Source: PENNSYLVANIA STATE UNIVERSITY submitted to
CHEMICAL ECOLOGY OF INTERACTIONS AMONG PLANTS, NON-PERSISTENT VIRUSES, AND VECTOR INSECTS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
TERMINATED
Funding Source
Reporting Frequency
Annual
Accession No.
0225975
Grant No.
2011-67011-30655
Project No.
PEN04447
Proposal No.
2010-05236
Multistate No.
(N/A)
Program Code
A7101
Project Start Date
Aug 1, 2011
Project End Date
Jul 31, 2013
Grant Year
2011
Project Director
Mauck, K. E.
Recipient Organization
PENNSYLVANIA STATE UNIVERSITY
208 MUELLER LABORATORY
UNIVERSITY PARK,PA 16802
Performing Department
Entomology
Non Technical Summary
Pathogens and other parasites often manipulate their hosts in ways that enhance transmission. For insect-vectored pathogens, host odors and in-plant chemicals are likely targets for such manipulation, because both plant- and animal-feeding insects use host-derived volatile and in-host compounds as key foraging cues and taste cues to determine host suitability. Yet, little is currently known about the chemical ecology of insect-vectored diseases. This project explores the effects of a common plant pathogen, Cucumber mosaic virus (CMV), on features of its host plants that influence key interactions with insect disease vectors (aphids). Initial results indicate that CMV greatly reduces host-plant quality for aphids (aphid populations perform poorly on infected plants and aphids rapidly emigrate from infected to healthy plants when given the opportunity). Nevertheless, aphids are preferentially attracted to the odors of infected plants, which exhibit elevated emissions of a blend of volatile compounds that is otherwise similar to the odor profile of healthy plants. These results indicate that exaggerating existing host-location cues can be a viable vector attraction strategy for pathogens that otherwise reduce the quality of hosts to vectors. These results also suggest that transmission mechanism may be a major factor shaping the evolution of pathogen-host interactions. This project expands upon these important initial findings by examining new strains of CMV infecting different host plants, determining how CMV changes host chemistry and, through these changes, aphid behavior, and how infection of a host plant with a virus indirectly affects other organisms such as insect predators that attack aphids and other herbivores.
Animal Health Component
(N/A)
Research Effort Categories
Basic
80%
Applied
20%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2122499101010%
2122499102010%
2122499107020%
2122499200010%
2123110101010%
2123110102010%
2123110107010%
2124030107020%
Goals / Objectives
The transmission and spread of insect-vectored diseases depend on complex interactions among pathogens, hosts, and vectors. My research on the ubiquitous, non-persistently transmitted (stylet-borne) plant virus, Cucumber mosaic virus (CMV) has shown that CMV induces chemical changes in a common plant host that makes it both attractive to aphid vectors (through odor cues), but repellant through taste cues (with dispersal occurring after the vector probes and acquires the pathogen - an essential step in transmission of CMV). These results contrast with chemically induced changes in other host plants infected by plant viruses that are acquired and transmitted only through long periods of feeding by the aphid vector (persistently transmitted viruses), and suggests that transmission mode may play a role in selecting for pathogen traits that facilitate the alteration of host chemistry in ways that increase contacts with vectors and, ultimately, increase virus transmission. Building upon these initial results the work proposed here aims to address three objectives: 1) to test the generality of initial findings by examining virus-host-vector interactions using new and diverse CMV isolate-host combinations; 2) to elucidate the nutritional, morphological, and phytochemical mechanisms underlying effects of CMV on host-vector interactions; and 3) to explore broader implications of CMV-induced changes in host chemistry, including effects on tritrophic plant-herbivore-natural enemy interactions. Plant viruses pose significant threats to sustainable food production that are likely to grow more serious as climate change, and other impacts of human activity, promote the movement of vectors, plants, and pathogens into new areas, resulting in increased incidence of novel virus-host interactions. The work proposed here will significantly enhance our understanding of the mechanisms involved in such interactions, the forces shaping their emergence in ecological and evolutionary time, and their expected impacts on the abundance and distribution of vector and non-vector insects.
Project Methods
Our analysis of the existing literature suggests that characterization of more non-persistent virus-host combinations is needed to understand the general patterns of virus-host-vector interactions mediating transmission. We will therefore extend our research to examine two new CMV isolates (one from legumes, CMV-L, and one from peppers, CMV-PEP) that are considered economically important, as pepper and legume vegetable crops are increasingly being affected by infections of crop-specific CMV variants. Experiments will employ CMV-PEP and CMV-L in a series of volatile-collection experiments designed to assess patterns of volatile emissions induced by CMV relative to those from healthy plants and to identify differences among strains and between each strain in native (bean/pepper) and novel (squash) hosts. We will also perform behavioral assays with aphids in order to explore effects on attraction of vectors (odor cues only) and effects of infection on dispersal of vectors following acquisition of the virus (contact cues allowed) (as described in Mauck et al. 2010). Chemical analyses using these same isolates and isolate-host combinations (native and novel hosts) will be used to examine effects of CMV infection on host chemistry and morphology in these systems. These analyses will involve examination of nutritional changes (metabolic profiling), defense induction and phytohormone signaling, and the ease with which vectors are able to navigate through host tissues with their stylet mouthparts (electrical penetration graphing). Finally, these isolate-host combinations will be employed in studies that investigate how infection in the host plant influences natural enemies of vector and non-vector herbivores feeding on those plants. These studies will employ developmental (growth) assays of natural enemies (parasitoids) using hosts on infected and healthy host plants, as well as behavioral assays that determine whether infection influences the ease with which natural enemies locate and use hosts.

Progress 08/01/11 to 07/31/13

Outputs
OUTPUTS: Activities: Support from this grant allowed me to perform experiments to measure biochemical changes in plants in response to virus infection, to assess the effects of plant viruses on host chemistry when infecting native and unrelated novel hosts, and to assess how infection of a host plant influences interactions between aphid herbivores feeding on the plant and parasitic wasps that attack the aphids. Events: Thanks to support from this grant I was able to attend the following events: World Science Festival, June 2012 (teaching participants about plant-insect-predator interactions and other aspects of plant chemistry); Gordon conference on plant volatiles, January 2012 (presentation of work performed during the fellowship); Entomological Society of America Annual Meeting (presentation of work performed during the fellowship). Services: While supported by this grant I performed mentoring of other graduate students in the lab regarding plant-virus-vector interactions and techniques for studying them. PARTICIPANTS: PI: Performed all experiments and write ups of publications for the project. PI advisors (Drs. Mark Mescher and Consuelo De Moraes) provided input on experimental design and data analysis, input on drafts of manuscripts. Collaborators (Drs. Sanford Eigenbrode and Nilsa Bosque-Perez) provided input on a recently published manuscript pertaining to the project. Training: The PI performed training for graduate students and post docs in the lab who were also working with plant viruses and biochemical analysis of plant tissues. TARGET AUDIENCES: Delivered hands-on program through the World Science Festival to non-scientists of many ages, including youth communities at risk for being under-served in terms of science education (inner-city). Outputs of research were communicated to scientists and other stake-holders through professional meetings, including the Entomological Society of America annual meeting. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.

Impacts
Change in knowledge: Thanks to support from this grant I was able to 1) gain experience in analytical chemistry methods for determining identity and amount of biological nutrients, 2) gain experience in performing behavioral assays with insects, 3) gain experience in statistical analysis techniques, and 4) communicate important concepts in chemical ecology to non-scientists. Change in actions: This grant allowed me to 1) use new knowledge of analytical techniques to implement new protocols in the lab, 2) use experience gained during outreach events to facilitate mentoring of new graduate students, 3) use knowledge gained during literature analysis to generate publications.

Publications

  • Mauck, K. E., C. M. De Moraes, and M. C. Mescher. 2012. Biochemical and physiological mechanisms underlying effects of Cucumber mosaic virus on host plant traits that mediate transmission by aphid vectors. Plant Cell and Environment (In Review).
  • Mauck, K. E. 2012. Chemical ecology of interactions among plants, non-persistently transmitted viruses, and insects. Ph.D. Thesis, The Pennsylvania State University, University Park, PA. 207 pp.
  • Mauck, K. E., N. A. Bosque-Perez, S. D. Eigenbrode, C. M. De Moraes, and M. C. Mescher. 2012. Transmission mechanisms shape pathogen effects on host-vector interactions: evidence from plant viruses. Functional Ecology 26(5):1162-1175.