Hijacking plant immunity: winners and losers in dual pest and pathogen attacks on a shared host

Abstracts are not currently available in GtR for all funded research. This is normally because the abstract was not required at the time of proposal submission, but may be because it included sensitive information such as personal details.

It is important to understand how host defences are modulated by prior attack by other species because plants, in the field, are exposed to multiple attacking organisms. Our data show that Sitobion avenae and Fusarium graminearium profoundly affect each other by altering the condition of their shared host plant, wheat. Fusarium head blight disease severity doubles on aphid infested plants but diseased plants are poorer hosts for aphids. Our goal is to determine the mechanisms underpinning this host manipulation by the aphid or pathogen. We will use a multi-omics approach to define the changes in the host transcriptome and metabolome to identify modulated defence. To isolate local and systemically induced defence suppression we will perform experiments with distal and local aphid feeding on the host and explore the effect of duration of exposure to attackers. To separate the effect of aphid saliva and honeydew we will use bioassays with artificially collected saliva/honeydew to quantify effects on pathogen growth. Conversely, we will determine the effect of secondary fungal metabolites (deoxinivalenol (DON) and nivalenol (NIV)), host metabolites and volatiles on aphid behaviour and performance. Studies will be facilitated by available DON/ NIV producers and Tri5 knockout-transformant strains unable to produce the mycotoxins. Chemical ecology studies will use electrophysiological recordings from aphid antennae to identify bioactive disease induced volatiles and olfactometer bioassays to measure aphid behavioural responses. Transcriptomic and metabolomic analyses will define changes in the functional pathways of both the host plant and the aphid, including putative DON and NIV detoxification mechanisms in aphids. The project will thus determine how the presence of another attacking organism alter host defence and change the fitness of the interacting organisms. It will identify the consequences of aphid-pathogen interactions for disease and pest infestation in wheat.

The project will primarily benefit the R&D community seeking to develop novel approaches to crop protection and the farming industry, who face the reality of multiple attacking organisms in their crops. These parties will benefit from a better understanding of wheat plant responses to aphids and Fusarium head blight (FHB) disease. To give an indication of the scale of the challenge, economic losses from FHB in the USA in wheat and barley are £563 million over two years with secondary economic losses of £1.16 billion [1]. Fungicides are applied to 99% of conventionally produced wheat crops in the UK and receive an average of 3 sprays per season. Sustainable disease control via improved disease resistance would save the industry £2.1million per annum in recovered loss and spray costs.

The project will have added value as it will not only provide new information about plant-aphid interactions, particularly how aphids suppress plant defence, but also add to knowledge of plant-pathogen interactions and our understanding of how crops respond to dual attack. Information about plant responses to attack will be of value to industrial plant pathologists, entomologists and crop breeders working in the area of crop protection. Outputs from the project will inform future crop varietal selection for improved resilience against multiple enemies. It will also inform the identification of new bioactive compounds for insect control.

Specifically, the crop protection and farming industries are anticipated to benefit through provision of:

- New transcriptomic and metabolomic resources for wheat interaction with a serious pest (grain aphid) and pathogen (Fusarium graminearum)
- New targets for breeding for aphid and disease resistance in wheat
- New molecules with repellent and/or antibiotic activity against aphids
- Information for agronomists about the increased disease and mycotoxin risk to wheat in the presence of aphids
- New knowledge to support collaborative projects to exploit the research findings

FHB is of huge significance due to the health threat posed by the mycotoxins produced by the fungal pathogen. The food industry must minimise the risk of mycotoxins in foods, through good practice undertaken during growing, harvesting and storage. This project will provide insights into factors increasing mycotoxin risk and information will benefit the food and feed industry seeking to minimise risk. It will also be benefit health professionals and the wider public, by making a contribution to sustainable, safe food supply chains.

Development of sustainable crop protection is crucial for attaining sustainable intensification of agriculture (2) and pressures from pests and diseases are expected to increase with climate change (3). Cereal crop production is constrained by plant pests and diseases, which reduce the yield and quality of harvested grain. They are becoming more difficult for farmers to manage because availability of pesticides is decreasing due to the evolution of pesticide resistance and changes in the law that ban pesticides, for example, neonics.

(1) Nganje and Johnson (2003) J. Can. Ag. Econ. Soc. 4:16-26
(2) Pretty et al. (2018) Nature Sustainability 1: 441-446
(3) Bebber et al. (2018) Nature Climate Change 3: 985-988