Belowground plant responses to root herbivory depend on the composition and structure of their root-colonising arbuscular mycorrhizal fungi

Abstract

ABSTRACTThere is growing interest in managing arbuscular mycorrhizal (AM) fungi in agriculture to support plant production. These fungi can support crop growth and nutrient uptake but also affect plant-herbivore interactions. Our knowledge of how native AM fungal diversity and community composition influence these interactions is limited, while our understanding of this in relation to root-herbivory is lacking altogether.To begin to address these knowledge gaps, plants were grown with no AM fungi or were inoculated with native fungal communities sourced from either a crop field (field community), a sclerophyll forest (forest community), or a crop field in fallow (fallow community). We then explored how the composition and structure (species richness and relative abundance) of root-colonising AM fungal communities was associated with the growth and belowground nutrient responses of a major crop (Sorghum bicolor) to attack from a root-feeding insect (Dermolepida albohirtum).DNA metabarcoding revealed plants associated with three distinct root-colonising AM fungal communities. Fungal taxon richness in roots was highest in the field community and lowest in the fallow community. Both the field and fallow communities were dominated by the putatively ruderal genera Glomus and Claroideoglomus, while the forest-derived community contained greater proportions of Paraglomus and Ambispora.In response to root herbivory, plants without AM fungi and plants colonised by the forest community exhibited root biomass losses of 61% and 44%, respectively. Similarly, these two groups also had reductions of 59% and 65% in their root phosphorus content, respectively, when subjected to the root herbivore. In contrast, plants associating with communities harbouring greater proportions of Glomus and Claroideoglomus (the field and fallow communities) did not exhibit reductions in root biomass or nutrient content.Our results show that plant responses to root-herbivory vary with root-colonising AM fungal community composition and structure. In a community context, our findings suggest that stronger associations with the genera Claroideoglomus and Glomus may potentially support crop tolerance-associated responses belowground. There is an urgent need for more exploration of how natural assemblages of AM fungi differentially mediate plant-herbivore interactions if we are to effectively manage soil fungi in sustainable agricultural systems.