Growth substrates alter aboveground plant microbial and metabolic properties thereby influencing insect herbivore performance

The gut microbiome of plant-eaters is affected by the food they eat, but it is currently unclear how the plant metabolome and microbiome are influenced by the substrate the plant grows in and how this subsequently impacts the feeding behavior and gut microbiomes of insect herbivores. Here, we use Plutella xylostella caterpillars and show that the larvae prefer leaves of cabbage plants growing in a vermiculite substrate to those from plants growing in conventional soil systems. From a plant metabolomics analysis, we identified 20 plant metabolites that were related to caterpillar feeding performance. In a bioassay, the effects of these plant metabolites on insects' feeding were tested. Nitrate and compounds enriched with leaves of soilless cultivation promoted the feeding of insects, while compounds enriched with leaves of plants growing in natural soil decreased feeding. Several microbial groups (e.g., Sporolactobacillus, Haliangium) detected inside the plant correlated with caterpillar feeding performance and other microbial groups, such as Ramlibacter and Methylophilus, correlated with the gut microbiome. Our results highlight the role of growth substrates on the food metabolome and microbiome and on the feeding performance and the gut microbiome of plant feeders. It illustrates how belowground factors can influence the aboveground properties of plant-animal systems, which has important implications for plant growth and pest control.