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Molecular Mechanism of Strigolactone Perception by DWARF14

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Molecular Mechanism of Strigolactone Perception by DWARF14 ARTICLE Received 21 Mar 2013 | Accepted 13 Sep 2013 | Published 17 Oct 2013 DOI: 10.1038/ncomms3613 Molecular mechanism of strigolactone perception by DWARF14 Hidemitsu Nakamura1,*, You-Lin Xue1,*, Takuya Miyakawa1,*, Feng Hou1, Hui-Min Qin1, Kosuke Fukui1, Xuan Shi1, Emi Ito2, Shinsaku Ito1, Seung-Hyun Park1, Yumiko Miyauchi1, Atsuko Asano1, Naoya Totsuka1, Takashi Ueda2, Masaru Tanokura1 & Tadao Asami1,3 Strigolactones (SLs) are phytohormones that inhibit shoot branching and function in the rhizospheric communication with symbiotic fungi and parasitic weeds. An a/b-hydrolase protein, DWARF14 (D14), has been recognized to be an essential component of plant SL signalling, although its precise function remains unknown. Here we present the SL-dependent interaction of D14 with a gibberellin signalling repressor SLR1 and a possible mechanism of phytohormone perception in D14-mediated SL signalling. D14 functions as a cleavage enzyme of SLs, and the cleavage reaction induces the interaction with SLR1. The crystal structure of D14 shows that 5-hydroxy-3-methylbutenolide (D-OH), which is a reaction product of SLs, is trapped in the catalytic cavity of D14 to form an altered surface. The D14 residues recognizing D-OH are critical for the SL-dependent D14 À SLR1 interaction. These results provide new insight into crosstalk between gibberellin and SL signalling pathways. 1 Department of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo 113-8657, Japan. 2 Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Tokyo 113-0033, Japan. 3 JST, CREST, 4-1-8 Honcho, Kawaguchi, Saitama, 332-0012, Japan. * These authors contributed equally to this work. Correspondence and requests for materials should be addressed to T.A. (email: [email protected]). NATURE COMMUNICATIONS | 4:2613 | DOI: 10.1038/ncomms3613 | www.nature.com/naturecommunications 1 & 2013 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3613 he terpenoid, small-compound strigolactones (SLs) are Results plant hormones that regulate plant shoot branching1,2, D14 interacts with the DELLA protein SLR1. To investigate Twhich is an important agronomic trait that determines whether D14 interacts with DELLA proteins, we performed a crop yields. In addition, SLs stimulate the germination of root yeast two-hybrid (Y2H) assay using D14 as the bait and SLR1, the parasitic weeds3,4 that cause devastating crop damage5 and induce only DELLA protein in rice, as the prey in the presence of various hyphal branching in symbiotic arbuscular mycorrhizal fungi that SLs, including (±)-20-epi-5-deoxystrigol (a racemic mixture of promote the growth of host plants by capturing essential inorganic natural SLs ( þ )-20-epi-5-deoxystrigol (1) and ( À )-ent-20-epi-5- nutrients from the soil6–8. Owing to the importance of SLs in deoxystrigol), (±)-GR24 (a racemic mixture of ( þ )-GR24 (2) agriculture, the mechanism and signal transduction pathway of SLs have been extensively researched to provide a perspective on the broader SL functions. However, the mechanisms responsible for SL –1 a Dilution 110 recognition by plants are poorly understood. SLs contain a structural core that consists of a tricyclic-lactone Dilution 110–1 epi-5-DS (ABC-ring) and a butenolide group (D-ring) that are connected via an enol ether linkage (compounds 1 À 4; Supplementary +His, Ade Fig. S1a). In plants, SLs are synthesized from carotenoids through carlactone (4) (ref. 9), a butenolide-containing compound with (±)-GR24 SL-like biological activity, by a sequential reaction of several Mock enzymes, including an iron-binding protein D27 (ref. 9), the carotenoid cleavage dioxygenases 7 and 8, and a cytochrome P450 (±)-epi-GR24 protein MAX1 (refs 10–12) (Supplementary Fig. S1b). In addition, studies on a set of branching mutants of some plant species have indicated that the d14 and d3/max2/rms4 genes are b O O O O closely related to a pathway downstream of SLs1,2,13,14 (Supplementary Fig. S1b). D14 genes encode a/b-hydrolase family proteins13–16 and their mutants exhibit a highly branched phenotype and are insensitive to O O O O O O SLs13–14.Thed3/max2/rms4 mutants are also SL insensitive1,2. D3/ MAX2/RMS4 genes encode members of the F-box-family protein17– 20 that participate in an Skp-cullin-F box (SCF) complex18 and have ′ diverse roles in the plant lifecycle14,21–30. Recently, it has been (–)-ent-2 -epi-GR7 (3) (–)-ent-GR7 (6) reported that petunia DAD2, an orthologue of rice DWARF14 (D14) protein, can hydrolyse the enol ether linkage of GR24 and 36 interacts with PhMAX2A, a petunia orthologue of Arabidopsis Bait Prey +His, Ade –His, Ade –His, Ade MAX2 protein, indicating that the formation of the DAD2– PhMAX2A complex initiates an SCF-mediated signal transduction D14 SLR1 pathway31. However, it still remains unclear how the hydrolyzation of SLs induces the formation of the DAD2–PhMAX2 complex and Vec SLR1 what is/are the target(s) of the SCF complex. The Arabidopsis gibberellin (GA) biosynthetic mutant ga1-3 D14 Vec exhibits enhanced shoot branching, and the overexpression of GA 2-oxidase genes in rice, in which GA levels are reduced, promotes Vec Vec 32 tillering . These results suggest that GAs regulate branching 110–1 10–2 110–1 10–2 110–1 10–2 together with or without SLs. The DELLA-family proteins are key negative regulators of GA signalling through interaction with c 30 growth promoting transcription factors, such as PIFs. DELLA 3 proteins have recently been reported to upregulate jasmonate (JA) 25 signalling by physically interacting with JAZs, repressors of JA 6 signalling33. Further, JAZs reportedly inhibit DELLAs À PIFs 20 interactions. Thus, JA inhibits plant growth by inducing the 15 degradation of JAZs and restoring the interaction of DELLAs with PIFs34 (Supplementary Fig. S1c). In addition, recent reports 10 suggest that a transcription factor, which broadly regulates brassinosteroid signalling, BZR1, mediates growth response to 5 35,36 Lengh of 2nd tiller (mm) GA via direct interaction with DELLAs . These reports 0 indicate that DELLAs have a role in regulating multiple signals. 0 0.01 0.1 1 To investigate whether DELLAs mediate crosstalk between GA Concentration of GR7 (μM) and SL signalling pathways, we explored the interaction between the rice D14 and the DELLA protein SLR1. Here we show that the Figure 1 | Interaction between D14 and SLR1. (a)GrowthofAH109 rice D14 interacts with SLR1 in an SL-dependent manner, thus transformants with pGBK-D14 and pGAD-SLR1 on SD-His, Ade plates with contributing to the negative regulation of GA signalling37 various SLs. epi-5-DS: (±)-20-epi-5-deoxystrigol. (±)-epi-GR24: (±)-20-epi- (Supplementary Fig. S1d). Moreover, a series of crystallographic GR24. (b)Structuresof(À )-ent-20-epi-GR7 (3)and(À )-ent-GR7 (6)and and biochemical studies suggest an advanced molecular mechan- growth of AH109 transformants on an SD-His, Ade plate with or without ism of D14 in SL perception and signal transduction. Our results 10 mM(À )-ent-20-epi-GR7 (3)or(À )-ent-GR7 (6). (c) Length of second provide new insight into the crosstalk between the GA and SL tillers of 3-week-old rice treated with ( À )-ent-20-epi-GR7 (3)or(À )-ent- signalling pathways. GR7 (6)(mean±s.d.; n ¼ 5). 2 NATURE COMMUNICATIONS | 4:2613 | DOI: 10.1038/ncomms3613 | www.nature.com/naturecommunications & 2013 Macmillan Publishers Limited. All rights reserved. NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3613 ARTICLE O abO 2,500 2,400 O O O T T 2,000 9 2,000 1,600 1,500 1,200 1,000 800 ** Total binding (d.p.m.) Specific binding (d.p.m.) 500 400 0 0 NC GR24 07010 20 30 40 50 60 Time (min) Figure 2 | SL-binding properties of D14 proteins. (a) Competition for T2-GR7 (9) binding to D14 by cold SLs (mean±s.d., n ¼ 3). NC, no competitor. d.p.m., disintegrations per minute. **Po0.01 (Student’s t-test) versus no competitor control. The structure of T2-GR7 (9) is shown as an inset. (b) Association rates of T2-GR7 (9) and D14. The specific binding of T2-GR7 (9) reached one-half of the maximum within 1 min (mean; n ¼ 2 À 3). 0 and ( À )-ent-GR24 (5)), and (±)-2 -epi-GR24 (a racemic mix- a 0 0 GFP-D14 nYFP-SLR1 Merged ture of ( þ )-2 -epi-GR24 and ( À )-ent-2 -epi-GR24). The result cYFP-D14 indicated that these SLs induced a D14–SLR1 interaction (Fig. 1a). When ( À )-ent-GR7 (6) was added to the medium, this D14–SLR1 interaction was not observed, whereas when ( À )-ent- 20-epi-GR7 (3), an enantiomer of ( À )-ent-GR7 (6), was added to the medium, this interaction was clearly observed (Fig. 1b). Among the other tested SLs, 5,6-dihydro-( À )-ent-20-epi-GR7 (dihydro-GR7, 7; Supplementary Fig. S2b) also induced the interaction between D14 and SLR1, but 5,6,30,40-tetrahydro-( À )- ent-20-epi-GR7 (tetrahydro-GR7, 8; Supplementary Fig. S2b) did not induce the interaction (Supplementary Fig. S2a). The b – + 0 GR24 inhibitory effect of ( À )-ent-2 -epi-GR7 (3) on the tiller bud ––++ outgrowth of rice was stronger than that of ( À )-ent-GR7 GA4 pMET––GID1– GID1 GID1 – GID1 (6) (Fig. 1c), indicating that the D14–SLR1 complex is formed in the presence of active SL forms. Similar results were obtained in +HA the Y2H assay using dihydro-GR7 (7, active form) and tetra- hydro-GR7 (8, less active form) (Supplementary Fig. S2). The –HA direct interaction between D14 and SLs was determined using a 3 non-equilibrium gel-permeation technique and [5,6- H]-5,6- Figure 3 | D14–SLR1 interaction in planta and the competition between 0 dihydro-( À )-ent-2 -epi-GR7 (T2-GR7, 9; Fig.
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