Source: UNIV OF IDAHO submitted to NRP
APHID RESPONSES TO VOLATILE ORGANIC COMPOUNDS PRODUCED BY VIRUS-INFECTED PLANTS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
Reporting Frequency
Annual
Accession No.
0196119
Grant No.
2003-35302-13354
Cumulative Award Amt.
(N/A)
Proposal No.
2003-01445
Multistate No.
(N/A)
Project Start Date
Aug 1, 2003
Project End Date
Jul 31, 2007
Grant Year
2003
Program Code
[51.2]- (N/A)
Recipient Organization
UNIV OF IDAHO
875 PERIMETER DRIVE
MOSCOW,ID 83844-9803
Performing Department
PLANT SOIL & ENTOMOLOGICAL SCI
Non Technical Summary
This project will examine the responses of the principal aphid vectors of two important disease-causing plant viruses to changes in the volatile organic compounds (VOC) produced by plants infected by these viruses. Potato leafroll virus (PLRV) is vectored primarily by the green peach aphid (GPA). Barley yellow dwarf virus (BYDV-PAV) is vectored primarily by the bird-cherry oat aphid (BCOA). We have discovered that wingless forms of these two aphid species are attracted to or arrested by VOC produced by their respective virus-infected host plants. These findings represent the first evidence of which we are aware showing that VOC from virus-infected plants influence vector behavior. The long-term goal addressed by this project is to improve understanding of the effects of virus-induced VOC on aphid vectors as a basis for innovations for monitoring vector populations and influencing their movements. Three objectives are proposed in each system: 1) Determine the responsiveness of winged forms to infection-induced changes in VOC from their host plant, 2) Determine the changes in aphid responses to VOC emitted during the progression of the disease, 3) Identify the specific infection-induced VOC causing aphid arrestment or attraction to infected plants. Results of each of these objectives in the two virus systems will be compared to discover commonalities in the mechanisms involved.
Animal Health Component
50%
Research Effort Categories
Basic
50%
Applied
50%
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2121310107080%
2121549107010%
2121550107010%
Goals / Objectives
1) Determined the responsiveness of alatae of each species to infection-induced changes in VOC from their host plant; 2) Determine the changes in aphid responses to VOC emitted during the progression of the disease in each system; 3) Identify the specific infection-induced VOC causing GPA arrestment on PLRV-infected potato and BCOLA arrestment on BYDV-infected wheat
Project Methods
To meet Objective 1, bioassays will be conducted to determine how the winged forms of the two aphid species respond to virus-infected and noninfected plants of each plant species. In a single replicate of these experiments, infected and noninfected potato plants or wheat plants will be placed randomly within a vented plexiglass cage. A sample of winged aphids will be released from a platform in the middle of the cage and their locations will be determined after 24 h. Refinements on this bioassay will assess immigration and emigration rates of the aphids. To meet Objective 2, wingless aphids will be used, following a protocol we have already shown to be effective in this context. Groups of aphids will be placed on screening above control leaves or above virus-infected leaves and their rate of emigration determined. This test will be performed using leaves of two different age classes within the plant and at weekly intervals beginning immediately after infection until disease symptoms have progressed to obviously damaging levels. Aphid responses will be compared to detect a change in response as the disease progresses. Volatile compounds in the headspace of the plants will also be analyzed at each of these time intervals to detect changes in the signal to which the aphids are responding. To meet Objective 3, the most attractive or arrestant blend of volatiles discovered while meeting Objective 2 will be collected in sufficiently large quantity for replicated bioassays. The extracted volatile blend will be deposited at physiological concentrations onto filter paper model leaves and aphid responses will be measured with the emigration bioassay described above. Electroantennogram recordings will also be made from the aphids to help determine which parts of the blend appear to be most active physiologically. Fractions of the volatile blend will be created using preparative gas chromatography and these fractions will be recombined and tested. If active, subsequent bioassays will be conducted with selected fractions removed to determine which fractions are most important alone or in combination for triggering the aphid response. Should an individual fraction be found attractive or arrestant, it will be further fractionated to isolate the activity. Individual components whose activity is suggested by this process will also be tested. Depending on aphid responses, the bioassay will be modified to determine if some of the components cause attraction vs arrestment (by changing their location at the beginning of the experiment). The information generated in this objective will be compared with the volatiles collected from plants in Objective 2 to determine whether changes in these compound concentrations help explain any differences in aphid response to the blends.

Progress 08/01/03 to 07/31/07

Outputs
OUTPUTS: During the lifetime of this project we conducted and reported on several experiments addressing all the project objectives. The work generated a body of new knowledge about the effects of certain plant viruses on plant chemicals that affect aphids that vector these viruses. This is a novel phenomenon that was previously poorly understood. Results were presented at professional meetings (12 presentations in total at two international, three regional and three national) and four invited lectures at universities. Four refereed papers were published (see below) and four more are still in preparation. These dissemination efforts have led to collaborations with colleagues at Washington State University, Cornell University and Penn Sate University. The results pertain to the emerging field of disease chemical ecology. The PD (Eigenbrode) will be co-organzing a symposium in 2008 at the International Chemical Ecology Society meeting in State College PA on this topic. One grant proposal virologist at the University of Idaho (A. Karasev) to examine mechanisms whereby infections alter volatile release from plants was funded by CSREES-NRI. The new funding will support one undergraduate and one graduate student. The work of one PhD student and two MS students was supported. The MS students completed their training and have continued in industry or graduate work. PARTICIPANTS: Sanford Eigenbrode - PD coordinated all activities associated with the project. Mentored one PhD student who worked on the project, worked on manscripts and presentations reporting project outcomes; Nilsa Bosque-Perez - co PI, Mentored one MS student who worked on the project. Worked on manscripts and presentations reporting project outcomes; Thomas Mowry - co PI, Mentored one MS student who worked on the project. Worked on manscripts and presentations reporting project outcomes; Karla Medina-Ortega - MS student, worked on aspects involving Barley yellow dwarf virus in wheat, produced a thesis and two papers in preparation; Brent Werner - MS student, worked on aspects involving dynamics of volatile production from infected potatoes, produced a thesis and one paper in preparation; Esther Ngumbi - PhD Student, worked on aspects of Potato leaf roll virus infection effects on aphids, produced one publication with several in preparation R. Srinivasan - PhD student conducted some experiments partially supported by the project; Juan Manuel Alvarez supervised Mr. Srinivasan; Hongjian Ding - Support Scientist, participated in all research activities associated with the project; Melia Nafus - undergraduate assistant worked on the project; Analiz Rodriguez - undergraduate researcher worked on the project and was co-author on a publication TARGET AUDIENCES: Scientists (Entomologists, Ecologists, Plant Pathologists)

Impacts
The presentations at meetings and visits to other institutions by the PD and other project personnel, and the publications, have resulted in new knowledge that has influenced projects by our colleagues and their students at other institutions. The students trained within the project have acquired new knowledge and gone on to continue professional careers in insect ecology and pest management. Conclusions of the project are: a) plants infected with luteoviruses can cause altered production of volatiles that affect the behavior of aphids that vector these viruses, b) Potato leafroll virus (PLRV) induces changes in the volatile blend that together influence behavior of the virus vector, the green peach aphid; no single volatile compound elevated by infection is sufficient, c) the effect is principally to arrest the aphids near infected plants, d) the effect changes over time such that volatile production and aphid responses are not detectable before 4 weeks and after 6 weeks after infection, e) aphid movement among plants depends upon infection status, f) antennectomized green peach aphids are not responsive to the virus induced changes, showing the primary importance of volatiles, g) alate green peach aphids preferrentially settle on PLRV-infecte potato plants, h) similar patterns occur for bird cherry oat aphid responding to wheat infected wtih Barley yellow dwarf virus, i) similar effects were not dectable using the pea aphid-Pea enation mosaic virus-pea plant pathosystem. These conclusions provide robust evidence for virus induced volatile effects on aphid vectors, but show that the effects vary among systems. 5) The work on potato and wheat viruses spawned related work on viruses affecting legumes, which has led to an ongoing virus risk forecasting effort in that crop.

Publications

  • Srinivasan, R., Alvarez, J.M., Eigenbrode, S.D. and Bosque-Perez, N.A. 2006. Influence of hairy nightshade Solanum sarrachoides (Sendtner) and Potato leafroll virus (Luteoviridae: Polerovirus) on the host preference of Myzus persicae (Sulzer) (Homoptera: Aphididae). Environmental Entomology 35:546-553.
  • Srinivasan, R., Alvarez, J.M., Bosque-Perez, N.A., Eigenbrode, S.D. and Novy, R.G. 2008. Effect of an alternate weed host, hairy nightshade, Solanum sarrachoides (Sendtner), on the biology of the two most important Potato leafroll virus (Luteoviridae: Polerovirus) vectors, Myzus persicae (Sulzer) and Macrosiphum euphorbiae (Thomas) (Aphididae: Homoptera). accepted Environmental Entomology.
  • Ngumbi, E., Eigenbrode, S.D., Bosque-Perez, N.A., Ding, H. and Rodriguez, A. 2007. Myzus persicae is arrested more by blends than by individual compounds elevated in headspace of PLRV-infected potato. Journal of Chemical Ecology 33:1733-1747.
  • Jimenez-Martinez, E.S., Bosque-Perez, N.A., Berger, P.H., Zemetra, R.S., Ding, H. and Eigenbrode, S.D. 2004. Volatile cues influence the response of Rhopalosiphum padi (Homoptera: Aphididae) to Barley yellow dwarf virus-infected transgenic and untransformed wheat. Environmental Entomology 33:1207-1216.


Progress 01/01/06 to 12/31/06

Outputs
Progress was made on all three of the objectives of the project. We contributed to a published a paper documenting responses of winged forms of Myzus persicae to Potato leaf roll virus (PLRV)-infected potato plants. Volatile cues were not strictly demonstrated to be involved. Using Solanum nigrum as an alternative model system, we showed that arrestment of M. persicae differed with the interval after infection by PLRV. Two M.S. students funded by this project completed their theses and graduated this year. Three manuscripts are in preparation, one describes the effects of PLRV infection status on the responses of aphids to volatiles from infected plants. A second documents the change in response of aphids to infected plants at different intervals after infection. The third documents responses of bird-cherry oat aphids (Rhopalosiphon padi) to volatiles from Barley yellow dwarf virus (BYLV)-infected wheat plants at different stages after infection. In ongoing work this year in potato, we showed clearly that the response of the aphids to infected plants depends upon the presence in the headspace of infected plants a combination of green leaf volatiles, monoterpenes and sesquiterpenes. Removing any one of these component classes reduced or eliminated the response. The aphids are responding to the blend rather than to any one component. The same objective has not been met working with the BYDV system. Individual compounds or blends relevant in this system appear to be universally attractive. The work with Potato leaf roll virus has been described in a manuscript in preparation and was presented at two professional meetings this reporting year. Work underway this year will prepare fractions of volatiles from headspace of potatoes and assay these for aphid responses. Fractionation of the volatiles was perfected this year. Other work initiated examines whether other cues besides volatiles contribute to aphid responses to infected plants. Antennectomized aphids have been prepared and appear to behave normally on plants. These insects will be bioassayed for their responses to infected and sham inoculated potato plants, with and without access to the leaf surface.

Impacts
Virus Induced Volatiles (VIVs) are heretofore unrecognized factors in the interactions between plant viruses and their vectors. The epidemiology of the diseases caused by these viruses is potentially influenced by VIVs and their eventual manipulation could help limit virus spread in agroecosystems. Active attractants and arrestants for the aphids could have applications for monitoring aphid populations to guide interventions. We are examining these effects in two of the most economically important plant viruses. Communications from colleagues indicate that other economically important viruses may also produce VIV, enlarging the potential relevance of the work.

Publications

  • No publications reported this period


Progress 01/01/05 to 12/31/05

Outputs
Activities in this project during the reporting period included several experiments in the greenhouse and laboratory to measure aphid responses to volatiles produced by virus-infected plants. The findings are: 1) Virus-induced volatiles from potato arrest and attract green peach aphid and the effect varies with disease progression but also with the type of infection: primary (due to aphid inoculation) and secondary (present in propagative tissues) 2) green peach aphids that have acquired the PLRV virus behave differently than virus free aphids, they are more readily arrested and relatively more sensitive to PLRV infection induced volatiles, 3) green peach aphid behavior (walking, antennating) differs over infected and uninfected plants and over specific volatiles typical of potato headspace, 4) neurophysiological responses (EAG) to these volatiles are weakly related to behavioral responses observed - strongest response associated with strongest behavior, but there is not a strict correlation, 5) a synthetic blend of volatiles from potato arrests the aphid much more than any individual compound, 6) Individual components identified in wheat headspace are not behaviorally active for bird cherry oat aphid, 7) bird cherry oat aphid responds to volatiles from infected wheat with increased immigration rates rather than decreased emigration as occurs for green peach aphid, 8) disease progression experiment with BYDV-wheat-bird cherry oat aphid is inconclusive, 9) work with alate aphids is inconclusive so far, but the alates appear to differ in preference from apterae. Two M.S. students have completed their research with funding from this project and are preparing publications from their theses. One Ph.D. student was recruited in May 2005.

Impacts
Virus Induced Volatiles (VIVs) are heretofore unrecognized factors in the interactions between plant viruses and their vectors. The epidemiology of the diseases caused by these viruses is potentially influenced by VIVs and their eventual manipulation could help limit virus spread in agroecosystems. Active attractants and arrestants for the aphids could have applications for monitoring aphid populations to guide interventions. We are examining these effects in two of the most economically important plant viruses. Communications from colleagues indicate that other economically important viruses may also produce VIV, enlarging the potential relevance of the work.

Publications

  • No publications reported this period


Progress 01/01/04 to 12/31/04

Outputs
Activities in this project during the reporting period included several experiments in the greenhouse and laboratory to measure aphid responses to volatiles produced by virus-infected plants. The findings are: 1) Virus-induced volatiles in the wheat-Barley yellow dwarf virus-bird-cherry oat aphid system are attractive or arrestant to the aphid. 2) The volatiles in this system are primarily attractants for the aphid. 3) Arrestment of green peach aphid by volatiles from Potato leaf roll infected potatoes changes with the progress of infection from 2 to 10 weeks after inoculation, being greatest at 4 and 6 weeks. 4) A similar pattern occurs for attraction of bird cherry oat aphid to Barley-yellow dwarf-infected wheat plants. 5) Dynamics of volatile production are being examined to explain these temporal patterns in the aphid response. 6) Within-plant differences in the response in the potato system are detectable; higher nodes produce the arresting volatiles. Experiments have been initiated to measure volatile production from individual leaves of infected potato plants. 7) The behavioral and electrophysiological response of M. persicae to individual VOC from infected plants has been determined. Some components in the blend are arrestants. 8) Closer study of aphid behavior has revealed changes in the movement rates, time spent walking and probing in the presence of physiological concentrations of these components. 9) Components vary in the strength of antennal response as measured by electroantennography. The arrestant E (2) hexene-1-ol produces the strongest response among those tested. Ongoing experiments are examining the effect of inserting components of the viral genome into potato to establish their effects on volatile production and aphid responses.

Impacts
Virus Induced Volatiles (VIVs) are heretofore unrecognized factors in the interactions between plant viruses and their vectors. The epidemiology of the diseases caused by these viruses is potentially influenced by VIVs and their eventual manipulation could help limit virus spread in agroecosystems. Active attractants and arrestants for the aphids could have applications for monitoring aphid populations to guide interventions. We are examining these effects in two of the most economically important plant viruses. Communications from colleagues indicate that other economically important viruses may also produce VIV, enlarging the potential relevance of the work.

Publications

  • Jimenez-Martinez, E.S., Bosque-Perez, N.A., Berger, P.H., Zemetra, R.S., Ding, H. and Eigenbrode, S.D. 2004. Volatile cues influence the response of Rhopalosiphum padi (Homoptera: Aphididae) to Barley yellow dwarf virus-infected transgenic and untransformed wheat. Environmental Entomology in press.


Progress 01/01/03 to 12/31/03

Outputs
This project aims to identify the implications of recent discoveries by us that potato plants infected with the luteovirus Potato leafroll virus (PLRV), emit a blend of volatile compounds (hereafter termed virus-induced volatiles or VIVs) that influence the behavior of the aphid (green peach aphid, GPA), the principal vector of this virus. The work will encompass this system and a parallel system involving wheat, Barley yellow dwarf virus (BYDV) and its principal vector, the bird-cherry oat aphid (BCOA). In each system we will examine the responses of aphids in different developmental stages (winged and non-winged) and to plants in different stages of virus infection. We will also identify the individual, active VIVs. Funding began in August 2003. Two M.S. students joined the project in September and one Ph.D. student will join the project in January 2004. We have completed one study demonstrating that VIVs in the wheat-BYDV-BCOA system are attractive or arrestant to BCOA. Potato plants are currently being produced at 5 stages of infection by PLRV for a large experiment set to begin in Jan. 2004. Work with the wheat-BYDV-BCOA system is still in the planning stages. We have also shown on a preliminary basis that GPA winged aphids are attracted to PLRV-infected potato plants although the role of VIVs in this response has not been determined. Collaborative work underway and linked to this project also includes investigations of the phenomenon using two other Solanum species in which active VIVs seem to be produced.

Impacts
Virus Induced Volatiles (VIVs) are heretofore unrecognized factors in the interactions between plant viruses and their vectors. The epidemiology of the diseases caused by these viruses is potentially influenced by VIVs and their eventual manipulation could help limit virus spread in agroecosystems. Active attractants and arrestants for the aphids could have applications for monitoring.

Publications

  • No publications reported this period