Strigolactone Promotes Degradation of DWARF14, an α/β Hydrolase Essential for Strigolactone Signaling in<i>Arabidopsis</i>

Chevalier, Florian; Nieminen, Kaisa; Sánchez-Ferrero, Juan C.; Rodríguez, María Luisa; Chagoyen, Mónica; Hardtke, Christian S.; Cubas, Pilar

doi:10.1105/tpc.114.122903

Cited by 216 publications

(224 citation statements)

References 94 publications

(187 reference statements)

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“…It can be envisioned that once the cell is committed to the branching fate through the activation of SL pathways, the plants want to shut down the branching signals as soon as possible. This could be achieved by destabilization of the receptor D14 upon ligand binding and effector coupling as reported here, followed by ubiquitination-mediated degradation as D14 is subject to proteolysis in cells in the presence of GR24 [22]. While many gaps remain in our understanding of this unusual signaling mechanism, the structural and mutational analyses of the D14/GR24 and D14/GR24/D3 complexes reported in this paper establish the GR24 binding mode in the D14 pocket and identify the D3-binding interface of D14.…”

Section: Discussionmentioning

confidence: 99%

“…Recent studies have identified the putative transcriptional repressor D53 [19,20] as well as the transcription factor BES1 as SCF D3 substrate targets in response to SL exposure and the D53 paralog SMAX1 in response to karrikin exposure. SLs induce association of D14 with D3/D53 and D3/BES1 complexes and promote SCF D3 -mediated degradation of D53 [19,20], BES1 [21], and D14 itself [22].…”

Section: Introductionmentioning

confidence: 99%

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Destabilization of strigolactone receptor DWARF14 by binding of ligand and E3-ligase signaling effector DWARF3

et al. 2015

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Strigolactones (SLs) are endogenous hormones and exuded signaling molecules in plant responses to low levels of mineral nutrients. Key mediators of the SL signaling pathway in rice include the α/β-fold hydrolase DWARF 14 (D14) and the F-box component DWARF 3 (D3) of the ubiquitin ligase SCF D3 that mediate ligand-dependent degradation of downstream signaling repressors. One perplexing feature is that D14 not only functions as the SL receptor but is also an active enzyme that slowly hydrolyzes diverse natural and synthetic SLs including GR24, preventing the crystallization of a binary complex of D14 with an intact SL as well as the ternary D14/SL/D3 complex. Here we overcome these barriers to derive a structural model of D14 bound to intact GR24 and identify the interface that is required for GR24-mediated D14-D3 interaction. The mode of GR24-mediated signaling, including ligand recognition, hydrolysis by D14, and ligand-mediated D14-D3 interaction, is conserved in structurally diverse SLs. More importantly, D14 is destabilized upon the binding of ligands and D3, thus revealing an unusual mechanism of SL recognition and signaling, in which the hormone, the receptor, and the downstream effectors are systematically destabilized during the signal transduction process.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Destabilization of strigolactone receptor DWARF14 by binding of ligand and E3-ligase signaling effector DWARF3

et al. 2015

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“…Previous reports show that the other known components of SL signaling, D14 and MAX2, are expressed in the same vascularassociated tissues as SMXL7 and are at least partially nuclear (Chevalier et al, 2014;Stirnberg et al, 2007). To explore the colocation of these proteins in more detail, we used both transient expression assays in N. benthamiana and stable expression in Arabidopsis.…”

Section: (E) To (G) Subcellular Localization Of Smxl7-yfp (E) D14-cementioning

confidence: 99%

“…In the second model, SLs are proposed to act throughout the shoot to trigger clathrin-mediated endocytosis of the PIN1 auxin efflux carrier (Crawford et al, 2010;Shinohara et al, 2013). This hinders the establishment of positive feedback-driven, canalized auxin export from buds into the stem, which has been proposed to be required for the outgrowth of buds (Li and Bangerth, 1999;Prusinkiewicz et al, 2009;Crawford et al, 2010;Shinohara et al, 2013 very likely to act as a SL receptor, since it binds and hydrolyses the synthetic SL analog GR24 and is required for sensitivity to SL (Liu et al, 2009;Hamiaux et al, 2012;Waters et al, 2012;Kagiyama et al, 2013;Zhao et al, 2013;Chevalier et al, 2014). D14 acts in concert with the MAX2 F-box protein, which forms part of an SCFtype ubiquitin ligase complex (Stirnberg et al, 2007;Hamiaux et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…The deletion of the NLS also compromised the ability of the fusion protein expressed from the 35S promoter to restore increased branching levels to the smxl678 max2 mutant ( Figure 1K). These data suggest that the nuclear localization of SMXL7 is required for its function.Previous reports show that the other known components of SL signaling, D14 and MAX2, are expressed in the same vascularassociated tissues as SMXL7 and are at least partially nuclear (Chevalier et al, 2014;Stirnberg et al, 2007). To explore the colocation of these proteins in more detail, we used both transient expression assays in N. benthamiana and stable expression in Arabidopsis.…”

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confidence: 99%

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SMAX1-LIKE7 signals from the nucleus to regulate shoot development in Arabidopsis via partially EAR motif-independent mechanisms

et al. 2016

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Strigolactones (SLs) are hormonal signals that regulate multiple aspects of shoot architecture, including shoot branching. Like many plant hormonal signaling systems, SLs act by promoting ubiquitination of target proteins and their subsequent proteasome-mediated degradation. Recently, SMXL6, SMXL7, and SMXL8, members of the SMAX1-LIKE (SMXL) family of chaperonin-like proteins, have been identified as proteolytic targets of SL signaling in Arabidopsis thaliana. However, the mechanisms by which these proteins regulate downstream events remain largely unclear. Here, we show that SMXL7 functions in the nucleus, as does the SL receptor, DWARF14 (D14). We show that nucleus-localized D14 can physically interact with both SMXL7 and the MAX2 F-box protein in a SL-dependent manner and that disruption of specific conserved domains in SMXL7 affects its localization, SL-induced degradation, and activity. By expressing and overexpressing these SMXL7 protein variants, we show that shoot tissues are broadly sensitive to SMXL7 activity, but degradation normally buffers the effect of increasing SMXL7 expression. SMXL7 contains a well-conserved EAR (ETHYLENE-RESPONSE FACTOR Amphiphilic Repression) motif, which contributes to, but is not essential for, SMXL7 functionality. Intriguingly, different developmental processes show differential sensitivity to the loss of the EAR motif, raising the possibility that there may be several distinct mechanisms at play downstream of SMXL7. INTRODUCTIONShoot system architectural characteristics strongly influence the productivity of many crop species, and architectural traits have been selected in both historical and contemporary breeding schemes. Understanding the mechanisms that regulate shoot architecture, and its environmental responsiveness, is therefore an important goal for plant research. It is well established that long-distance hormonal signals, including auxin, cytokinin, and strigolactone (SL), are key regulators of shoot architecture and allow communication both within the shoot system and between the shoot and root . For instance, cytokinin produced in the root system in response to the availability of nitrate ions is systemically transported to the shoot, where it promotes branching (Kiba et al., 2011; Müller et al., 2015). Similarly, root-derived SL plays a key role in negatively regulating branching in response to low phosphate availability in the rhizosphere (Kohlen et al., 2011). However, our understanding of the molecular mechanisms that act downstream of these hormones to alter developmental processes in the shoot is currently limited. This is particularly true of SLs. Analysis of the phenotypes of SL biosynthesis and signaling mutants has revealed roles for SLs in the regulation of shoot branching, branching angle, plant height, stem thickness, and leaf blade elongation . The role of SLs in regulating shoot branching has been intensively studied, resulting in two contrasting, nonexclusive models for their mode of action. In the first, SLs are proposed to act locally in axill...

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Differential role of MAX2 and strigolactones in pathogen, ozone, and stomatal responses

et al. 2020

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Strigolactones are a group of phytohormones that control developmental processes including shoot branching and various plant–environment interactions in plants. We previously showed that the strigolactone perception mutant more axillary branches 2 (max2) has increased susceptibility to plant pathogenic bacteria. Here we show that both strigolactone biosynthesis (max3 and max4) and perception mutants (max2 and dwarf14) are significantly more sensitive to Pseudomonas syringae DC3000. Moreover, in response to P. syringae infection, high levels of SA accumulated in max2 and this mutant was ozone sensitive. Further analysis of gene expression revealed no major role for strigolactone in regulation of defense gene expression. In contrast, guard cell function was clearly impaired in max2 and depending on the assay used, also in max3, max4, and d14 mutants. We analyzed stomatal responses to stimuli that cause stomatal closure. While the response to abscisic acid (ABA) was not impaired in any of the mutants, the response to darkness and high CO2 was impaired in max2 and d14‐1 mutants, and to CO2 also in strigolactone synthesis (max3, max4) mutants. To position the role of MAX2 in the guard cell signaling network, max2 was crossed with mutants defective in ABA biosynthesis or signaling. This revealed that MAX2 acts in a signaling pathway that functions in parallel to the guard cell ABA signaling pathway. We propose that the impaired defense responses of max2 are related to higher stomatal conductance that allows increased entry of bacteria or air pollutants like ozone. Furthermore, as MAX2 appears to act in a specific branch of guard cell signaling (related to CO2 signaling), this protein could be one of the components that allow guard cells to distinguish between different environmental conditions.

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Strigolactone Promotes Degradation of DWARF14, an α/β Hydrolase Essential for Strigolactone Signaling inArabidopsis

Cited by 216 publications

References 94 publications

Destabilization of strigolactone receptor DWARF14 by binding of ligand and E3-ligase signaling effector DWARF3

Destabilization of strigolactone receptor DWARF14 by binding of ligand and E3-ligase signaling effector DWARF3

SMAX1-LIKE7 signals from the nucleus to regulate shoot development in Arabidopsis via partially EAR motif-independent mechanisms

Differential role of MAX2 and strigolactones in pathogen, ozone, and stomatal responses

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