Variations in Soil Microbiome Assembly Determine Hatching Induction of the Carrot Cyst Nematode Heterodera carotae

Plants shape their microbiota through root exudation to resist environmental constraints. These plant's exuded metabolites also serve as hatching signals for cyst nematodes, a major crop pest, to trigger their parasitic cycle. The "suicide hatching" strategy takes advantage of these exudates as a decoy, inducing hatching of juveniles in the absence of the host plant. We questioned here the effect of the soil microbiota on the suicide hatching induction. We used the carrot cyst nematode (Heterodera carotae, Jones) and evaluated the impact of three rotation crops (leek, turnip, and barley) and their associated fungal and bacterial communities on the hatching efficacy of carrot exudates in two types of soil. Our results indicated that hatching induction is lower when leek was previously cultivated. By analysing the covariation between hatching and microbiota composition, we identified fungal ASVs, notably Fusarium equiseti, whose abundances correlate significantly with nematode hatching. We validated that diacetoxyscirpenol, a compound produced by this species, significantly reduces nematode hatching induction. Our results demonstrated that rotation crops modulate the composition of the soil microbiome and can promote the abundance of fungi modulating the suicide hatching success. These results provide insights into plant-microbiota-nematode interactions for optimizing pest biocontrol strategies.