Parasites often manipulate their hosts in ways that favor the transmission of the parasite to other hosts. For pathogens that are transmitted by insect vectors, host odors are a likely target for such manipulation, because both plant- and animal-feeding insects use odor cues when foraging for food. But, little is known about how pathogen effects on host odors and other aspects of host chemistry influence the ecology of disease transmission by insects. This project will explore the effects of a widespread plant pathogen, cucumber mosaic virus on features of its host plant that influence key interactions with aphids, a common insect vector for the virus. Preliminary results indicate that aphids perform poorly on plants infected by cucumber mosaic virus, and rapidly leave infected plants when given an opportunity to move to healthy plants. Surprisingly, aphids are nevertheless attracted to the odors of infected plants, which release elevated levels of a blend of airborne chemicals that is otherwise similar to the odor of healthy plants. These findings suggest that it may be a good strategy for pathogens to exaggerate the cues used by insect vectors to find hosts. This research project will test that hypothesis by combining techniques and concepts from ecology, chemistry, and plant physiology to examine the understudied interactions among pathogens, plants, and insect vectors, and the consequences of these changes to interactions between pest insects and their natural enemies.

The knowledge gained from this study will be useful in developing management strategies for controlling viruses in agriculture. More generally, results from this project have broader relevance to understanding disease ecology and evolution, including human diseases that are spread by insect vectors, such as malaria. The proposed research will be integrated with educational activities aimed at training high-school and undergraduate science students. This project is well suited for K-12 education because it is easily broken down into units addressing distinct hypotheses that can provide research opportunities for students with little previous laboratory experience. This project will also support the dissertation research of a graduate student.

Project Report

Parasitic organisms often rely on vector insects to move them from one host to another. In order for parasite acquisition and inoculation to occur a vector must locate and visit an infected host, engage in specific feeding behavior for a sufficient amount of time to acquire the parasite, and then disperse to feed on a new host. Vector foraging and feeding behavior are influenced by host characteristics that communicate information about quality, such as smell, taste, and appearance (size or color). Parasite infection can cause significant changes in host physiology that may have effects on these characteristics, making hosts more or less attractive, palatable, or nutritious for vectors. A large body of research examining parasites that infect animal hosts has shown that many of these organisms possess adaptations for changing host smell, taste, quality, or appearance in ways that make them more likely to be transmitted by vectors or acquired by intermediate hosts. However, this phenomenon of parasite manipulation has not been well studied in parasites infecting plants, even though plant parasites are important for natural plant communities, agriculture, and human health. To better understand how plant viruses change host smell, taste, quality, and appearance this project examined the changes that occur in a common crop host plant (squash) in response to infection by a common, economically important plant virus (Cucumber mosaic virus [CMV]). Since these changes can influence how insects interact with the host plant, we also examined the behavior and preferences of aphids that are vectors of CMV, insects that are not vectors but which are pests on squash, and predatory insects that help control both aphids and other pest insects. We found that CMV infection changes the host plant to make it less nutritious and better defended against aphid vectors, which encourages these insects to move to a new plant after feeding and acquiring virus particles, enhancing virus spread. These changes also influence non-vector pests, which do not like the taste of CMV-infected plants and so do not remain and feed on these plants when healthy plants are available. However, we also found that predators can still find prey placed on CMV-infected plants, and that prey insects feeding on CMV-infected plants are less able to defend themselves against predators. Our results show that CMV can change host plants in ways that enhance virus spread and that protect the plant from attack by non-vector insects. This information is important for predicting virus outbreaks, breeding plants with resistance to plant viruses, and leveraging the benefits that viruses may confer to plants (such as enhanced resistance to insect pests). To ensure that other researchers are aware of our discoveries, the co-PI has presented this work at eight different professional venues and published three peer-reviewed papers, with two more in review or preparation for submission. In addition to providing important insight into plant-virus interactions using economically relevant model organisms, this project also served as a basis for the co-PI to oversee small sub-projects performed by several undergraduate students visiting the U.S. from Brazil, and a visiting masters student from Belgium. The co-PI also used specific components of this research to teach thousands of children and adults about insect-plant interactions and disease ecology by overseeing the insect zoo component of the Penn State Great Insect Fair (State College, PA) and through the "Smell Lab" at the World Science Festival street fair (NYC, NY).

National Science Foundation (NSF)
Division of Environmental Biology (DEB)
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Alan James Tessier
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Pennsylvania State University
University Park
United States
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