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

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.

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.

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 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 (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