Mechanisms involved in plant resistance to the green peach aphid Myzus persicae

Lead Research Organisation: John Innes Centre
Department Name: Cell and Develop Biology

Abstract

The green peach aphid (GPA) Myzus persicae and other sap-feeding insects, including other aphids, whiteflies, psyllids, froghoppers, leafhoppers, planthoppers and Lygus bugs, are economically important pests worldwide. They do not only cause direct feeding damage, but also transmit more than half (> 500) of all described plant viruses and a variety of economically important plant pathogenic bacteria. A recent example is a froghopper-transmitted bacterial pathogen (Xylella fastidiosa), which is threatening olive tree plantations in Italy and may spread to other olive-growing regions in the Mediterranean (the Guardian, 8 Jan 2015).

Whereas Bacillus thuringiensis (Bt) toxin transgenic crops (grown in USA, Brazil and Asia) are resistant to major pests, such as moths and beetles, Bt is not effective against sap-feeding insects. Therefore, sap-feeding insect pests have increased on these transgenic crops.

GPA alone colonizes over 400 plant species of more than 50 plant families and this aphid species transmits more than 100 different plant viruses, including 6 distinct sugar beet viruses.

Sap-feeding insects are predominantly controlled by extensive insecticide applications causing these insects to develop resistance to the insecticides. GPA has developed resistance to 71 different insecticides and, as such, holds the record of most insect resistances among all insects. Neonicotinoids are one of few insecticides that can effectively control GPA. However, GPA clones resistant to these chemicals have been identified in several parts of Europe. Moreover, neonicotinoids are being taken off the market owing to increasingly restrictive (EU and national) legislation fuelled by concerns of consumers about insecticide toxicity to human health and the ecosystem.

Uncontrolled, GPA can reduce sugar beet yields by 45%, making this crop uneconomic in Europe. A similar fate is predicted for other crops susceptible to GPA, including oilseed rape, broccoli, cauliflower, cabbage, tomato, potato, pepper, sugar beet etc.

To reduce insecticide use and safeguard the food supply in Europe and worldwide, alternative methods to control GPA and other sap-feeding insects, such as the generation of plant varieties that are resistant to GPA, are essential and need to become available in the coming few years.

We anticipate that a major impact of this proposal is to make a major leap forward to achieve this goal.

Approach: GPA and other insects produce virulence proteins (effectors) in their saliva that interact with plant proteins (targets) to modulate key plant processes, such as plant defense responses, that make the plants more susceptible to aphid colonization. Hence, we wish to increase plant resistance to aphids by preventing effector-target interactions through the introduction of effector-insensitive target alleles into plants using transgenic and non-transgenic approaches.

If successful, this project will open up a plethora of new avenues to obtain resistance to GPA, and possibility other sap-feeding insects, of multiple economically important plant species.

This project is a collaboration with SESVanderHave UK LTD (SV), a leading breeder of sugar beet varieties with a proven performance worldwide. A goal of this proposal is for SV to develop resources and technologies so that they will be in an excellent position to take advantage of the new discoveries made in this project and obtain GPA-resistance sugar beet more quickly.

Currently low numbers of students are being trained in (a combination of) entomology, agriculturally important insect pests and plant breeding. Therefore, we will engage young students in our project.

Since we anticipate that this project will provide an example of how plant-breeding approaches can generate sustainable resistance to insect pests, we will organize outreach activities to engage plants breeders and downstream processors of multiple crops in our approach.

Technical Summary

The green peach aphid (GPA) Myzus persicae is an agronomically important pest worldwide. This aphid colonizes > 400 different plant species in > 50 plant families. Remarkably, a single GPA clone (consisting of genetically identical individuals) has this wide plant host range. Being polyphagous GPA is one of few exceptions given that about 80% of all insect herbivore species can colonize only one or several closely related plant species.

The Hogenhout group sequenced and assembled the GPA genome and used the sequence to identify GPA effectors. These effectors are present in the GPA saliva and interact with specific proteins (targets) in plant cells leading to suppression of processes early in the plant defence response. We identified plant targets of two of these GPA effector proteins and have evidence that they are essential for aphid colonization. Moreover, we found that the plant targets are conserved among plant species, including Arabidopsis thaliana, Nicotiana benthamiana and Beta vulgaris (sugar beet).

The goal of this project is to introduce effector-insensitive target alleles to increase resistance to GPA of both a model plant species (A. thaliana) and a crop species (sugar beet).

This project is a collaboration with SESVanderHave UK LTD (SV), a leading breeder of sugar beet varieties with a proven performance worldwide. Via further development of TILLING resources and genome-editing technologies, SV will be at an excellent position to take advantage of the new discoveries in this project and obtain GPA-resistance sugar beet relatively quickly.

We anticipate that this project will open up a plethora of new avenues to obtain resistance to GPA, and possibility other sap-feeding insects, of multiple economically important plant species. We will organize outreach activities to engage plants breeders and downstream processors of crops in our approach and to entice young students to do a PhD in projects focused on plant-insect interactions.

Planned Impact

PROBLEM: The green peach aphid (GPA) Myzus persicae is an economically important pest on multiple crops worldwide. Neonicotinoids are one of few insecticides that can effectively control GPA (for example, 95% of sugar beet seed sold in the UK is treated routinely with neonicotinoids, with similar uptake in Europe and USA). However, GPA clones resistant to these chemicals have been identified in several parts of Europe. Moreover, neonicotinoids are being taken off the market owing to increasingly restrictive (EU and national) legislation fuelled by concerns of consumers about insecticide toxicity to human health and the ecosystem. Unfortunately, uncontrolled, aphid pests threaten production and the viability of the wider industry it supports (for example, 13,000 jobs & £1 billion in the UK for sugar beet alone). A similar fate is predicted for other crops susceptible to GPA, including oilseed rape, broccoli, cauliflower, cabbage, tomato, potato, pepper etc.

The UK production is particularly threatened by aphid-borne diseases due to our milder maritime climate, 12 month growing season and 160 day harvesting campaign. Northern Europe faces similar risks. Critically the wide host and geographical range of GPA accelerates resistance to neonicitinoid insecticides, increasing the urgency for a durable genetic solution in sugar beet and other crops without indescriminate use of insecticides.

SOLUTION: To reduce insecticide use and safeguard the food supply in Europe and worlwide, alternative methods to control GPA and other sap-feeding insects, such as the generation of plant varieties (via seed) that are resistant to GPA, are essential and need to become available in the coming few years.

We anticipate that a major impact of this proposal is to make a major leap forward to achieve this goal.

APPROACH: GPA and other aphids produce virulence proteins (effectors) in their saliva that interact with plant proteins (targets) to modulate key plant processes, such as plant dfense responses, that make the plants more susceptible to aphid colonization. Hence, we wish to increase plant resistance to aphids by preventing effector-target interactions through the introduction of effector-insensitive target alleles into plants using transgenic and non-transgenic (plant breeding) approaches.

This project involves the SESVanderHave UK LTD (SV), a leading breeder of sugar beet varieties with a proven performance worldwide. SV will develop resources and technologies so that they will be in an excellent position to take advantage of the new discoveries made in this project and obtain GPA-resistance sugar beet more quickly.

ECONOMIC IMPACT: For beet alone, the total market is valued at around £30m (sugar beet £23m, fodder beet £3m, energy beet £0.5m) in the UK. The top 6 Northern European countries (including the UK) have a total sugar beet seed market worth £260m. This is expected to increase following the 2017 sugar reform. With the most efficient production globally, these countries are well placed to exploit new export markets, potentially doubling production and with it the requirement for Sugar Beet Seed. The global sugar beet market was 4,312,000ha in 2014, approximately £500m.

Upon success, this project will constitute a considerable paradigm shift and open up a plethora of new avenues to obtain resistance to GPA, and possibility other sap-feeding insects, of multiple economically important crops.

OUTREACH: Since we anticipate that this project will provide an example of how plant-breeding approaches can generate sustainable resistance to insect pests, we will organize outreach activities to engage plants breeders and downstream processors of crops in our approach. Moreover, we will engage the general public by contributing to the revitalizing the science museum via interactive elements to showcase how science and innovation has delivered the next great solutions to issues that threaten food production
 
Description We identified aphid virulence factors that play fundamental roles in aphid colonization of plants and characterized mechanisms of how these virulence factors modulate plant processes. Our industrial collaborators are using this information to identify sugar beet varieties that have increased resistance to aphids and to test specific hypothesis via the generation of transgenic super beet lines.
Exploitation Route We submitted two patent applications. Additional funding was obtained to generate more data to support these patent applications. The project supported an iCASE student as well. The student closely collaborates with the industrial partner.
Sectors Agriculture, Food and Drink,Chemicals,Education,Environment,Manufacturing, including Industrial Biotechology

 
Description My group has shared knowledge and research progress on aphid-plant interaction research and mechanisms involved in virus transmission by aphids with industry, that is SESVanderHave, who are collaborators on the BBSRC-LINK project. SESVanderHave is using this information to characterize aphid resistance in sugar beet. Two patent applications were submitted and additional funding was obtained the further the work started in this grant and to support the patent applications. The project also resulted in an iCASE studenthip and the student working on this studentship has established close contacts with the industrial partner.
First Year Of Impact 2017
Sector Agriculture, Food and Drink,Education,Environment,Manufacturing, including Industrial Biotechology
Impact Types Societal,Economic

 
Description Hosted colleague from industry for teaching lab technique
Geographic Reach National 
Policy Influence Type Influenced training of practitioners or researchers
Impact Taught industrial partner specific lab technique.
 
Description Assess sugarbeet resistance to aphids
Amount £9,870 (GBP)
Organisation Sesvanderhave 
Sector Private
Country Belgium
Start 02/2019 
End 02/2020
 
Description In kind contribution to LINK grant
Amount £414,657 (GBP)
Organisation Sesvanderhave 
Sector Private
Country Belgium
Start 04/2016 
End 09/2019
 
Description Institute Innovation Funds
Amount £124,000 (GBP)
Organisation John Innes Centre 
Sector Academic/University
Country United Kingdom
Start 11/2018 
End 12/2020
 
Description iCASE PhD studentship
Amount £27,800 (GBP)
Funding ID 1805607 
Organisation John Innes Centre 
Sector Academic/University
Country United Kingdom
Start 10/2016 
End 09/2020
 
Title Insect cell based expression system 
Description We successfully setup insect cell (Sf9 cells)-based protein production system using the baculovirus bac-to-bac method. Different purification methods were tried out to obtain enough protein for crystallography. 
Type Of Material Technology assay or reagent 
Year Produced 2018 
Provided To Others? Yes  
Impact At least two labs at JIC and TSL are using the system. 
 
Description Collaboration with University of Kyoto 
Organisation University of Kyoto
Country Japan 
Sector Academic/University 
PI Contribution Collaborator is involved in a research project of a PhD student in the lab
Collaborator Contribution Collaborator provided transgenic plant lines for screening
Impact Progress made with research goals of PhD student project
Start Year 2018
 
Description Collaboration with University of Oxford 
Organisation University of Oxford
Department Department of Plant Sciences
Country United Kingdom 
Sector Academic/University 
PI Contribution Visited colleagues at University of Oxford to discuss specific project and experimental approaches
Collaborator Contribution Contributed knowledge and resources for new experiments
Impact Progress with achieving research goals by graduate student and postdoctoral researcher in the lab. Making plans for a collaborative research proposal.
Start Year 2019
 
Description Collaboration with plant breeding company on an iCASE studentship 
Organisation Sesvanderhave
Country Belgium 
Sector Private 
PI Contribution PhD student in the laboratory is generating aphid genome sequence data and population structure analyses. Student is enrolled in supervisory system at JIC and engages with experienced researchers in the lab and at JIC.
Collaborator Contribution Provides staff and resources for conducting the study and involved student in research project at the company for 3 months.
Impact PhD student made excellent progress with his research and generated data useful for the host lab at JIC and the industrial partner.
Start Year 2016
 
Description Collaboration with sugar beet seed breeding company 
Organisation Sesvanderhave
Country Belgium 
Sector Private 
PI Contribution Expertise on sap-sucking insect pests, such as aphids and leafhoppers, and molecular plant-insect interactions, insect genomics, the Arabidopsis thaliana model system and translation of knowledge obtained from a model plant to a crop. Writing of projects to obatin research funding.
Collaborator Contribution Sugar beet germplasm collections and genome sequence data an expertise in sugar beet genetics and breeding strategies.
Impact Outputs and outcomes are confidential. Two patents were filed.
Start Year 2017
 
Description Collaborations with The Sainsbury Laboratory 
Organisation John Innes Centre
Department The Sainsbury Laboratory
Country United Kingdom 
Sector Charity/Non Profit 
PI Contribution Provide knowledge on the aphid-plant interactions experimental system.
Collaborator Contribution Colleagues at The Sainsnury Laboratory have contributed knowledge and expertise to a PhD student project in my lab.
Impact The PhD student made good progress with achieving research goals of his PhD project.
Start Year 2017
 
Description Formal research collaboration with SESVanderHave 
Organisation Sesvanderhave
Country Belgium 
Sector Private 
PI Contribution My research group has provided advise on strategies to obtain aphid resistant sugar beet, exchanged knowledge on research progress in plant-insect interactions of the lab, and wrote BBRSC-LINK award to fund research.
Collaborator Contribution SESVanderHave provides access to sugar beet breeding lines, genome sequence resources for these lines and insecticide-free field sites for collection of aphid populations in UK and Europe. They also funded a postdoctoral researcher in my group for one year, contributed 50% in-kind funds for the BBSRC-LINK award and funds a iCASE studentship in my group. PhD student Roland Wouters was recruited for the iCASE project. Roland is making good progress.
Impact Generated knowledge on plant-insect interactions. Organized visits of the SESVanderHave team to JIC (two times per year) and my group at JIC to SESVanderHave headquarters in Tienen, Belgium (two times per year). Organized regular Skype calls to discuss research progress and ideas for future research.
Start Year 2013
 
Description Contributed an 'Accessible Science Talk' for the Research and Support Staff Voice (RSSV) 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Professional Practitioners
Results and Impact The JIC Research and Support Staff Voice (RSSV) organised a day (9 Oct 2018) of talks as part of the JIC Annual Science Meeting, delivered by top scientists from JIC and TSL. Every talk was accessible to a wide audience including scientists, support and partnership staff and communicates the great work carried out at JIC and TSL, presented in a manner that will be understandable and interesting for all.
Year(s) Of Engagement Activity 2018
 
Description Engagement with SV 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Industry/Business
Results and Impact Three-monthly meetings with industrial collaborators
Year(s) Of Engagement Activity 2017,2018,2019
 
Description Hosted Alexander Stacey, BSc student Biological Sciences, University of East Anglia, UK. 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Undergraduate students
Results and Impact Student worked on a research project in the summer of 2018 and his BSc research project from Jan-Mar '19.
Year(s) Of Engagement Activity 2018,2019
 
Description Hosted Alexandra Kolodyazhnaya, BSc student Novosibirsk State University, Russia 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Undergraduate students
Results and Impact Student did a research project in my lab as part of the JIC/TSL/EI International Undergraduate Summer School programme at JIC.
Year(s) Of Engagement Activity 2018
 
Description Hosted Libby Hanwell, BSc student Biological Sciences, University of East Anglia, UK 
Form Of Engagement Activity A formal working group, expert panel or dialogue
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Undergraduate students
Results and Impact Hosted the student for a research project in the summer of 2018 and her BSc research project from Oct-Dec '18
Year(s) Of Engagement Activity 2018,2019
 
Description ICE, Florida, USA 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Presented an invited talk at the International Conference of Entomology (ICE), Orlando, Florida, USA.
Year(s) Of Engagement Activity 2016
 
Description Invited research seminar at iDiv, Leipzig, Germany 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact I was invited by PhD students to give a research presentation at the Integrative Biodiversity Research Institute (iDiv), Halle-Jena-Leipzig, Germany, 18 Apr 2018. I was hosted by Crispus Mbaluto, PhD student at iDiv.
Year(s) Of Engagement Activity 2018
 
Description Invited research seminar at the Max Planck Institute, Cologne, Germany 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact I was invited to give a research seminar at the Max Planck Institute for Plant Breeding, Cologne, Germany. Approximately 50 people, including PhD students, attended.
Year(s) Of Engagement Activity 2018
 
Description Invited research seminar at the annual Life Sciences conference, Beijing, China 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Presented a talk in a paralell session focused on insect pests at the Life Sciences Conference, Beijing, China, 28-31 Oct '19.
Year(s) Of Engagement Activity 2018
 
Description Presented a talk at Monogram 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Presented a talk at Monogram, JIC, Norwich, UK, 24-16 Apr 2018.
Year(s) Of Engagement Activity 2018
 
Description Presented talk at JIC "Science for Innovation Showcase" event 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Industry/Business
Results and Impact Presented a talk at the JIC "Science for Innovation Showcase" event, Norwich, UK, 7-8 Feb '18. I explored opportunities to collaborate with industry.
Year(s) Of Engagement Activity 2018
 
Description VBD, Liverpool 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Presented a research talk about my lab's recent progress made in aphid-plant interactions research at the UK Vector-Borne Diseases meeting.
Year(s) Of Engagement Activity 2016