Cultivation substrates alter plant metabolic profiles with concomitant impacts on herbivore performance.

INTRODUCTION: Herbivore microbiomes are strongly influenced by host plant quality and diet composition. However, it remains unclear how different cultivation substrates modulate the plant metabolome and how these shifts subsequently influence the performance and microbiome of aboveground herbivores. METHODS: We utilized common beans cultivated in soil and hydroponic systems to investigate the multi-trophic interactions involving the substrate microbiome, plant metabolome and the polyphagous spider mite Tetranychus pueraricola. RESULTS: Our results showed that while T. pueraricola exhibited an increased oviposition on hydroponic leaves, they achieved markedly higher biomass when reared on soil-grown common beans. The beta diversity of the mite microbiome differed markedly between two systems and showed close associations with substrate microbial composition. Metabolomic profiling revealed significant enrichment in isoflavonoid biosynthesis and carbon metabolism pathways between hydroponic and soil-grown leaves. Specifically, the upregulation of key secondary metabolites in hydroponic leaves correlated with suppressed mite weight. Comprehensive correlation analyses further indicated that cultivation substrate affected multi-scale associations among substrate microbiome and leaf metabolome and mite microbiome. DISCUSSION: Our results demonstrate that growth substrates potentially contribute to divergence in herbivore microbiome and performance, as well as plant metabolism. These findings highlight the significant influence of cultivation substrate on aboveground plant-herbivore interactions, providing new insights for optimizing crop management and ecological pest control.