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.

Automated summary

Plants face both aboveground and belowground attackers, and the response of Brussels sprouts' primary roots to root herbivory by cabbage root fly larvae was studied, along with aboveground herbivory by cabbage aphids or diamondback moth caterpillars. The study found that root herbivory leads to major transcriptomic rearrangement, modulated by aboveground feeding caterpillars. Knocking out aliphatic glucosinolate biosynthesis enhanced the performance of the specialist root herbivore, suggesting a downregulation of an effective defense by the herbivore. These findings contribute to understanding how plants cope with root herbivory and may aid in developing sustainable solutions for controlling devastating root pests.