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

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Plants cannot run away when an attacker comes to attack them. Being unable to flee means that they are under pressure to resist attackers... they do this by switching on defences such as the production of antibiotic plant chemicals. Meanwhile, the attackers have adapted to supress plant defence responses to colonise their host. An interesting and important question is, "what happens when plants are exposed to more than one attacker?" Here we consider the case of wheat, a globally important crop for global food security, and two of its key attackers: aphids (greenfly) and Fusarium head blight (FHB) disease. FHB is a major disease of wheat caused by Fusarium graminearium, an aggressive fungal pathogen. The disease also produces toxins (called mycotoxins), deoxynivalenol (DON) and nivalenol (NIV), in the grain, which are harmful to humans and animals when consumed. 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 control because availability of pesticides is going down due to the evolution of pesticide resistance and changes in the law that ban pesticides, for example, neonics. Most previous studies of plant diseases and pests have considered them in isolation and little is known of the interactions between them. Aphids occur in cereal fields at the same time as FHB and interact with the disease and the wheat host plant. Our project will discover how wheat plants respond to these attackers, not only on their own but also when exposed to dual attack. Our early findings show that FHB disease infection is doubled on plants with aphids when compared to clean plants. Here we will determine how and why this happens. We will investigate the biochemical and molecular basis of this aphid-induced plant defence suppression. We will conduct gene expression analyses of the wheat host and the aphid and will analyse differences in biochemical production. We will define and characterise the modulated host-defence networks in our biological experiments and determine their biological significance. Insects are influenced by the odours that plants release: a diseased plant smells different from a healthy one and may become repellent. We will collect plant odours, identify their chemical structures and expose aphids to them to test how they respond. We will make electrical recordings from insect antennae to determine which chemicals they can smell and do behaviour tests to see if they are attracted or repelled. Finally, the project will carry out experiments to determine if the aphids are able to metabolise the toxins produced by the FHB disease. The results from changes in the gene expression and metabolism of the aphid exposed to the mycotoxins will identify new detoxification pathways in the insect relevant to future targets for insect control. Our project will allow us to define novel molecular and metabolomic targets for making our crops more resilient to the aphid pest and the pathogen causing FHB disease in wheat.The research will advance scientific understanding of how plants respond to combined attack from a pest and a disease. The information this project will provide is essential because we do not know how the aphids change the host to increase its susceptibility to FHB in wheat. This is a novel approach because most previous studies have overlooked how attackers sharing a host plant influence each other by manipulating the host. Outcomes of our work will create future opportunities to improve crop resilience to these attacking organisms.