Root-knot nematode Meloidogyne incognita uses secondary-metabolite-mediated soil microbiome shifts to locate host plants.

Plant-parasitic nematodes are among the most destructive soil-dwelling pests, posing severe threats to global agriculture. However, the interplay between plant metabolites, rhizosphere microorganisms and their potential role in guiding pathogenic nematodes to their hosts remains poorly understood. Here we explored this gap by investigating the role of benzoxazinoids (BXs), a class of defensive metabolites of maize plants, in influencing the host-seeking behaviour of root-knot nematodes (RKNs). Our findings revealed that, surprisingly, BXs secreted by maize roots, particularly 6-methoxy-benzoxazolin-2-one, not only enhance RKN infection but also serve as powerful attractants. Remarkably, BX effects were observed only in the presence of a soil matrix. Further analysis demonstrated that 6-methoxy-benzoxazolin-2-one modulates the abundance and composition of rhizosphere bacteria, which in turn play a crucial role in RKN attraction and infection. We discovered that rhizosphere bacteria of BX-producing plants emit volatile compounds such as methyl ketones and 2-phenylethanol, which are then used by RKNs to locate host plants. RKNs detect these volatiles through chemosensory genes, including Mi-odr-1, Mi-odr-7 and Mi-gpa-6. Our study provides mechanistic insights into how RKNs use secondary-metabolite-shaped plant-microbe interactions to enhance their host-seeking behaviour and maximize their performance.