Above and Belowground Microbes Are Associated with Variation of the Leaf Metabolome, but Herbivory Has Nominal Effects

Plant-associated microbes affect the functioning of their host. However, holistic studies that consider interactions between plants and microbes both above and belowground are lacking. We hypothesise that soil is a reservoir for both root and leaf microbes, and that herbivory disrupts the composition of the leaf microbial community. We further hypothesise that the root-associated microbial communities correlate with the leaf metabolome (as a measure of function), suggesting a linkage between the root microbes and the leaf phenotype. To test these hypotheses, the microbial communities of herbivore-damaged and undamaged leaves, roots and the surrounding soil were characterised from 15 Plantago major populations sampled across Denmark. Microbial communities were then compared against the leaf metabolome. Initially, we found herbivory had no effect on the leaf microbiome or the metabolome. We did find that the fungal communities showed significant overlap between leaf, root and soil samples, but the bacteria were mainly specialised to each sample type. Interestingly, the leaf microbiome correlated with the leaf metabolome, but the root bacteria and fungi did not. However, additional analyses of arbuscular mycorrhizal fungi found these specialist root microbes were associated with variation in the leaf metabolome. This study demonstrates the complexity of plant metabolome-microbiome interactions, and the need to fully integrate the microbiome of different tissue types to fully understand plant-microbe interactions.