The Many Models of Strigolactone Signaling

Abstract

Strigolactones (SLs) are a class of plant hormones involved in several biological processes that are of great agricultural concern. While initiating plant-fungal symbiosis, SLs also trigger germination of parasitic plants that pose a major threat to farming. In vascular plants, SLs control shoot branching, which is linked to crop yield. SL research has been a fascinating field that has produced a variety of different signaling models, reflecting a complex picture of hormone perception. Here, we review recent developments in the SL field and the crystal structures that gave rise to various models of receptor activation. We also highlight the increasing number of discovered SL molecules, reflecting the existence of cross-kingdom SL communication.

Figure 1.. History of Discoveries in the Strigolactone (SL) Field.

Brown lines indicate key discoveries of the biological functions of SLs. Red lines indicate discoveries concerning the signaling mechanism. Blue lines indicate discoveries of SL molecules. Based on [,,,,–,,,–,,,,–48,51,61,62,65,68,70,71]. Abbreviations: AM, arbuscular mycorrhiza; CLIM, covalently linked intermediate molecule.

Figure 2.. Chemical Structure of Strigolactones (SLs).

Canonical SLs feature a complete A, B, C, D ring structure and are split into two different families resulting from different conformations between the B and C ring. The 2′R conformation of the D-ring is conserved in all SLs (blue). (A) Strigol-type SLs have a conserved β orientation of the C-ring within the B-/C-ring junction (red). Modifications on the A-ring are variable (magenta). (B) Orobanchol-type SLs have a conserved α orientation of the C-ring within the B-/C-ring junction (red). Note the variety of the nature of the A-ring (magenta), as an epoxide in fabacol, a benzene in solanacol, and a cycloheptadiene in medicaol. (C) Noncanonical SLs feature an intact D-ring connected to the rest of the molecule in the same conformation as in canonical SLs (blue). However, the remaining ring system can adopt a different chemistry. (D) The synthetic SL analog GR24.

Figure 3.. Crystal Structures Containing Parts of the Strigolactone (SL) Analog GR24.

In each of (Ai–Hi), the position and electron difference maps of ligands in the D14 substrate-binding pocket are shown. In each of (Aii–Hii), the electron density of ligands after refinement of the ligands is illustrated. Difference electron density maps are F_o-F_c electron density maps at 3.0 σ calculated from ligand-deleted models. Maps after refinement are 2F_o-F_c electron density maps at 1.0 σ. Ligands were modeled with Coot [80], X-ray data were refined with Phenix [81], and visualizations were made with CCP4mg [82]. (A) Protein Data Bank (PDB) structure 3WIO of rice D14 with the hydroxy D-ring GR24 hydrolysis product [30]. (B) PDB structure 6BRT of rice D14 with the hydroxy D-ring GR24 hydrolysis product [68]. (C) PDB structure 4IHA of rice D14 in complex with a GR24 hydrolysis intermediate (open lactone) covalently linked to the active site Ser147 [11]. (D) PDB structure 5DJ5 of rice D14 in complex with an intact GR24 molecule [61]. (E) PDB structure 5DJ5 with an alternative interpretation of the electron density, showing the same GR24 hydrolysis intermediate as in (C). (F) PDB structure 5HZG of the AtD14-D3-ASK1 complex with electron density interpreted as a covalently linked intermediate molecule (CLIM) [62]. (G) PDB structure 5HZG of the AtD14-D3-ASK1 complex with electron density interpreted as an iodide ion [15]. (H) PDB structure 5HZG with an alternative interpretation of the electron density, showing a histidine-butenolide complex.

Figure 4.. Model of Strigolactone (SL) Signaling.

(A) The SL receptor D14 has a preformed binding pocket [10,11,59] for the SL molecule that comprises a tricyclic ABC part connected to the D-ring (red). (B) After binding of the intact SL molecule [65,68], the F-box protein D3 (MAX2) binds to D14 with its dislodged C-terminal helix, arresting D14 in a catalytically inactive state [68]. (C) Binding of the transcriptional repressor D53 to D3 causes D3 to retrieve its dislodged helix, restoring the catalytic activity of D14 [68]. D14 hydrolyzes the SL molecule, obtaining a covalent butenolide modification at the active site histidine (His) [12,38,62]. (D) During or after binding of the D3-D53 complex, the transcriptional repressor D53 is polyubiquitinated [53,54]. (E) D53 is degraded, initiating the SL gene response [53,54]. (F) D14 is then degraded [66,67] and D3 recycled.