The heterotrophic lifestyle of parasitic plants relies on the development of the haustorium, a specific infectious organ required for attachment to host roots. While haustorium development is initiated upon chemodetection of host-derived molecules in hemiparasitic plants, the induction of haustorium formation remains largely unknown in holoparasitic species such as Phelipanche ramosa. This work demonstrates that the root exudates of the host plant Brassica napus contain allelochemicals displaying haustorium-inducing activity on P. ramosa germinating seeds, which increases the parasite aggressiveness. A de novo assembled transcriptome and microarray approach with P. ramosa during early haustorium formation upon treatment with B. napus root exudates allowed the identification of differentially expressed genes involved in hormone signaling. Bioassays using exogenous cytokinins and the specific cytokinin receptor inhibitor PI-55 showed that cytokinins induced haustorium formation and increased parasite aggressiveness. Root exudates triggered the expression of cytokinin-responsive genes during early haustorium development in germinated seeds, and bio-guided UPLC-ESI(+)-/MS/MS analysis showed that these exudates contain a cytokinin with dihydrozeatin characteristics. These results suggest that cytokinins constitutively exudated from host roots play a major role in haustorium formation and aggressiveness in P. ramosa.

Department of Chemical Biology and Genetics Centre of the Region Haná for Biotechnological and Agricultural Research Faculty of Science Palacký University Olomouc CZ 78371 Czech Republic

IRHS UMR1345 INRA AGROCAMPUS Ouest Université d'Angers SFR 4207 QUASAV 42 rue Georges Morel 49071 Beaucouzé cedex France

ONIRIS USC 2013 LABERCA Atlanpole La Chantrerie BP 50707 44307 Nantes France

Plateau Technique Mutualisé ANAN SFR 4207 QUASAV 42 rue Georges Morel 49071 Beaucouzé France

Université de Nantes Laboratoire de Biologie et Pathologie Végétales EA 1157 SFR 4207 QUASAV UFR Sciences et Techniques 44322 Nantes France

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