A structural homologue of the plant receptor D14 mediates responses to strigolactones in the fungal phytopathogen Cryphonectria parasitica

Abstract

 Strigolactones (SLs) are plant hormones and important signaling molecules required to promote the arbuscular mycorrhizal (AM) symbiosis. While in plants an /-hydrolase, DWARF14 (D14), was shown to act as a receptor that binds and cleaves SLs, the fungal receptor for SLs is unknown.  Since AM fungi are currently not genetically tractable, in this study, we used the fungal pathogen Cryphonectria parasitica for which gene deletion protocols exist, as a model, as we have previously shown that it responds to SLs. By means of computational, biochemical and genetic analyses we identified a D14 structural homologue, CpD14.  Molecular homology modelling and docking support the prediction that CpD14 interacts with and hydrolyses SLs. The recombinant CpD14 protein shows / hydrolytic activity in vitro against the SLs synthetic analogue GR24; its enzymatic activity requires an intact Ser/His/Asp catalytic triad. CpD14 expression in the d14-1 loss-offunction Arabidopsis thaliana line did not rescue the plant mutant phenotype. However, gene inactivation by knock-out homologous recombination reduced fungal sensitivity to SLs.  These results indicate that CpD14 is involved in SLs responses in C. parasitica and strengthen the role of SLs as multifunctional molecules acting in plant microbe-interactions.

Chemistry of Strigolactones, Key Players in Plant Communication

“…Canonical SLs as 5DS (3), solanacyl acetate (23), and solanacol (22) in aqueous solutions were reported less stable than GR24 (56). [83][84] Generally, hydroxy-SLs with hydroxyl group on the A-or B-ring, such as strigol (1), orobanchol (10), and sorgomol (6), are less stable than non-hydroxy-SLs such as sorgolactone (5), 5DS (3), and solanacyl acetate (23). [17,[84][85] The low stability of noncanonical SL biosynthetic intermediates [e. g., CL (27), CLA (29), MeCLA (31), and derivatives] and noncanonical SLs [heliolactone (36), zealactone (41)] was also reported.…”

“…SLs have been also found active on phytopathogenic fungi. [6] SLs were identified in 2008 as the ninth class of hormones, initially discovered for the control of aerial plant architecture. [7] The discovery of a new class of hormones such as SLs is a major advance in plant biology.…”

“…The involvement of SL in the establishment of mycorrhizal symbioses and their presence in the majority of land plants, including bryophytes (descendants of the first land plants) and even certain algae, suggest that they played a decisive role in the colonization of the terrestrial environment by plants around 450 million years ago. SLs have been also found active on phytopathogenic fungi [6] . SLs were identified in 2008 as the ninth class of hormones, initially discovered for the control of aerial plant architecture [7] .…”

Synthesis and Biological Properties of Fluorescent Strigolactone Mimics Derived from 1,8-Naphthalimide

“…This variation in structure could induce a variation in the receptor-SL mimic affinity as well as variations in the conformational changes, which could explain the heterogeneity in the biological outcome observed. Recently, a fungal homolog from Cryphonectria parasitica, of the plant DWARF14 (D14) SL receptor, was reported and characterized [90]. This receptor is able to hydrolyze GR24 and this enzymatic activity requires the known catalytic triad Ser/His/Asp.…”

Strigolactones as a hormonal hub for the acclimation and priming to environmental stress in plants

“…D14 receptors include members that have undergone wide differentiation in plants and beyond. A recent study found a D14‐like protein in the phytopathogen Cryphonectria parasitica that interacts with strigolactones, hydrolyses them and is needed for their perception, even though the ecological significance of strigolactones for this organism is unresolved (Fiorilli et al, 2022 ). Also the perception of strigolactones as germination stimulants in seeds of parasitic plants relies on an expanded family of D14‐like receptors, called HYPOSENSITIVE TO LIGHT (HTL).…”