key resistance compounds found in Solanum trichomes and trichome exudates, and which influence a wide range of insect pests from sucking to chewing insects (Leckie et al. 2012, Lucatti et al. 2013). Finally, we chose IL10-3 because it has a different terpene profile from M82, with especially low abundances of several major sesquiterpenes, including δ-elemene, caryophyllene, and α-humulene. Terpenes in general, and sesquiterpenes specifically, are major constituents of trichome chemistry, and in Solanum they play key roles in insect resistance, host-location behavior, and attraction of natural enemies (Bleeker et al. 2012). Together these lines and M82 represent diversity along three major resistance trait axes. Remaining resistance trait axes will be quantified and bioassayed as part of Objective 5.General ApproachThe experiments for Objectives 1-4 follow the same general format: four monocultures and seven polycultures presented to insect pests in the presence or absence of natural enemies in lab or field settings. The monoculture treatments are M82, IL1-1, IL1-3, or IL10-3 in isolation, and the polyculture treatments are all pairwise combinations of M82 and ILs plus all three ILs (Table 1). Examining the insect response variables in the monocultures allows us to see the consequences of all the lines (and their respective phenotypes) in the absence of diversity. Each polyculture treatment represents one or more different axes of trait diversity (Table 1). For example, growing M82 in polyculture with IL1-1 gives intra-crop diversity in glycoalkaloids (Fig. 6). Growing IL1-1 and IL1-3 gives diversity in both glycoalkaloids and acyl sugars. Growing all three ILs together gives diversity along all three trait axes. It is also important to note that the polycultures, in addition to giving a controlled amount of trait diversity, also give a controlled amount of genetic diversity, which we can map directly to the tomato genome. For example, the polyculture with M82 and IL1-1 has intra-crop genetic diversity only in region 1 of chromosome 1. Moreover, the pennellii chromosomal substitutions are similar in size across ILs. This means that all pairwise polycultures have the same amount of genetic diversity; they differ only in the genomic location of the diversity. This allows us to pinpoint where in the genome intraspecific diversity is most influential for the ecology of higher trophic levels, a major advance for the study of the ecological consequences of plant diversity.Table 1. Monoculture and polyculture treatments and their trait diversity levels.Plant treatmentTrait diversityM82None (M82 for all traits)IL1-1None (unique glycoalkaloid profile)IL1-3None (unique acyl sugar profile)IL10-3None (unique terpene profile)M82 + IL1-1Glycoalkaloid diversityM82 + IL1-3Acyl sugar diversityM82 + IL10-3Terpene diversityIL1-1 + IL1-3Glycoalkaloid and acyl sugar diversityIL1-1 + IL10-3Glycoalkaloid and terpene diversityIL1-3 + IL10-3Acyl sugar and terpene diversityIL1-1 + IL1-3 + IL 10-3Diversity along all three trait axesWe will interpret the outcome of all polyculture-monoculture experiments by comparing response variables (e.g., insect performance or population dynamics, plant damage, natural enemy recruitment) in a polyculture to the mean of those response variables across the monocultures represented in the polyculture. If the trait diversity in a given polyculture negatively influences insect performance, then insect performance in that polyculture will be significantly lower than the mean performance across the monocultures represented in that polyculture. We will make these comparisons for each individual diversity axis as well as for polycultures with multiple diversity axes.Our proposed work is focused on how intra-crop trait diversity directly influences insect pests and natural enemies, but intra-crop diversity could also indirectly influence insects by changing plant-plant competition (Moreira et al. 2015). This mechanism does not apply to Objectives 1 and 5 because the plants will be grown in pots and will thus not be competing for resources . Our methods for field experiments reduce the likelihood of plant competition by adequately spacing plants and fertilizing and irrigating as needed, thus making this mechanism less important. Regardless, we still test for the existence of competition effects by repeating diversity treatments in Objectives 2 and 4 using greenhouse-grown plants sunk into the ground in pots, preventing resource competition. If these experiments identify effects of intra-crop diversity on plant-plant competition, we will repeat Objective 3 using potted plants, which will allow us to tease apart the direct effects of diversity on insects from the indirect effects that occur via diversity altering plant-plant competition.

Progress 04/01/18 to 03/31/23

Outputs
Target Audience:The agricultural research community Changes/Problems:During covid,in person work and data collection were challenging. We responded to this by shifting some of our emphasis to analyzing existing plant chemical data, making us more efficient at producing new knowledge related to the grant objectives. What opportunities for training and professional development has the project provided?Over the course of the project, one postdoc, one graduate student, one post bacc, and more than eight undergraduate students were mentored and trained on agricultural research. How have the results been disseminated to communities of interest?Yes, published in peer reviewed journals, presented at scientific conferences, seminars. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Over the course of the project, we have accomplished all of these objectives. Our work has resulted in many scientific presentations and four publications (one in revision) on all of these objectives. We have examined pest physiology and responses to predatoers (Obj. 1), effects on pest movement (Obj. 2), predator-prey interactions (Obj. 3), and recruitment of natural enemies (Obj. 4). We also assembled a large database of plant chemistry (Obj. 5) that can be used as a foundation for future studies.

Publications

  • Type: Journal Articles Status: Under Review Year Published: 2023 Citation: Glassmire, A.E., K.C. Hauri, D.B. Turner, L.N. Zehr, K. Sugimoto, G. Howe, and W.C. Wetzel. In review. The frequency and chemical phenotype of neighboring plants determines the effects of intraspecific plant diversity.


Progress 04/01/22 to 03/31/23

Outputs
Target Audience:The agricultural research community Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?One graduate student, one post bacc, and three undergraduates were mentored and trained in connection with the project How have the results been disseminated to communities of interest?Published in peer reviewed journals, presented at scientific conferences, seminars. What do you plan to do during the next reporting period to accomplish the goals?To continue analyzing data and writing and publishing papers.

Impacts
What was accomplished under these goals? We analyzed previously collected data, wrote and submitted one manuscript, assembled a trait database, and analyzed the trait database, which we are preparing for publication.

Publications


    Progress 04/01/21 to 03/31/22

    Outputs
    Target Audience:The agricultural research community Changes/Problems:Covid made in person work and data collection challenging. We responded to this by shifting some of our emphasis to analyzing existing data, making us more efficient at producing new knowledge related to the grant objectives. What opportunities for training and professional development has the project provided?One postdoc, one graduate student, and two undergraduates trained on agricultural research. How have the results been disseminated to communities of interest?Published in peer reviewed journals, presented at scientific conferences, seminars. What do you plan to do during the next reporting period to accomplish the goals?To continue analyzing data and writing papers.

    Impacts
    What was accomplished under these goals? We have now published papers advancing our understanding of objective 1, objective 2, objective 3, and we have collected data on the other objectives.

    Publications

    • Type: Journal Articles Status: Published Year Published: 2022 Citation: Hauri, K.C., A.E. Glassmire, B. Randall, L. Zehr, and W.C. Wetzel. 2022. Plant chemical diversity and its frequency have distinct but complementary effects on insect foraging. Journal of Applied Ecology.


    Progress 04/01/20 to 03/31/21

    Outputs
    Target Audience:Agricultural research community Undergraduate trainees Graduate trainees Changes/Problems:We are making good progress on the objectives, but safety restrictions on in person work during 2020 due to covid-19 limited our ability to collect data to some extent. Fortunately, we had already completed the bulk of the proposed data collection and have data for multiple papers. This means that, even though we will be slowed somewhat by covid-19, we still foresee successful completion of the proposed work. What opportunities for training and professional development has the project provided?Trained undergraduate and graduate students and a research technician on agricultural research methods. How have the results been disseminated to communities of interest?Published papers Conference presentations Departmental seminars Twitter What do you plan to do during the next reporting period to accomplish the goals?We plan to finish data collection and focus on analyses and writing. We are currently nearing submission on two manusripts and have more in the pipeline.

    Impacts
    What was accomplished under these goals? In this reporting period, we made major progress on several objectives. This included two papers published and multiple presentations and departmental seminars given to disseminate the results of our research. Becaues of safety restrictions placed on in person research due to covid-19, we focused on data, data analyses, and writing during this reporting period. Fortunately, we had already collected a lot of data and were in a good position to analyze and write.

    Publications

    • Type: Journal Articles Status: Published Year Published: 2020 Citation: Glassmire, A.E., L. Zehr, and W.C. Wetzel. 2020. Disentangling the dimensions of plant chemical diversity: alpha and beta diversity have distinct effects on an insect herbivore. Ecology 101: e03158.
    • Type: Conference Papers and Presentations Status: Published Year Published: 2020 Citation: Glassmire, Andrea E., Luke Zehr, and W.C. Wetzel. 2020. Chemical diversity in plant neighborhoods drives insect community assemblage. Annual Meeting of the Entomological Society of America, digital meeting.
    • Type: Journal Articles Status: Published Year Published: 2021 Citation: Hauri, K.C., A.E. Glassmire, and W.C. Wetzel. 2021. Plant chemical diversity rather than cultivar diversity predicts pest suppression by natural enemies on tomato. Ecological Applications 31: e2289.


    Progress 04/01/19 to 03/31/20

    Outputs
    Target Audience:agricultural scientists the agricultural research community postdocs trainees, graduate students, undergraduate students Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?We trained 4 undergradutes, one graduate student, and on postdoc on field work, lab work, insect identification, data analysis, writing, and oral presentation skills. How have the results been disseminated to communities of interest?Papers, manuscripts in review, oral presentations, poster presentations What do you plan to do during the next reporting period to accomplish the goals?In the next reporting period, we are going to focus on identifying insects from past experiments, analyzing data, writing, and publishing our manuscripts. However, we are also planning to start a new experiment focused on pest population dynamics.

    Impacts
    What was accomplished under these goals? In this reporting period, we made major progress on each of our project objectives. Thisincluded the submission of three manuscripts for to journals for peer review and five presentations at scientific conferences. For our first objective on the effects of intra-crop defense diversity on pest physiology, we submitted a manuscript for review in the journal Ecology and completed a lab experiment. For our second objective on pest movement, we completed a major field experiment, analyzed the data, and are nearly done with a draft manuscript. For our third objective on pest dynamics and predator-prey interactions, we finished a manuscript and submitted it to the journal Ecological Applications. For our fourth objective on natural enemy recruitment, we made progress on identifying insects and analyzing data from a field experiment we conducted in the previous reporting period. We will start writing a manuscript based on this experiment later in spring 2020 to be submitted to a journal by the end of the year. For our fifth objective, we have made progress quantifying and describing new chemical feastures in our tomato genotypes. In addition, I completed and submitted a perspective paper on plant chemical diversity and its role in ecology. It was published in Ecology Letters in early 2020.

    Publications

    • Type: Journal Articles Status: Published Year Published: 2020 Citation: Wetzel, W.C. and S.R. Whitehead. 2020. The many dimensions of phytochemical diversity: linking theory to practice. Ecology Letters 23: 16-32.
    • Type: Journal Articles Status: Under Review Year Published: 2020 Citation: Glassmire, A., L. Zehr, and W.C. Wetzel. In review. Disentangling the dimensions of phytochemical diversity: alpha and beta have contrasting effects on herbivore performance.
    • Type: Journal Articles Status: Under Review Year Published: 2020 Citation: Hauri, K.C., A.E. Glassmire, and W.C. Wetzel. In review. Chemical diversity rather than cultivar diversity predicts natural enemy control of herbivore pests.
    • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Jullie, A., A.E. Glassmire, and W.C. Wetzel. Undergraduate poster presentation at the MSU Undergraduate Research & Arts Forum.
    • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Frick, M., A.E. Glassmire, and W.C. Wetzel. Undergraduate oral presentation at the MSU Undergraduate Research & Arts Forum.
    • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Hauri, K., and W.C. Wetzel. Oral presentation at North Central Branch Meeting of the Entomological Society of America.
    • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Hauri, K., and W.C. Wetzel. Oral presentation at the Annual Meeting of the Entomological Society of America.
    • Type: Conference Papers and Presentations Status: Published Year Published: 2019 Citation: Glassmire, A.E., and W.C. Wetzel. Oral presentation at the Annual Meeting of the Entomological Society of America.


    Progress 04/01/18 to 03/31/19

    Outputs
    Target Audience:Undergraduate trainees Graduate trainees Post-doctoral trainees The agricultural research community Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided?This research has provided training and professional development for one graduate student, one postdoctoral scholar, and four undergraduate researchers. The student and postdoc are currently collaboratively writing multiple manuscripts with the Project Director. They have also both presented their work multiple times at national and international conferences. How have the results been disseminated to communities of interest?Our work has alreadyled to six presentations at national/international conferences, and we have two manuscripts in preparation, which are to be submitted in summer and fall2019. What do you plan to do during the next reporting period to accomplish the goals?For the next reporting period, we will complete the T. ni component of obj. 2 and start the aphid component of objectives 1, 2, 3, and 4. We will also continue the trait measurements for objective 5.

    Impacts
    What was accomplished under these goals? We are currently on schedule to complete the objectives in the proposal. We have completed the fieldwork and labwork for the T. ni component of objectives 1, 3, and4. We are currently conducting experiments for objective 2. We have completely multiple facets of objective 5. This work has alreadyled to six presentations at national/international conferences, and we have two manuscripts in preparation, which are to be submitted in summer and fall2019. Our preliminary results are promising and suggest our work will represent an important contribution to the field.

    Publications

    • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: W. C. Wetzel. Dimensions of phytochemical diversity: A multi-scale framework for studying the ecology and evolution of plant defense. Ecological Society of America Annual Meeting. New Orleans, LA. August 2018.
    • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: A. Glassmire and W. C. Wetzel. Phytochemical diversity of tomato plants influence oviposition preference of a specialist moth, Manduca sexta. Ecological Society of America Annual Meeting. New Orleans, LA. August 2018.
    • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: A. Glassmire and W. C. Wetzel. Phytochemical diversity of tomato plants influence oviposition preference of a specialist moth, Manduca sexta. Entomological Society of America Annual Meeting. Vancouver, Canada. November 2018.
    • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: K. Hauri and W. C. Wetzel. Crop defense diversity influences the predator-prey interaction between an insect pest and a biocontrol predator. Entomological Society of America Annual Meeting. Vancouver, Canada. November 2018.
    • Type: Conference Papers and Presentations Status: Published Year Published: 2018 Citation: N. Britwum and W. C. Wetzel. The consequences of intraspecific diversity in defense traits on the host preference of an important agricultural pest, Trichoplusia ni. Ecological Society of America Annual Meeting. New Orleans, LA. August 2018.