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.
The goal of this project is to understand the mechanisms and functions of a phenomenon that we term "plant vaccination" and first observed in the wild tobacco Nicotiana attenuata. A mirid bug, Tupiocoric notatus induces cross resistance to other herbivores in the native habitat but its significant feeding damage does not have any consequences for plant fitness. As a consequence plants with Tupiocoris bugs have a higher fitness in the native habitats than plants without bugs if other herbivores are also attacking the plants. Thus we seek to identify the mechanisms for how plants can compensate for the tissue loss to Tupiocoris herbivory and the allocation of resources into the expression of chemical resistance traits. Further we try to evaluate the fitness costs and benefits of this specific plant response for both the plant and the herbivore within a coevolutionary framework (see proposal document). Herbivory is thought to be detrimental to plant fitness and commonly results in a metabolic shift in the plant: photosynthetic processes are typically down-regulated, while resource allocation to defenses is increased in herbivore-attacked plants resulting in fitness costs of induced plant responses. We found that wild tobacco, Nicotiana attenuata, attacked by Tupiocoris notatus mirid bugs becomes resistant against more damaging herbivores through mirid-induced direct and indirect defenses. However, mirid-induced resistance and tissue loss do not result in a reduction of plant fitness. These findings suggest induced metabolic responses allowing the plant to compensate for the lost tissue and resources allocated into defenses. In the search for the underlying mechanisms, allowing the plant to compenstate for Tupiocoris damage, 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 N. attenuata leaves. An in detail analysis of the induction mechanisms revealed that the plant metabolic changes are specifically elicited by compounds in the in 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. The results have been summarized in a paper that has been accepted and currently awaits publication in New Phytologist. Therein, we also discuss the observed increase in the plant’s primary metabolic activity as a mechanism that allows plants to alleviate negative fitness effects of mirid attack and mediates the vaccination effects that result in a net benefit in environments with multiple herbivores. This paper provides the basis for the now following further investigations into the mechanisms and functions of herbivory-induced compensatory responses and the associated plant vaccination.
