Structural Basis for Assembly of Hsp90-Sgt1-CHORD Protein Complexes: Implications for Chaperoning of NLR Innate Immunity Receptors

Zhang, Minghao; Kadota, Yasuhiro; Prodromou, Chrisostomos; Shirasu, Ken; Pearl, Laurence H.

doi:10.1016/j.molcel.2010.05.010

Cited by 113 publications

(151 citation statements)

References 55 publications

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“…Several plant receptor proteins function with the help of chaperones and cochaperones, including HSP90 (heat shock protein 90), RAR1 (required for Mla12 resistance), and SGT1 (suppressor of G2 allele of skp1) (Shirasu, 2009;Zhang et al, 2010). SGT1 was originally identified in Saccharomyces cerevisiae as an essential cell cycle protein that interacts with Skp1p, a component of the conserved eukaryotic Skp1/Cullin/F-box (SCF) E3 ubiquitin ligase.…”

Section: Introductionmentioning

confidence: 99%

A Secreted Effector Protein ofUstilago maydisGuides Maize Leaf Cells to Form Tumors

et al. 2015

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The biotrophic smut fungus Ustilago maydis infects all aerial organs of maize (Zea mays) and induces tumors in the plant tissues. U. maydis deploys many effector proteins to manipulate its host. Previously, deletion analysis demonstrated that several effectors have important functions in inducing tumor expansion specifically in maize leaves. Here, we present the functional characterization of the effector See1 (Seedling efficient effector1). See1 is required for the reactivation of plant DNA synthesis, which is crucial for tumor progression in leaf cells. By contrast, See1 does not affect tumor formation in immature tassel floral tissues, where maize cell proliferation occurs independent of fungal infection. See1 interacts with a maize homolog of SGT1 (Suppressor of G2 allele of skp1), a factor acting in cell cycle progression in yeast (Saccharomyces cerevisiae) and an important component of plant and human innate immunity. See1 interferes with the MAPK-triggered phosphorylation of maize SGT1 at a monocot-specific phosphorylation site. We propose that See1 interferes with SGT1 activity, resulting in both modulation of immune responses and reactivation of DNA synthesis in leaf cells. This identifies See1 as a fungal effector that directly and specifically contributes to the formation of leaf tumors in maize.

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Section: Introductionmentioning

confidence: 99%

A Secreted Effector Protein ofUstilago maydisGuides Maize Leaf Cells to Form Tumors

et al. 2015

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“…NLR activation upon direct or indirect recognition of an effector molecule induces a signaling cascade leading to pathogen containment often involving host programmed cell death (the hypersensitive response [HR]) and accumulation of the systemic resistance signaling hormone salicylic acid (SA) (Bent and Mackey, 2007;Vlot et al, 2009). Many NLRs additionally require HSP90 and its cochaperones SGT1 and RAR1 for stability and/or activation (Shirasu, 2009;Zhang et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Perturbation of Arabidopsis Amino Acid Metabolism Causes Incompatibility with the Adapted Biotrophic Pathogen Hyaloperonospora arabidopsidis

et al. 2011

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Reliance of biotrophic pathogens on living plant tissues to propagate implies strong interdependence between host metabolism and nutrient uptake by the pathogen. However, factors determining host suitability and establishment of infection are largely unknown. We describe a loss-of-inhibition allele of ASPARTATE KINASE2 and a loss-of-function allele of DIHYDRODIPICOLINATE SYNTHASE2 identified in a screen for Arabidopsis thaliana mutants with increased resistance to the obligate biotrophic oomycete Hyaloperonospora arabidopsidis (Hpa). Through different molecular mechanisms, these mutations perturb amino acid homeostasis leading to overaccumulation of the Asp-derived amino acids Met, Thr, and Ile. Although detrimental for the plant, the mutations do not cause defense activation, and both mutants retain full susceptibility to the adapted obligate biotrophic fungus Golovinomyces orontii (Go). Chemical treatments mimicking the mutants' metabolic state identified Thr as the amino acid suppressing Hpa but not Go colonization. We conclude that perturbations in amino acid homeostasis render the mutant plants unsuitable as an infection substrate for Hpa. This may be explained by deployment of the same amino acid biosynthetic pathways by oomycetes and plants. Our data show that the plant host metabolic state can, in specific ways, influence the ability of adapted biotrophic strains to cause disease.

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“…The detailed activation mechanism of NLR R proteins is unclear. During the past decade, intensive studies on RAR1, SGT1, and HSP90 using genetic and biochemical approaches established these components as members of a protein complex required for chaperone activities to properly fold and stabilize NLR R proteins (7,8). Interestingly, mammalian SGT1 and HSP90 were also shown to be required for NLRmediated immune responses.…”

mentioning

confidence: 99%

Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation

Cheng

Huang

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

222

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The nucleotide-binding domain and leucine-rich repeats containing proteins (NLRs) serve as immune receptors in both plants and animals. Overaccumulation of NLRs often leads to autoimmune responses, suggesting that the levels of these immune receptors must be tightly controlled. However, the mechanism by which NLR protein levels are regulated is unknown. Here we report that the F-box protein CPR1 controls the stability of plant NLR resistance proteins. Loss-of-function mutations in CPR1 lead to higher accumulation of the NLR proteins SNC1 and RPS2, as well as autoactivation of immune responses. The autoimmune responses in cpr1 mutant plants can be largely suppressed by knocking out SNC1. Furthermore, CPR1 interacts with SNC1 and RPS2 in vivo, and overexpressing CPR1 results in reduced accumulation of SNC1 and RPS2, as well as suppression of immunity mediated by these two NLR proteins. Our data suggest that SKP1-CULLIN1-F-box (SCF) complex-mediated stability control of plant NLR proteins plays an important role in regulating their protein levels and preventing autoimmunity.

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Structural Basis for Assembly of Hsp90-Sgt1-CHORD Protein Complexes: Implications for Chaperoning of NLR Innate Immunity Receptors

Cited by 113 publications

References 55 publications

A Secreted Effector Protein ofUstilago maydisGuides Maize Leaf Cells to Form Tumors

A Secreted Effector Protein ofUstilago maydisGuides Maize Leaf Cells to Form Tumors

Perturbation of Arabidopsis Amino Acid Metabolism Causes Incompatibility with the Adapted Biotrophic Pathogen Hyaloperonospora arabidopsidis

Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation

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