Contrary to conventional wisdom, not all insect herbivores impose negative fitness consequences on their plant hosts and not all induced plant responses affect the attacking insects negatively. This project hypothesizes that the underlying recognition and signaling mechanisms of the plant are subject to a co-evolutionary arms race between plants and insects, so that specifically induced plant responses could be to the benefit/disadvantage of both sides; the responding plant and the herbivore manipulating the plant. Previous studies suggest the existence of compensatory regulation mechanisms that may specifically influence both primary and secondary metabolism to increase plant defense without decreasing photosynthesis and growth. This project will elucidate the function of induced changes in plant primary and secondary metabolism of the wild tobacco Nicotiana attenuata when attacked by the mirid bug Tupiocoris notatus, evaluating fitness consequences for the plant and the insect and uncovering the underlying physiological mechanisms of those responses. Integrative functional analysis of plant responses to herbivory are used to understand the ecological mechanisms that drive plant-insect co-evolution. The manipulation of such a plant defense mechanism in crop and horticultural plants would allow the development of more sustainable, yet cost efficient methods of pest control. Moreover, identifying mechanisms that increase photosynthetic activity is a major opportunity to increase agricultural productivity.

Broader Impacts The project's broader impacts involve the professional development of two young scientists and combine research foci of both laboratories, one of which focuses on the analysis of plant photosynthesis processes and the other on herbivore-induced plant defenses. Undergraduate students will be involved in all stages of the project and will be able to gain academic credit for their involvement in practical research courses in both academic institutions. The geographic proximity of Cornell and Ithaca College allows the students to take advantage of the research environments of both institutions. Under the framework and guidance of the new Molecular and Chemical Ecology Initiative of Cornell aspects of this project will be used to develop undergraduate and graduate educational curriculum. In addition to undergraduate education this project will include the training of a postdoctoral associate and a graduate student.

Project Report

Wild tobacco, Nicotiana attenuata, attacked by Tupiocoris notatus mirid bugs becomes resistant against more damaging herbivores through mirid-induced direct and indirect defenses. Thereby, mirid-induced resistance and tissue loss do not result in a reduction of plant fitness. Thus specific induced responses allowi the plant to compensate for the lost tissue and resources allocated into defenses. With this project we found that (a) feeding by Manduca sexta larvae results in a strong down-regulation of photosynthesis, while (b) feeding by Tupiocoris bugs results in a specific induction of elevated photosynthetic activity in the remaining tissue of insect-damaged N. attenuata leaves. An in-detail analysis of the induction mechanisms revealed that the plant metabolic changes are specifically elicited by compounds in the mirid salivary secretions. The elevated CO2 assimilation rate is sufficient to compensate for the loss of photosynthetically active tissue and balances the net photosynthesis of infested leaves. Moreover, we found that Tupiocoris bugs prefer plant genotypes with low constitutive resistance (tobacco species, N. tabacum, respond similarly and show increased photosynthesis in response to Tupiocoris damage and decreased photosynthesis in response to damage by Manduca caterpillars. In contrast another host species, tomato (Solanum lycopersicon), did not respond at all to herbivory with changes in primary metabolism. These results suggest a high specificity of the plant response and genotypic variation in the response of the host plant and possible co-evolutionary paths that can lead to a quasi-mutualistic interaction between plants and their attackers. However the overcompensating plant response comes with disproportionate opportunity costs. Plants that were attacked by Tupiocoris and simultaneously suffered drought stress experienced stronger reduction in seed set than undamaged control plants or Manduca caterpillar- damaged plants under drought stress. Tupiocoris-damaged plants under normal water conditions had no reduced fitness when compared to control plants, and Manduca damage significantly reduced plant fitness. These results suggest that the increased photosynthetic activity induced by Tupiocoris attacks may result in increased negative fitness effects for the plant when additional stresses, such as drought, are acting on the plant. Drought is expected to be an important stress in the plants’ natural environment, the Great Basin desert in Utah, and may explain the maintenance of high plant genotypic variation in induced responses to Tupiocoris and preferences of Tupiocoris. As a hint to the underlying physiological mechanisms, increased drought caused a disproportionate increase in ABA production in plants that were attacked by Tupiocoris as compared to control plants or plants attacked by Manduca. ABA increases are usually associated with drought stress and allow plants to regulate conductance to save water. This is relevant to the hypothesis that the Tupiocoris-Nicotiana specific interaction can be considered mutualistic, because additional stresses like drought can affect the balance between two interactors in a mutualistic relationship. A macro-evolutionary analysis of plant induced resistance specificity to herbivory on Solanaceae plants revealed a strong relationship between plant mating system (e.g. self-compatible/self-incompatible) and the specificity and magnitude of inducibility. This project found that the evolutionary transition to self-compatibility is associated with a shift in defensive strategy from high constitutive resistance to increased inducibility of resistance, and that self-compatible plants respond with higher specificity to herbivore damage, thus are better able to differentiate between different damaging agents. This finding is transformational because it provides a new hypothesis for the evolution of induced resistance. The analysis of secondary metabolite production revealed that a) compound diversity is highly correlated with resistance to herbivores, b) self-compatible plants produce significantly fewer compounds in various compound classes than self-incompatible plants, and c) resistance patterns are strongly linked to phytohormone expression. These findings led to the new hypothesis that inducibility and high constitutive compound diversity represent alternative plant defense strategies. Our related study in Solidaga altissima revealed that the relief from herbivory as an agent of natural selection leads to evolution of reduced herbivore resistance, but this loss in resistance is specific to certain herbivore species and does not affect others. Following up on this interesting pattern, we found that distinct groups of secondary metabolites produced in Solidago plants are correlated with the resistance to certain individual herbivore species. The specificity of induced responses can consistently be found across different plant genotypes. This means that although plant genotypes may differ in their resistance to different herbivore species, they all will respond very similarly to a given herbivore species. This suggests important ecological functions of the specificity of plant responses and whole community effects of specificity per se. In addition to the high scientific merits, this project provided professional development and educational opportunities for three postdocs, two graduate students and five undergraduate student. Results and experimental procedures generated in this project are used in Cornell chemical ecology classes. Support for one research associate allowed maintenance of an analytical core facility that supported research in more than 20 research units on Cornell campus.

Agency
National Science Foundation (NSF)
Institute
Division of Integrative Organismal Systems (IOS)
Application #
0950225
Program Officer
Irwin Forseth
Project Start
Project End
Budget Start
2010-04-15
Budget End
2014-03-31
Support Year
Fiscal Year
2009
Total Cost
$456,690
Indirect Cost
Name
Cornell Univ - State: Awds Made Prior May 2010
Department
Type
DUNS #
City
Ithica
State
NY
Country
United States
Zip Code
14850