Costunolide Influences Germ Tube Orientation in Sunflower Broomrape – A First Step Toward Understanding Chemotropism

Abstract

Orobanche cumana WALLR. is a host-specific root parasite of cultivated sunflowers with increasing economic importance in Europe, North Africa, and parts of Asia. While sesquiterpene lactones (STLs) released from sunflower roots were identified as natural germination stimulants of O. cumana seeds in the soil, the chemical nature of the signals guiding the emerging germ tube toward the host root has remained unknown hitherto. Thus, we designed a bioassay that allowed the observation of broomrape germination and subsequent germ tube development in the presence of substances with putative chemotropic activity. Root exudates and sunflower oil extracts, both containing STLs in micromolar concentrations, caused the positive chemotropic orientation of germ tubes. A similar positive chemotropic effect was achieved with costunolide, one of the four STLs of sunflower present in the exudate and oil extracts. In contrast, GR24, a synthetic strigolactone (SL) with germination-inducing activity on O. cumana seeds, showed no effect on the germ tube orientation. The effect of costunolide was concentration-dependent and within the range of its natural micromolar occurrence in roots. We assume that an STL gradient is responsible for the stronger inhibition of elongation growth on the host-facing flank of the germ tube compared with the far side flank. This would confer a double role of STLs from sunflower root exudates in the sunflower–broomrape interaction, namely, as germination stimulants and as chemotropic signals.

Dynamics of germination stimulants dehydrocostus lactone and costunolide in the root exudates and extracts of sunflower

“… 28 , 29 It mainly plays a role in the early induction of O. cumana seed germination and gemtube. 26 Moreover, DCL and CL were found increasing with developmental stage, which indicates that these compounds might have other physiological activities.…”

“…Among germination stimulants isolated from sunflower, DCL and CL were considered as germination and gemtube inducer on O. cumana . 25 , 26 Since DCL and CL exudation are linked in germination and gemtube of O. cumana , we focused on these two compounds in different sunflower cultivars and the dynamic with the growth stages of sunflower. Based on our results, both DCL and CL were detected in both root exudates and extracts of these two sunflower cultivars.…”

“… 23 The STLs present in leaves, stems, oil extracts, cotyledons, hypocotyls, roots, and seedling of sunflower 24 , 25 act as germination stimulants and signal for chemotropic signals of the parasite’s germtube. 25 , 26 …”

Strigolactones are chemoattractants for host tropism in Orobanchaceae parasitic plants

“…Intriguingly, the germ tube of Orobanche cumana , a holoparasite, is guided by costunolide, a sunflower-derived sesquiterpene lactone, but not by GR24, a synthetic SL analogue 49 . In comparison, O. cumana germination is stimulated by costunolide and GR24 27, 49 . Therefore, it is likely that the nature of chemoattractants is different among phylogenetic clades 2 , in contrast with the commonality of using SLs as germination stimulants in obligate parasites.…”

“…2), this chemotropism phenotype may have been acquired during parasite evolution. Intriguingly, the germ tube of Orobanche cumana , a holoparasite, is guided by costunolide, a sunflower-derived sesquiterpene lactone, but not by GR24, a synthetic SL analogue 49 . In comparison, O. cumana germination is stimulated by costunolide and GR24 27, 49 .…”