Biological crop protection: a new 'slow down/speed up' strategy for aphid management

Lead Research Organisation: University of Warwick
Department Name: School of Life Sciences

Abstract

Aphids are important insect pests of a wide range of crop plants. For crops grown outdoors, including field vegetables and arable plants, the standard way of managing aphids has been to apply synthetic chemical insecticides. Originally these were very effective, but excessive use of pesticides has caused some key aphid pests to evolve resistance. At the same time, there are concerns about the environmental impact of pesticide use, which has led to many products being withdrawn from sale. Such as the neonicotinoids. This has left farmers with few workable options for controlling aphid pests which have now become a major threat to farm production. A sustainable form of aphid management that can be used by farmers is urgently needed.

To make crop protection more sustainable and less prone to resistance, it is better not to over-rely on any one intervention. Diversification of tactics can be achieved through Integrated Pest Management (IPM), a way of controlling pests by combining different, complementary control agents in an environmentally sensitive way. These should principally be biological methods that include breeding pest resistant crop varieties, the use of natural enemies such as parasitic wasps, together with 'biopesticide' products based on beneficial microbes or natural products. These crop protection tools are safe for people and the environment and so they should provide a better form of crop protection. Chemical insecticides do have a role in IPM, but they are used only when necessary in order to reduce the chances of pests evolving resistance to them. Unfortunately, because farmers have been so reliant on chemical insecticides as the principle form of pest control, there is currently no effective IPM system in place yet for the majority of aphid pests in field crops. The development of IPM has been held back by a lack of new pest control agents and the knowledge about how they interact when used together.

The project involves five interlinked pieces of work. (1) Data on gene expression from multiple brassica crop types is used to identify plant lines that have a high probability of showing resistance to aphids, and this will be confirmed in experiments with aphids feeding on plants in the laboratory. The gene expression data will allow genetic makers to be developed that can be used by seed companies in their plant breeding programmes. (2) The biological basis for plant resistance to aphids is determined using a series of laboratory and field experiments. (3) Research on fungal biopesticides is done to determine how their performance is affected by the environmental conditions in the field, and also to understand how crop plant resistance affects their efficacy against aphids. (4) Complementary research looks at how different types of brassica plant, with resistance to aphids, affect the function of parasitic wasps, which are important natural control agents of aphids on field crops. (5) The interaction of resistant crops, fungal biopesticides and parasitoids are studied in the field in an IPM system.

The aim of this project is to develop the new knowledge and tools needed for an IPM system for aphid pests of field crops. The work centres on the peach potato aphid, Myzus persicae, which is a pest of a wide range of crops and has evolved resistance to many commonly used insecticides. The experiments involve vegetable brassicas and oilseed rape but the intention is to extend the system to other crops (sugar beet, potatoes) in future research. The research is based on a hypothesis that brassica plants with partial resistance that slows down aphid development makes the pest more susceptible to biological control agents and speeds up control with biopesticides and parasitic wasps.

The project will benefit farmers and growers and others in the supply chain. The general public will benefit from improved food security and better care of the environment.

Technical Summary

This project will underpin the development of a 'slow down / speed up' IPM system for aphid pests of field crops that combines plant breeding and biological control, focusing on the peach potato aphid, Myzus persicae. Our approach involves slowing down the growth rate of pests while speeding up the performance of their natural enemies. We will investigate the hypothesis that brassica genotypes with partial resistance that slows down aphid development makes the pest more susceptible to biological control agents including biopesticides and parasitoids.

Studies have shown that defence responses in Arabidopsis against M. persicae are based around phytohormone signalling pathways and the phytoalexin camalexin. Expression analysis of gene homologues in Brassica accessions indicates that identifying partial resistance to M. persicae in Brassica crop breeding material is highly likely. The project explores how this partial host-plant resistance can be combined with biocontrol agents

The research has 5 components: (1) Candidate Brassica genotypes with potential resistance will be confirmed using a combination of transciptome analysis and phenotyping experiments. (2) The molecular basis for partial resistance to M. persicae will be investigated, informed by experiments that quantify aphid feeding and development on Brassica genotype breeding lines with aphid resistance markers. (3) Fungal biopesticides will be evaluated against M. persicae on resistant brassica genotypes and research will be done to quantify how biopesticide performance is affected by the fluctuating environmental conditions occurring in field crops. (4) The responses of parasitoids to volatiles from aphid-infested Brassica genotypes will be quantified and the role of cis-jasmone in parasitoid attraction will be elucidated. (5) Field experiments will then be done to measure aphid control on different Brassica genotypes following treatment with fungal biopesticides, parasitoids and cis-jasmone.

Planned Impact

This project will provide new knowledge and tools that will allow an Integrated Pest Management system to be developed for aphid pests of field crops. This particular project will concentrate on Myzus persicae feeding on brassicas. The project will benefit farmers and growers, crop breeding companies, biopesticide producers, agronomists and others in the supply chain. The general public will benefit from improved food security and better care of the environment.

Myzus persicae is one of the most important crop pests worldwide and causes economic losses on a wide range of crops. It is very difficult to control using a conventional approach because of widespread multiple pesticide resistance. At the moment, farmers rely on neonicotinoid pesticides but restrictions of the use of certain neonicotinoids on flowering crops, which look set to be extended to all field crops, will leave farmers with very few effective conventional pesticides. The development of a new approach to aphid pest management is one of the highest priorities for farmers, growers and policy makers.

Replacing routine applications of synthetic chemical insecticides with a biological control-based IPM system should result in fewer negative effects of excessive pesticide use on the environment, and give improved sustainability of production. The system will avoid the risk of the crop harvested having insecticide residue levels that exceed official limits.

The project will produce genetic markers for Brassica crop improvement as well as identifying partially resistant Brassica accessions. Crop breeding companies will be able to use these in marker-assisted selection to incorporate partial resistance into commercial Brassica varieties. We will also investigate aphid biocontrol with fungal biopesticides and parasitoids. Crop protection companies are very interested in developing and using fungal biopesticides, natural enemies and other biocontrol products on field crops and this research will be of obvious benefit to them.

Importantly, by taking an IPM approach, we will not be seeking a single 'silver bullet' solution for aphid pests, but rather the aim is to combine different pest management tools in complementary ways, ideally by making use of synergies between them. To this end we will provide new information on (i) the induction of innate immune pathways in Brassica by entomopathogenic fungi; (ii) attraction of parasitoids to Brassica genotypes with partial resistance to aphids; and (iii) the combined effects of partial resistance, fungal biopesticides and parasitoids (including use of cis-jasmone as an attractant) in an IPM system. The potential threat of hyperparasitism in field crops will be investigated. This approach has not been used before for aphids on field crops and represents a step change in pest management science.

Our approach will also help open up the market for biocontrol by improving our knowledge on how environmental conditions in the field affect biocontrol agent performance, and by pioneering a new approach to improve the effectiveness of biocontrol agents by combining them with host plant resistance. This will have a significant positive effect for the biocontrol industry. This currently represents only 5% of the total crop protection market but it has a compound annual growth rate of 15% (compared to 3% for conventional pesticides) and is estimated to be worth $7 billion by 2022. At the moment, most of the biocontrol industry in Europe is based around protected cropping, but the largest potential market is in field crops. Sales of insecticides in Europe (most of which are used on field crops) are valued at >800M Euros p.a. (European Crop Protection Association statistics). Even if biocontrol agents used in the field obtained just 5% market share this would be worth 40M Euros p.a., and given that biopesticides cost on average 5M Euros to develop this would be a valuable return on investment.

Publications

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Description Aphids are a serious constraint on crop production, and at present the normal way to control them is using regular, high volume applications of synthetic chemical pesticides. However these are harmful for biodiversity, particularly for non-target insects which provide essential ecosystem services. There is an urgent need to develop a better system of pest management in which unsustainable practices are replaced with sustainable, ecological solutions while still enabling high yields and crop quality. The best way to do this is using Integrated Pest Management in which a range of alternative crop protection tools are combined together including biologically-based methods. This project focuses on the peach potato aphid Myzus persicae which is particularly difficult to manage because it has evolved resistance to many types of chemical pesticide. At present, there are few biological IPM tools available for brassica crops. The aim of this project is to provide new information for management of aphid pests in brassica crops using biologically based controls including (i) durable, partial host plant resistance (ii) fungal biopesticides, and (ii) enhanced parasitoid activity.

We evaluated the development of populations of the peach potato aphid Myzus persicae and the cabbage aphid Brevicoryne brassicae on 18 accessions of Brassica oleracea / wild Brassica species selected from a brassica germplasm collection. The accessions were assessed under controlled environment conditions with high replication (30 plants per accession). Aphid population development varied significantly across the accessions, with the most resistant lines producing aphid populations that were about one third the size of the most susceptible. This resistance was associated with reductions in intrinsic rate of increase and mean relative growth rate, as measured under laboratory conditions. A field cage comparison of four contrasting lines (one partially resistant and one susceptible line of each of Brassica oleracea and Brassica napus) showed that resistance to Myzus persicae was also expressed in one B. oleracea line in outdoor conditions.

Analysis of gene expression patterns (RNA seq) in contrasting (susceptible vs partially resistant) B. oleracea lines response to feeding by M. persicae showed that, after 2 and 6 hours of aphid exposure, a greater number of genes were uniquely differentially expressed in the susceptible line, but at 24 hours of aphid exposure this trend was reversed (ie. greater d.e. in the partially resistant line). Analysis of JA levels in plant tissue 24 hours after the start of aphid feeding showed a significant, large (>3 fold) increase in JA concentration in the susceptible line, whereas levels of salicylic acid (SA) were greatly reduced compared to the partially resistant line. These data indicate that the balance of these known defence-related phytohormones underlie the phenotypes observed .

Experiments were done to compare aphid (Myzus persicae) development [intrinsic rate of increase, population doubling time and mean relative growth rate] on two Brassica oleracea accessions previously identified as being either susceptible or resistant. Aphid development experiments were done under standardised environmental conditions. Data indicate that the two B. oleracea accessions have different levels of aphid resistance, significantly impacting aphid development and fecundity. Methodologies to collect feeding data for this aphid species on these two B. oleracea accessions have been refined. Work was then done to compare gene expression patterns in the two contrasting (susceptible vs partially resistant) B. oleracea accessions in response to feeding by M. persicae. The susceptible accession showed a spike in the expression of genes associated with the jasmonic acid (JA) signalling pathway within 2 hours of aphid feeding, which subsided by 6 hours. The partially resistant line also showed increased expression of some components of the JA pathway, but the response was delayed until 6 or 24h after the onset of feeding. Analysis of JA levels in plant tissue using mass spectrometry 24 hours after the start of aphid feeding showed a significant, large (>3 fold) increase in JA concentration in the susceptible line. JA signalling has been shown previously to be activated by aphid feeding in a Myzus-Arabidopsis model system, but our findings suggest that - in brassica crops - elevated JA is associated with a failed plant immune response.

We investigated the effect of a plant defence activator, cis-jasmone (CJ), in Brassica napus, Brassica rapa and Brassica oleracea. Plants were sprayed with cis-jasmone or blank formulation and then tested with Myzus persicae and their parasitoid Diaeretiella rapae. CJ treated plants had significantly lower aphid settlement than control plants. Conversely, D. rapae parasitoids spent a significantly longer time foraging on CJ treated plants. Our results reveal that CJ treatment makes plants less attractive to and less suitable for M. persicae but more attractive to D. rapae in a range of brassica cultivars. These effects are probably due to changes in volatile emission indicating activation of defence and presence of conspecific competitors to aphids but presence of prey to parasitoids. Increases in volatile emission were found in CJ induced plants but varied with genotype.

The susceptibility of adults and nymphs of M. persicae and B. brassicae to 10 strains of entomopathogenic fungi (EPF) from four fungal species was quantified in a laboratory bioassay. While 5 strains caused > 50% mortality of adult aphids within 5 days, most strains show very low virulence against aphid nymphs, however 1 strain caused 80% mortality of nymphs within 3 days. This was associated with a fast germination rate, which probably enables the fungal strain to mount an infection before spores are lost through moulting. When bioassays were done with contrasting lines of Brassica (susceptible vs partially resistant), it was found that EPF that caused low mortality of nymphs of susceptible lines caused high mortality on partially resistant lines, attributable to the aphid development time being slowed down, creating a longer window for infection by the EPF.

A field trial was set up in June 2021 at a SARIC club industry partner's site (Elsoms seeds) to compare natural aphid infestation, population growth and natural enemies on two Brassica napus lines, treated with or without the plant defence activator cis-jasmone (CJ). The B. napus lines (Temple, susceptible industry standard) and Samurai (partially resistant) were grown from seed in insect-proof cages in a glasshouse and planted out at the 4-5 true leaf stage. The CJ was applied four days after transplanting. Weekly assessments were done of numbers and species of aphids, parasitised aphids and parasitoid species and any other aphid natural enemies and pests on 10 plants per plot. Both healthy and parasitised Myzus persicae were recorded from the first assessment one week after planting. A single spray application of cis jasmone was made in early July, but this did not result in significant effects on aphid populations. The reasons for this are unknown, but we hypothesise that this may be because new plant growth post spraying may not have been affected by cis jasmone (which works by causing changes in gene expression in plant tissue to stimulate the production of plant defence systems) - in future use this may require repeat spray applications and / or development of new formulations.
Exploitation Route The next phase of the project is to see how brassica plants with aphid resistance can be used together with fungal biopesticides and parasitoids in an integrated, biological control programme. The aim is to provide (1) breeding material for seed companies, and (2) a new approach for field crop protection that combines natural plant resistance and biocontrol agents, and which will help reduce overreliance on synthetic chemical pesticides.
Sectors Agriculture, Food and Drink

 
Description 24/02/2021 - Vegetable variety - how diversity in our crops keeps food on our plates. Warwick Food Global Research Priorities (GRP) Webinar 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Webinar on the use of vegetable germplasm collections as a foundation for crop breeding and their importance for the development of new, sustainable approaches for crop protection, done through the Warwick Food Global Research Priorities webinar series
Year(s) Of Engagement Activity 2021
URL https://web.microsoftstream.com/video/5ffc26d4-828f-470a-820b-e9cf915ecb50
 
Description Association of Applied Biologists, "Advances in Biocontrol and IPM: challenges and opportunities" webinar (100 people including industry and academics) 25 Feb 2021 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Industry/Business
Results and Impact Presentation on new approaches to pest management for Association of Applied Biologists on line meeting, the audience were a mix of researchers, academics and members of the crop protection industry
Year(s) Of Engagement Activity 2021
 
Description D. Chandler. Outline of project presented as part of plenary talk on biocontrol and IPM for AAB 'Advances in Pesticide Application' meeting 28 - 30 January Brighton UK 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Outline of project presented as part of plenary talk on biocontrol and IPM for AAB 'Advances in Pesticide Application' meeting 28 - 30 January Brighton UK
Year(s) Of Engagement Activity 2020
 
Description D. Chandler. Outline of project presented as part of talk on biopesticides and IPM to AHDB & British Growers Association meeting on advances in agronomy of field legumes, 5 November 2019 eterborough UK. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Industry/Business
Results and Impact Outline of project presented as part of talk on biopesticides and IPM to AHDB & British Growers Association meeting on advances in agronomy of field legumes, 5 November 2019 eterborough UK.
Year(s) Of Engagement Activity 2019
 
Description D. Chandler. Outline of project presented as part of talk on biopesticides and IPM to AHDB 'IPM in field vegetable crops' meeting 5 February 2020 Wellesbourne UK 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Outline of project presented as part of talk on biopesticides and IPM to AHDB 'IPM in field vegetable crops' meeting 5 February 2020 Wellesbourne UK
Year(s) Of Engagement Activity 2020
 
Description D. Chandler. Outline of project presented as part of talk on biopesticides and IPM to AHDB Advances in Agronomy meeting, 11 February 2020 Malvern UK. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Industry/Business
Results and Impact Outline of project presented as part of talk on biopesticides and IPM to AHDB Advances in Agronomy meeting, 11 February 2020 Malvern UK.
Year(s) Of Engagement Activity 2020
 
Description D. Chandler. Outline of project presented as part of talk on biopesticides and IPM to AHDB Advances in Agronomy meeting, 12 February 2020 Newmarket UK. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Industry/Business
Results and Impact Outline of project presented as part of talk on biopesticides and IPM to AHDB Advances in Agronomy meeting, 12 February 2020 Newmarket UK.
Year(s) Of Engagement Activity 2020
 
Description D. Chandler. Outline of project presented as part of talk on biopesticides and IPM to AHDB Field Vegetables Panel, 27 February 2020, Leamington Spa UK. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Outline of project presented as part of talk on biopesticides and IPM to AHDB Field Vegetables Panel, 27 February 2020, Leamington Spa UK.
Year(s) Of Engagement Activity 2020
 
Description D. Chandler. Outline of project presented as part of talk on biopesticides and IPM to Defra VeGIN (vegetable improvement network) meeting, 27 November 2019 Peterborough UK. 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Outline of project presented as part of talk on biopesticides and IPM to Defra VeGIN (vegetable improvement network) meeting, 27 November 2019 Peterborough UK.
Year(s) Of Engagement Activity 2019
 
Description J. Roberts, S. Leather, T. Pope, W. Kirk, T. Bruce, G. Prince, G. Teakle, D. Chandler. 'Slow down - speed up' aphid pest management. Presentation to Association of Applied Biologists meeting Advances in Biocontrol & IPM, 20 - 21 November 2019 Lincolnshire UK 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Presentation to Association of Applied Biologists meeting Advances in Biocontrol & IPM, 20 - 21 November 2019 Lincolnshire UK
Year(s) Of Engagement Activity 2019
 
Description New approaches to IPM for aphid pests in horticultural crops. Presentation for AHDB Aphid Biology & Management webinar 25 November 2020 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Presentation about aphid Integrated Pest Management to 50 growers as part of an AHDB webinar
Year(s) Of Engagement Activity 2020
 
Description presentation 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach International
Primary Audience Professional Practitioners
Results and Impact Joberts, J. et al. Slow down speed up aphid management. International Congress of Entomology, Helsinki 17 - 22 July 2022.
Year(s) Of Engagement Activity 2022
 
Description presentation 
Form Of Engagement Activity A talk or presentation
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Professional Practitioners
Results and Impact Chandler, D. Getting the best out of biopesticides in IPM systems. Presentation to BCPC Pests and Beneficials meeting 'IPM, bringing it together', NIAB Cambridge 25 January 2023
Year(s) Of Engagement Activity 2023