Mycorrhizal fungi enhance nutrient uptake but disarm defences in plant roots, promoting plant-parasitic nematode populations

Arbuscular mycorrhizal (AM) fungi are ubiquitous components of the soil biota which live symbiotically with terrestrial plants. Plant-parasitic nematodes are an important group of soil-dwelling invertebrates that inflict considerable damage to crops, representing a serious threat to food security. The effects of the AM symbiosis on plant-parasitic nematodes can be variable, and the mechanisms driving such variability remain ambiguous. We tested the impacts of inoculation with AM fungi on the root metabolic profile and nutritional chemistry of two varieties of wheat (Triticum aestivum), and how this affected populations of the plant-parasitic nematode Pratylenchus neglectus. AM fungi reduced plant biomass by almost 24%, yet increased root concentrations of phosphorus, potassium and zinc by 50%, 15% and 16%, respectively. Contrary to our predictions, nematode populations were 47–117% higher on AM inoculated plants, depending on variety. Untargeted metabolomic profiling revealed significant effects of mycorrhizal colonisation on certain markers of biological interest, these compounds were the benzoxazinoid glucoside defence compounds DIBOA-Glc, HMBOA-Glc and HDMBOA-Glc. Overall, mycorrhizae reduced abundances of these defence metabolites, which were potentially driving AM fungi – nematode interactions; although for DIBOA-Glc this was dependent on wheat variety. Moreover, there was a negative correlation between total AM colonisation and DIBOA-Glc concentrations. Our results demonstrate AM fungi can reduce plant biomass and supress root defence compounds associated with plant resistance to invertebrate pests, while still providing nutritional benefit to the host plant. This highlights that mycorrhizal colonisation of wheat varieties can have simultaneous positive and negative effects on different plant traits which drive plant-herbivore interactions. In working towards effective exploitation of the AM symbiosis in sustainable plant production, the context dependent outcomes of mycorrhizal-plant-nematode interactions is a key challenge. Untargeted metabolomic profiling offers the ability to reveal some of the driving mechanisms underpinning such complex tripartite interactions in the soil.