Divergent rearrangements of rhizosphere microbiomes to aboveground herbivory in Fibrous and Taproot Plants

Abstract

Aboveground insect herbivory can modify underground ecological processes, root dynamics, and the corresponding rhizosphere microbial communities. Although many studies have addressed rhizosphere microbial responses to herbivory, differences between plant families with contrasting root architectures and root exudates remain poorly understood. Here, we investigated how herbivory influences rhizosphere microbes in Asteraceae (fibrous-rooted plants) and Solanaceae (taproot plants) under mechanical damage and Spodoptera litura feeding treatments. We analyzed the relationships among root morphological traits, rhizosphere microbial communities, and root exudates. Our results demonstrated that root morphological traits determined divergent microbial responses between the two families. At 3 and 6 days of treatment, microbial diversity, community composition, and network complexity showed contrasting patterns: they declined with increasing herbivory intensity in Asteraceae, but increased in Solanaceae. Regulatory strategies were family-specific: Asteraceae responded mainly via root traits such as specific root length, whereas Solanaceae depended on combined shifts in root morphology and quercetin exudation. Quercetin displayed distinct spatiotemporal dynamics: it returned to control levels by day 6 in Asteraceae, but remained suppressed in Solanaceae under moderate-to-high herbivory. Our study enhances the understanding of aboveground-belowground interactions and provides a mechanistic basis for predicting herbivory impacts on rhizosphere communities across plant functional groups through root traits and root exudates.