DWARF14 is a non-canonical hormone receptor for strigolactone

Abstract

Classical hormone receptors reversibly and non-covalently bind active hormone molecules, which are generated by biosynthetic enzymes, to trigger signal transduction. The α/β hydrolase DWARF14 (D14), which hydrolyses the plant branching hormone strigolactone and interacts with the F-box protein D3/MAX2, is probably involved in strigolactone detection. However, the active form of strigolactone has yet to be identified and it is unclear which protein directly binds the active form of strigolactone, and in which manner, to act as the genuine strigolactone receptor. Here we report the crystal structure of the strigolactone-induced AtD14-D3-ASK1 complex, reveal that Arabidopsis thaliana (At)D14 undergoes an open-to-closed state transition to trigger strigolactone signalling, and demonstrate that strigolactone is hydrolysed into a covalently linked intermediate molecule (CLIM) to initiate a conformational change of AtD14 to facilitate interaction with D3. Notably, analyses of a highly branched Arabidopsis mutant d14-5 show that the AtD14(G158E) mutant maintains enzyme activity to hydrolyse strigolactone, but fails to efficiently interact with D3/MAX2 and loses the ability to act as a receptor that triggers strigolactone signalling in planta. These findings uncover a mechanism underlying the allosteric activation of AtD14 by strigolactone hydrolysis into CLIM, and define AtD14 as a non-canonical hormone receptor with dual functions to generate and sense the active form of strigolactone.

The F-Box Protein ZYGO1 Mediates Bouquet Formation to Promote Homologous Pairing, Synapsis, and Recombination in Rice Meiosis

“…ASK1 is involved in many aspects of plant growth and development through the interactions with different F-box proteins (Gray et al, 1999;Zhao et al, 2001;Yao et al, 2016). During male meiosis, ASK1 is also required for chromosome condensation, homologous pairing, synapsis, and chromosome separation Zhao et al, 2006).…”

Regulation of Strigolactone Biosynthesis by Gibberellin Signaling

“…The activities of SLs depend on D3 and D14: D3 encodes the F-box protein and D14 encodes SL receptor, which act in SL signaling. D53, which encodes a substrate of the SCF D3 complex, was recently reported to be a repressor of SL signaling in rice, and the degradation of D53 protein by SL, in cooperation with D14 and D3, is considered as a key event in SL signaling (Jiang et al, 2013;Zhou et al, 2013;Yao et al, 2016;de Saint Germain et al, 2016).…”

From little things big things grow: karrikins and new directions in plant development

“…However, in plants D14 undergoes proteolysis in response to strigolactone application (Chevalier et al 2014), so this may be the dominant mechanism for removal of D14 in its activated and closed state. Finally, strigolactone hydrolysis by D14 is insufficient to confer a signalling function, because the non-functional d14-5 protein exhibits enhanced rates of hydrolysis, but strongly impaired interaction with D3/MAX2 (Yao et al 2016). Collectively, these data demonstrate conclusively that D14 is not merely an enzyme, but also serves as a strigolactone receptor that binds and subsequently hydrolyses its ligand to transduce a signal.…”

“…Consistent with this interpretation, crystallography demonstrated the ligand-dependent interaction of D14 and D3/MAX2, together with the Arabidopsis SCF. component ASK1 (Yao et al 2016). This crucial evidence revealed that binding of strigolactone to GR24 causes the lid domain of D14 to flatten and partially collapse the ligand-binding cavity, trapping a strigolactone hydrolysis product within.…”

“…Extensive biochemistry experiments have enhanced this genetic evidence. D14 hydrolyses strigolactones, albeit very slowly, by nucleophilic attack upon the strigolactone D-ring, which is oriented towards the catalytic serine (Hamiaux et al 2012;Yao et al 2016;de Saint Germain et al 2016). Mutation of the catalytic triad residues renders D14 nonfunctional as an enzyme, and also as a transducer of strigolactone signalling in planta (Hamiaux et al 2012).…”