Germination Stimulants of Phelipanche ramosa in the Rhizosphere of Brassica napus Are Derived from the Glucosinolate Pathway

Abstract

Phelipanche ramosa is a major parasitic weed of Brassica napus. The first step in a host-parasitic plant interaction is stimulation of parasite seed germination by compounds released from host roots. However, germination stimulants produced by B. napus have not been identified yet. In this study, we characterized the germination stimulants that accumulate in B. napus roots and are released into the rhizosphere. Eight glucosinolate-breakdown products were identified and quantified in B. napus roots by gas chromatography-mass spectrometry. Two (3-phenylpropanenitrile and 2-phenylethyl isothiocyanate [2-PEITC]) were identified in the B. napus rhizosphere. Among glucosinolate-breakdown products, P. ramosa germination was strongly and specifically triggered by isothiocyanates, indicating that 2-PEITC, in particular, plays a key role in the B. napus-P. ramosa interaction. Known strigolactones were not detected by ultraperformance liquid chromatography-tandem mass spectrometry, and seed of Phelipanche and Orobanche spp. that respond to strigolactones but not to isothiocyanates did not germinate in the rhizosphere of B. napus. Furthermore, both wild-type and strigolactone biosynthesis mutants of Arabidopsis thaliana Atccd7 and Atccd8 induced similar levels of P. ramosa seed germination, suggesting that compounds other than strigolactone function as germination stimulants for P. ramosa in other Brassicaceae spp. Our results open perspectives on the high adaptation potential of root-parasitic plants under host-driven selection pressures.

Response of wild and weedy broomrapes to synthetic strigolactone analogue GR24

“…The importance of other compounds for germination of broomrapes was also demonstrated for weedy P. ramosa and its host Brassica napus. In the rhizosphere of non-mycotrophic B. napus were identified isothiocyanates, which are breakdown products of glucosinolates, to be the main germination stimulants for P. ramosa present in B. napus (Auger, et al, 2012). The authors did not detect any known strigolacone by ultraperformance liquid chromatography-tandem mass spectrometry in the rhizosphere.…”

“…Several chemical compounds were identified as a germination inducing compounds. They include dihydrosorgoleone, the strigolactones, the sesquiterpene lactones (Bouwmeester, et al, 2003), dehydrocostus lactone (Joel, et al, 2011), peagol, peagoldione (Evidente, et al, 2009) and glucosinolate-breakdown products (Auger, et al 2012). The most studied compounds are host-derived strigolactones (SLs).…”

Profiling of secondary metabolites in root exudates of Arabidopsis thaliana

“…They play a pivotal role in the mobilization and acquisition of nutrients (Ma et al, 2001;Schmid et al, 2014), attract and repel certain microbe species (Rudrappa et al, 2008), inhibit the growth of competing plant species (Biedrzycki et al, 2010) or stimulate the germination of parasite seeds (Auger et al, 2012). Certainly, their qualitative and quantitative composition depends on the plant species, the developmental stage (Aulakh et al, 2001;Chaparro et al, 2013) as well as abiotic and biotic factors (Bouwmeester et al, 2007).…”

Knowing the Parasite: Biology and Genetics of Orobanche

“…Although most of the GSs identified so far belong to the SL family and correspond to butenolides signaling molecules, other molecules have also been identified such as sesquiterpene lactones, polyphenols, and isothiocyanates involved in the germination of O. cumana (Raupp & Spring, 2013), O. foetida (Evidente et al, 2010), and P. ramosa (Auger et al, 2012), respectively. In contrast, although the key role of SLs as GSs has been known for several decades, almost nothing is known about the early molecular events governing the germination of root parasitic plants in response to SLs, nor about how SLs interact with parasitic phytohormones during this process.…”