Specialist root herbivore modulates plant transcriptome and downregulates defensive secondary metabolites in a brassicaceous plant.

Plants face attackers aboveground and belowground. Insect root herbivores can lead to severe crop losses, yet the underlying transcriptomic responses have rarely been studied. We studied the dynamics of the transcriptomic response of Brussels sprouts (Brassica oleracea var. gemmifera) primary roots to feeding damage by cabbage root fly larvae (Delia radicum), alone or in combination with aboveground herbivory by cabbage aphids (Brevicoryne brassicae) or diamondback moth caterpillars (Plutella xylostella). This was supplemented with analyses of phytohormones and the main classes of secondary metabolites; aromatic, indole and aliphatic glucosinolates. Root herbivory leads to major transcriptomic rearrangement that is modulated by aboveground feeding caterpillars, but not aphids, through priming soon after root feeding starts. The root herbivore downregulates aliphatic glucosinolates. Knocking out aliphatic glucosinolate biosynthesis with CRISPR-Cas9 results in enhanced performance of the specialist root herbivore, indicating that the herbivore downregulates an effective defence. This study advances our understanding of how plants cope with root herbivory and highlights several novel aspects of insect-plant interactions for future research. Further, our findings may help breeders develop a sustainable solution to a devastating root pest.

Shoot and root insect herbivory change the plant rhizosphere microbiome and affects cabbage-insect interactions through plant-soil feedback.

Plant-soil feedback (PSF) may influence plant-insect interactions. Although plant defense differs between shoot and root tissues, few studies have examined root-feeding insect herbivores in a PSF context. We examined here how plant growth and resistance against root-feeding Delia radicum larvae was influenced by PSF. We conditioned soil with cabbage plants that were infested with herbivores that affect D. radicum through plant-mediated effects: leaf-feeding Plutella xylostella caterpillars and Brevicoryne brassicae aphids, root-feeding D. radicum larvae, and/or added rhizobacterium Pseudomonas simiae WCS417r. We analyzed the rhizosphere microbial community, and in a second set of conspecific plants exposed to conditioned soil, we assessed growth, expression of defense-related genes, and D. radicum performance. The rhizosphere microbiome differed mainly between shoot and root herbivory treatments. Addition of Pseudomonas simiae did not influence rhizosphere microbiome composition. Plant shoot biomass, gene expression, and plant resistance against D. radicum larvae was affected by PSF in a treatment-specific manner. Soil conditioning overall reduced plant shoot biomass, Pseudomonas simiae-amended soil causing the largest growth reduction. In conclusion, shoot and root insect herbivores alter the rhizosphere microbiome differently, with consequences for growth and resistance of plants subsequently exposed to conditioned soil.