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Plant-parasitic nematodes are among the most harmful pests of cultivated crops causing important economic losses. The ban of chemical nematicides requires the development of alternative agroecological approaches to protect crops against nematodes. For cyst nematodes, egg hatching is stimulated by host plant root exudates. Inducing “suicide hatching” of nematode second-stage juveniles (J2), using root exudates in the absence of the host plant, may constitute an effective and innovative biocontrol method to control cyst nematodes. However, before considering the development of this approach, understanding the effect of soil biotic component on cyst nematode hatching by root exudates is a major issue. The effectiveness of this approach could be modulated by other soil organisms consuming root exudates for growth as soil microbiota, and this must be evaluated. To do that, four different native agricultural soils were selected based on their physicochemical properties and their microbiota composition were characterized by rDNA metabarcoding. To disentangle the effect of microbiota from that of soil on hatching, four recolonized artificial soils were obtained by inoculating a common sterile soil matrix with the microbiota proceeding from each agricultural soil. Each soil was then inoculated with cysts of the potato cyst nematode, Globodera pallida , and low or high doses of potato root exudates (PREs) were applied. After 40 days, viable J2 remaining in cysts were counted to determine the efficiency of root exudates to stimulate hatching in different soils. Results showed that (i) when physicochemical and microbiota compositions varied among native soils, the hatching rates remained very high albeit small differences were measured and no dose effect was detected and (ii) when only microbiota composition varied among recolonized soils, the hatching rates were also high at the highest dose of PREs, but a strong dose effect was highlighted. This study shows that abiotic and biotic factors may not compromise the development of methods based on suicide hatching of cyst nematodes, using root exudates, molecules inducing J2 hatch, or trap crops.

Background In western France, rapeseed farmers face significant yield losses due to root parasitism caused by Phelipanche ramosa, a holoparasite plant of the Orobanchaceae family. Recently, a reduction of parasitic plant development has been observed in fields with history of severe infestation. In a same given pedoclimatic environment, this so-called soil-suppression of parasitism might presumably result from microbial mechanisms targeting P. ramosa. We tested this hypothesis on two soils from neighboring rapeseed fields, with similar physicochemical properties but contrasted parasitism, characterized as suppressive and conducive. We assessed these soils in a hydroponic co-cultivation system of P. ramosa and B. napus, and simultaneously sampled rhizosphere exudates weekly, as well as rhizosphere and rapeseed roots at three time points along parasite development. Comparisons were thus drawn between conducive and suppressive soils, both in untreated or gamma-sterilized conditions, regarding the effects of soil derived signaling metabolites on broomrape key early parasitic stages (i.e. germination and pre-haustorium development), late parasite development as well as soil bacterial and fungal structures. Results We demonstrate that the suppressive soil mitigates broomrape parasitism by reducing both parasite attachments and development, while causing tubercle necrosis. Activity assays on initial soils as well as co-cultivation rhizosphere exudates reveal that pre-attachment stages of broomrape are not affected by suppression. Root exudates, either they were collected from plants cultivated on suppressive or conducive soils, exerted similar contribution on the induction of broomrape seed germination and on haustoria formation. Thus, attachment and post-attachment stages are more likely to be suppressed by soil microbiota. Given the observed dissimilarities in microbial composition between the soils, we suggest that rather than bacteria, fungi play a greater part in parasitism suppression. Because suppression is not correlated with fungal diversity during co-cultivation, we suspect that in addition to general microbial interactions, specific groups of fungi participate in parasitism reduction. Further correlation network analyses (WGCNA) propose that three clusters of ASVs are indeed correlated with suppressive parasitic traits by their abundance. In these clusters, 7 ASVs are inversely correlated with parasitic attachment and one is positively correlated with the occurrence of necrotic tubercles, while being more abundant in the suppressive soil (DEseq2). These 7 ASVs are from Nectriaceae, Niessliaceae, Bartaliniaceae, Holtermanniaceae families as well as from Helotiales and Pleosporales orders, while the last ASV is identified as a Berkeleyomyces sp., a necrotrophic fungal genus known as a causal agent of black root rot. Conclusion This study explains the observed contrasted parasite development on two physiochemically similar soils by linking parasitic infestation to fungal dynamics in the rhizosphere. This finding extends our knowledge of disease suppressive soils to plant parasitism and proposes biological leads for potential biocontrol of broomrape.