Carr Group: Disrupting aphid-mediated transmission of cucumber mosaic virus

Supervisor

Professor John Carr

Please note Professor Carr is only recruiting MPhil Students.

Brief Summary

The student will determine if a rationally devised ‘mixed cropping’ system can disrupt the transmission of plant viruses by insect vectors

Importance of Research

The transmission of plant viruses in cropping systems is mainly controlled using chemical insecticides to kill the insect ‘vectors’ that carry inoculum. The approach has limited effectiveness, is expensive and is not sustainable. The project will explore a different approach using plant microcosms under controlled conditions to feed into epidemiological modelling.  

Project Summary

Background Cucumber mosaic virus (CMV), a cucumovirus, and the potyvirus turnip mosaic virus (TuMV) are positive-sense RNA viruses that are useful models for research and important real-world pathogens that cause caused significant crop losses (1, 2). In nature, both viruses are predominantly transmitted by aphids in a non-persistent fashion, i.e., virus particles are carried loosely in the tips of the stylet mouthparts, acquired after a short feed on the epidermis, and washed out of the stylet when the aphid salivates during the initial stages of feeding (3,4). In several hosts, CMV induces production of chemicals that inhibit prolonged feeding by aphids (5, 6, 7), which is thought to encourage the dispersal of viruliferous aphids to neighbouring plants and enhance localised transmission of the virus (8,9). In some hosts, including cucurbits (5) and Arabidopsis thaliana (10) the blend of volatile organic compounds (VOCs) becomes more attractive to aphids, drawing aphids towards infected plants, which further enhances the acquisition of CMV by its vectors (8). Similar effects have been observed in this lab for TuMV (10).        

Preliminary Data Inspired by the natural transmission-accelerating effects of CMV, we hypothesised that we could disrupt aphid mediated transmission of CMV by devising mixtures of healthy plants with different degrees of attractiveness to aphids, that would enable us to slow down transmission (10) or to decoy aphids to plants which were CMV-resistant (expressing RNAi constructs directed against CMV RNA) (10). Therefore, we screened a range of Arabidopsis accessions to identify those which were more attractive than Col-0 to the aphid Myzus persicae. We found that accession Ei-2 was suitable for our experiments (10), possibly because the VOCs emitted by Ei-2 plants are distinct from those emitted by Col-0 plants (10). 

Mixing plants of different Arabidopsis accessions that differed in aphid attractiveness modified CMV transmission dynamics under controlled conditions during the initial migration of virus-bearing aphids from infected plants to new hosts. Including small proportions of CMV-resistant plants in mixtures can decoy aphids to deposit their viral cargo selectively into hosts unable to support replication. We suspect this could ‘sanitise’ vectors and inhibit further viral transmission (10). But is this approach a robust means of ‘crop’ protection and is it as good as simply deploying uniform populations of resistant plants?

What will the successful applicant do?

The aim is to obtain data to parametrise mathematical models being developed with our epidemiological colleagues and also to complete a research paper on the artificial manipulation of aphid mediated CMV transmission using rationally devised plant mixtures.

Confirm the results already obtained with one round (dispersal: 8) of virus transmission by M. persicae nymphs in microcosms of Col-0, Ei-2, or Ei-2 and Col-0 in various proportions (10). In preparation for multi-dispersal experiments improve and optimise the ease of tracking virus transmission using modified variants of CMV and TuMV engineered to express the green fluorescent protein. Progress to multiple ‘dispersals’ (8) using adult (i.e., actively reproducing) M. persicae over periods of 2-5 days. The aim is to determine if attractive/resistant plants present in the mixtures can quench a miniature ‘epidemic’ by attracting viruliferous aphids to preferentially feed on and deposit inoculum in ‘dead-end’ hosts.

Aphids can be specialist or generalists (11), and all the microcosm work has been done using M. persicae, a generalist aphid. Since we know that CMV-induced changes in aphid-Arabidopsis interactions can differ for specialist aphids (12) we will determine if time permits how a crucifer specialist (e.g., Lipaphis erysimi) and specialists on other plant groups (e.g., Aphis fabae, Macrosiphum euphorbiae) that are capable of transmitting CMV and TuMV (13) respond to these Arabidopsis accessions and to the mixtures investigated in Sections 1 and 2. The aim here is to determine if plant arrays that arrest CMV transmission by a generalist will also arrest transmission by non-specialist aphid vectors.

Training Provided 

Molecular plant pathology including work with engineered plants, molecular virology including work with engineered viruses, entomological methods

References

  1. Scholthof, K-B.G., et al. (2011) Molecular Plant Pathology 12(9), 938–954. https://doi.org/10.1111/j.1364-3703.2011.00752.x
  2. Nellist, C.F., Ohshima, K., Ponz, F., & Walsh, J.A. (2022) Turnip mosaic virus, a virus for all seasons. Annals of Applied Biology 180, 312–327. https://doi.org/10.1111/aab.12755
  3. Fereres A., & Perry, K.L. (2019). “Movement Between Plants: Horizontal Transmission,” in Cucumber Mosaic Virus. Eds. P. Palukaitis and F. García-Arenal (USA: American Phytopathological Society), pp. 173–184. doi:10.1094/9780890546109.019
  4. Powell, G. (1991). Cell membrane punctures during epidermal penetration by aphids: consequences for the transmission of two potyviruses. Annals of Applied Biology 119, 313–321. https://doi.org/10.1111/j.1744-7348.1991.tb04870.x
  5. Mauck, K. E., De Moraes, C. M., & Mescher, M. C. (2010). Deceptive chemical signals induced by a plant virus attract insect vectors to inferior hosts. Proceedings of the National Academy of Sciences of the United States of America, 107(8), 3600–3605. https://doi.org/10.1073/pnas.0907191107
  6. Rhee, S. J., Watt, L. G., Bravo, A. C., Murphy, A. M., & Carr, J. P. (2020). Effects of the cucumber mosaic virus 2a protein on aphid-plant interactions in Arabidopsis thaliana. Molecular Plant Pathology, 21(9), 1248–1254. https://doi.org/10.1111/mpp.12975
  7. Wamonje, F. O., Tungadi, T. D., Murphy, A. M., Pate, A. E., Woodcock, C., Caulfield, J. C., Mutuku, J. M., Cunniffe, N. J., Bruce, T., Gilligan, C. A., Pickett, J. A., & Carr, J. P. (2020). Three aphid-transmitted viruses encourage vector migration from infected common bean (Phaseolus vulgaris) plants through a combination of volatile and surface cues. Frontiers in Plant Science, 11, 613772. https://doi.org/10.3389/fpls.2020.613772
  8. Donnelly, R., Cunniffe, N. J., Carr, J. P., & Gilligan, C. A. (2019). Pathogenic modification of plants enhances long-distance dispersal of nonpersistently transmitted viruses to new hosts. Ecology, 100(7), e02725. https://doi.org/10.1002/ecy.2725
  9. Cunniffe, N. J., Taylor, N. P., Hamelin, F. M., & Jeger, M. J. (2021). Epidemiological and ecological consequences of virus manipulation of host and vector in plant virus transmission. PLoS Computational Biology, 17(12), e1009759. https://doi.org/10.1371/journal.pcbi.1009759
  10. Bravo Cazar, A. L. (2019). Disrupting insect-mediated transmission of plant viruses. Doctoral Thesis, University of Cambridge. https://doi.org/10.17863/CAM.40681
  11. Nalam, V., Louis, J., & Shah, J. (2019). Plant defense against aphids, the pest extraordinaire. Plant Science 279, 96–107. https://doi.org/10.1016/j.plantsci.2018.04.027
  12. Tungadi, T., Watt, L. G., Groen, S. C., Murphy, A. M., Du, Z., Pate, A. E., Westwood, J. H., Fennell, T. G., Powell, G., & Carr, J. P. (2021). Infection of Arabidopsis by cucumber mosaic virus triggers jasmonate-dependent resistance to aphids that relies partly on the pattern-triggered immunity factor BAK1. Molecular Plant Pathology, 22(9), 1082–1091. https://doi.org/10.1111/mpp.13098
  13. Kennedy, J. S., Day, M. F., & Eastop, V. F. (1962). A conspectus of aphids as vectors of plant viruses. London, UK: Commonwealth Institute of Entomology. https://doi.org/10.4039/Ent951119-10

Contact

John Carr

Research Group

Virology and Molecular Plant Pathology