Arbuscular mycorrhizal fungal-induced tolerance is determined by fungal identity and pathogen density

Societal Impact Statement Plant-parasitic nematodes are a major concern for global food security, and many existing control options are being phased out due to adverse impacts on the environment. Here, we show that although application of arbuscular mycorrhizal fungi (AMF) increases host tolerance to these parasites, these benefits decrease as the parasite burden increases, limiting long-term benefits. This effect was consistent between experiments in the glasshouse and in the field environment, demonstrating the relevance of research into usable technologies. Our findings have potential to aid decision making regarding application of AMF inocula for optimum results in agricultural systems. Plant-parasitic nematodes are a leading global threat to crop production and food security aims. Control strategies based on nematicides and fertilisers are increasingly undesirable due to economic and environmental impacts. Arbuscular mycorrhizal fungi (AMF) may induce host tolerance against pests such as the potato cyst nematode (PCN). Here, we determined the impact of PCN density on the tolerance induced by AMF-host interactions. Additionally, we evaluated the effects of five AMF inocula on PCN fitness though glasshouse and field trials. Greater PCN densities reduce the increased tolerance that AMF may confer on their hosts. This may be due to reduced mycorrhizal colonisation of hosts under higher PCN infection and potentially a threshold at which the presence of PCN severely impacts fungal growth. When tested in the field, the outcomes of AMF inoculation on crop yields were still positive. Inoculation of soil in the field also increased PCN multiplication, suggesting that AMF-induced tolerance may become reduced in the near future when the threshold PCN density is reached. Addition of AMF to agricultural soils may provide a short-term benefit yet lead to a long-term detriment by increasing PCN populations. The effects observed were driven by only one out of the five introduced AMF species, indicating that the remaining species were redundant for this application. This raises important considerations for future application of AMF inocula in agricultural systems and aids our understanding of how widely used 'beneficial' soil amendments impact the agricultural ecosystem.