Role of Strigolactones in the Host Specificity of Broomrapes and Witchweeds

Abstract

Root parasitic plants of the Orobanchaceae, broomrapes and witchweeds, pose a severe problem to agriculture in Europe, Asia and especially Africa. These parasites are totally dependent on their host for survival, and therefore, their germination is tightly regulated by host presence. Indeed, their seeds remain dormant in the soil until a host root is detected through compounds called germination stimulants. Strigolactones (SLs) are the most important class of germination stimulants. They play an important role in planta as a phytohormone and, upon exudation from the root, function in the recruitment of symbiotic arbuscular mycorrhizal fungi. Plants exude mixtures of various different SLs, possibly to evade detection by these parasites and still recruit symbionts. Vice versa, parasitic plants must only respond to the SL composition that is exuded by their host, or else risk germination in the presence of non-hosts. Therefore, parasitic plants have evolved an entire clade of SL receptors, called HTL/KAI2s, to perceive the SL cues. It has been demonstrated that these receptors each have a distinct sensitivity and specificity to the different known SLs, which possibly allows them to recognize the SL-blend characteristic of their host. In this review, we will discuss the molecular basis of SL sensitivity and specificity in these parasitic plants through HTL/KAI2s and review the evidence that these receptors contribute to host specificity of parasitic plants.

Keywords: Broomrapes; HTL/KAI2; Host specificity; Receptor-ligand specificity; Strigolactones; Witchweeds.

Fig. 1

Chemical structures of SLs commonly used in experiments. GR24 is a commonly used synthetic SL that is usually supplied as a racemate of two optical isomers: rac-GR24, which consists of equal amounts of GR24^5DS and GR24^ent−5DS (see the box). Other GR24 analogs exist, GR24^4DO and GR24^ent−4DO, but are usually discarded during production. ABCD-rings are marked on GR24^5DS, and 2ʹR and 2ʹS configurations of the D-ring are marked on the two stereoisomers in rac-GR24. Strigol, Orobanchol, 5DS and 4DO are naturally occurring SLs that have been used in several studies. These can be divided into strigol- and orobanchol-type SLs, depending on the stereochemical configuration of the junction between the B- and C-rings. Importantly, all natural SLs have 2ʹR-configured D-rings, whereas rac-GR24 consists of both naturally and unnaturally configured GR24. Structures were drawn using the program ChemDraw.

Fig. 2

Hypothetical mechanisms of parasitic plant seed germination in response to SLs. Parasitic plants of the Orobanchaceae germinate in response to host-exuded SLs, which are detected using a diverse clade of HTL/KAI2 receptors. It is essential that parasites only respond to the signals corresponding with their host; therefore, signal integration is an important part of host detection. Shown are different models by which HTL/KAI2 paralogs may transduce signals upon binding SL, by interacting with MAX2 and degrading (presumably) SMXLs. Each panel represents a plausible way in which a given HTL/KAI2 could interact with its partners. (A) Positive regulation by degradation of a germination-inhibiting regulator. (B) Negative regulation by degradation of a germination-inducing regulator. (C) Negative regulation by sequestration of a signaling partner, as postulated by Nelson (2021). Certain modifications of HTL/KAI2 may prevent the interaction with either SMXL (as shown here) or MAX2, thereby sequestrating HTL/KAI2 and its signaling partner and preventing further signaling. (D) Positive or negative regulation based on which type of SL is present. Different kinds of SLs may trigger distinct conformational changes, e.g. SL 1 may promote the degradation of regulators that inhibit germination, whereas SL 2 might promote the degradation of regulators that induce germination.