Abstract
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.
Highlights
Some terrestrial plant species have developed unique features in the course of evolution, leading them to adopt a heterotrophic lifestyle
The results showed that fraction 16 (27–28 min) co-eluted with isorhamnetin which had no haustorium induction activity on P. ramosa (Supplementary Tables S4A, S5B), and interestingly fraction 9 co-eluted with different CK standards displaying early haustorial structures (EHSs) induction, including c/tZ, tZ, tZR, tZ riboside-O-glucoside (tZROG), DHZ, DHZ riboside (DHZR), and DHZ riboside-O-glucoside (DHZROG) (Supplementary Table S5A; Fig. 5A, B)
We demonstrated that radicles of P. ramosa germinated seeds treated with uninfected B. napus root exudates displayed a growth arrest, a swollen apex, and epidermal cell outgrowth corresponding to EHS development previously described in either hemiparasitic or holoparasitic plants (Baird and Riopel, 1983; Joel and Losner-Goshen, 1994; Bandaranayake and Yoder, 2013; Cui et al, 2016)
Summary
Some terrestrial plant species have developed unique features in the course of evolution, leading them to adopt a heterotrophic lifestyle. In achlorophyllous species (holoparasites) such as Orobanche cumana and Phelipanche aegyptiaca, the early haustorium development is revealed by a swelling of the root tip, caused by the extension of the apical cells and a polar outgrowth of epidermal cells, but it gives rise to short cell extensions termed papillae (Joel and Losner-Goshen, 1994; Fernández-Aparicio et al, 2016) Both haustorial hairs and papillae produce adhesive molecules meant to anchor the haustorium to the host root (Baird and Riopel, 1985; Joel and Losner-Goshen, 1994)
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