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Functional role of the Myzus persicae (Green Peach Aphid) effector repertoire in host plant manipulation.

Reference	BB/J005258/1
Principal Investigator / Supervisor	Dr Jorunn Indra Berit Bos
Co-Investigators / Co-Supervisors
Institution	The James Hutton Institute
Department	Cell & Molecular Sciences
Funding type	Research
Value (£)	364,550
Status	Completed
Type	Research Grant
Start date	21/05/2012
End date	20/05/2015
Duration	36 months

Abstract

Aphids are phloem-feeding insect that cause significant economic losses worldwide. Myzus persicae is one of the most destructive aphid species, partly due to its very broad host range. Recent studies identified salivary proteins from M. persicae that share functional features with plant pathogen effectors. With the emerging concept that aphids, like plant pathogens, deliver effectors inside their hosts to promote infestation, understanding the functions of these secreted molecules is key for development of novel and sustainable control strategies. The overall aim of this proposal is to understand how aphids modify host cellular processes and promote infestation. Specifically, we will aim to functionally characterize aphid effectors, identify their plant host targets, and understand the roles of these targets in host-aphid associations. We will identify and characterize novel M. persicae effectors by: 1) In planta over-expression of M. persicae candidate effectors in combination with aphid performance assays; 2) Localization of M. persicae candidate effectors in planta using fluorescent fusion-proteins; 3) Identification, using Yeast-2-Hybrid (Y2H) assays and in planta pull-down experiments, of host plant targets of M. persicae effectors; 4) Investigating the contribution of M. persicae effector targets to aphid virulence using in planta host target silencing and over-expression in combination with aphid performance assays. This project will implicate plant and aphid proteins in an economically important interaction. Furthermore, this work will provide a snapshot of the plant-aphid interface and may unveil processes relevant to unrelated but important plant-insect interactions. Therefore, results are expected to impact the development of novel control strategies with low environmental and economic costs that are applicable to most if not all important crops.

Summary

Aphids are sap-feeding insects that induce extensive feeding damage, achieve high population densities and transmit economically important plant diseases worldwide. These insects cause significant economic losses in staple food and bioenergy crops, including potato, soybean, cereals, and oilseed rape. Aphid infestations are expected to increase in the future as a result of environmental changes and increased restrictions on the use of pesticides. To develop durable approaches and achieve sustainable control of aphid epidemics, it is critical to understand aphid parasitism at the molecular level. Key questions herein are: What proteins do aphids deliver inside host plants to enable infestation? How do aphids affect host cell processes? Can we generate crop varieties that have durable resistance to aphids, and thereby reduce dependence on pesticides? Like most plant parasites, aphids require intimate associations with their hosts to gain access to nutrients. Aphids have specialized mouthparts, stylets, which they use to probe different plant cell types, and to feed on plant sap in the plant vascular system. Interestingly, aphid feeding induces clogging of phloem sieve elements in the plant vascular system, which is suppressed by aphids in successful host interactions. Furthermore, aphids can perturb plant developmental processes by, for example, inducing leaf curling or the formation of galls. Suppression of plant defences and altering host physiology is common among plant pathogens and generally involves the secretion of pathogen molecules, or effectors, into host plants that manipulate plant cellular processes. This manipulation of plant cell processes may involve suppression of host defences as well as altering plant cellular processes to promote the release of nutrients through targeting of specific plant (defence) proteins. Recent evidence suggests that aphids, like other plant parasites, secrete effectors that share functional features with plant pathogen effectors. Among the over 5000 aphid species, Myzus persicae (green peach aphid) is one of the most destructive pests worldwide, partly due to its broad host range that spans hundreds of different plant species. This host range includes important crop plants, including potato, as well as model plants Nicotiana benthamiana and Arabidopsis thaliana for which an extensive set of experimental tools and resources are available. In this project, we aim to identify effectors from the aphid species M. persicae and characterize their role in plant infestation. More specifically, we will perform functional assays in N. benthamiana plants to identify novel (candidate) M. persicae effectors. To investigate the role of aphid effectors in plant cell manipulation, we will identify the plant proteins in N. benthamiana and potato that are directly targeted, and potentially modified, by M. persicae effectors. Also, we will determine the contribution of identified M. persicae effector plant targets to plant infestation. The expected results of this project will allow a comprehensive view of the strategies that aphids employ to infest plants. Specifically, this work will implicate plant and insect proteins in an economically important interaction. An understanding of the plant cellular processes targeted by aphids and the effectors required for parasitism will facilitate the development of novel and sustainable aphid control strategies to increase crop yield and reduce pesticide usage.

Impact Summary

The proposed project fits with the BBSRC strategic priorities of "food security" and "bio-energy and industrial biotechnology". In addition, the proposed project is complementary to ongoing research at the James Hutton Institute (JHI) supported by Scottish Government work-packages, which aims to understand and combat potato diseases, including those caused by aphids and aphid-transmitted viruses. Findings of the proposed research will, in the long term, contribute to the development of novel strategies to control infestations by aphids and potentially other pests, thereby improving crop yields and food security both in the UK and elsewhere, including in developing countries. With some of the aphid host plants, like oilseed rape, playing an important role in bio-fuel production, increasing crop yields is expected to positively impact the generation of bio-energy. The proposed research is expected to benefit i) plant breeding and biotechnology companies, ii) farmers worldwide, including in developing countries, iii) the general public (including potential future academics), and iv) research staff. The proposed project will benefit plant breeding and biotechnology companies in developing novel and effective control strategies against infestations of aphids and other pests. The proposed project may potentially reveal aphid effectors that are essential for plant infestation, and consequentially are interesting targets for the development of chemical control compounds. Furthermore, identification of plant (defence) proteins that are targeted by aphid effectors may provide key information for generating novel resistances in economically important crops. Finally, the identification of aphid salivary proteins may help elucidate virus transmission mechanisms. Thus, the development of novel efficient aphid control strategies will increase crop yields, while reducing pesticide costs, for farmers in the UK and elsewhere, including in developing countries. A reduction in theuse of insecticides will benefit the general public. Currently, aphid control strategies, and those of other plant pests, rely on the use of pesticides that are a threat to human and environmental health. By enabling sustainable agriculture, the proposed project will contribute to a natural environment and reduce the environmental impact of agricultural practices. The PI of the proposed project is committed to actively contribute to outreach activities to engage the general public and potential future academics. The PI will actively be involved in the JHI's outreach program. In addition, the PI and the PDRA hired on the project will display the work, as relevant to society, at the local outreach events, such as those organized by the Dundee Science Centre, attended by local schools and the general public. In addition, the PI will train summer students, honours students, and interns in laboratory techniques to engage potential future academics in biological sciences research. Research staff involved in the proposed project will benefit in terms of career development. The proposed research draws on a vast array of molecular biology and biochemistry techniques that are considered transferable skills in the biological sciences. Upon completion of the work, staff will have developed excellent research skills. In addition, the PDRA and PI will seek to further develop their professional skills by communicating science to the general public and industry. The identification and characterization of aphid effectors and their host targets will have a significant impact in the fields of plant-insect and plant-microbe interactions and thereby increase the profile of the PI and PDRA. With results of the proposed research expected to be of high impact and of great interest to the research community, this project will likely generate multiple publications in peer-reviewed journals as well as lead to invitations to national and international meetings.

Committee	Research Committee B (Plants, microbes, food & sustainability)
Research Topics	Crop Science, Plant Science
Research Priority	Global Security
Research Initiative	X - not in an Initiative
Funding Scheme	X – not Funded via a specific Funding Scheme

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