NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature

Howard Hughes Medical Institute-Gordon and Betty Moore Foundation, Department of Biology, PO Box 90338, Duke University, Durham, North Carolina 27708, USA.
Nature (Impact Factor: 41.46). 06/2012; 486(7402):228-32. DOI: 10.1038/nature11162
Source: PubMed


Salicylic acid (SA) is a plant immune signal produced after pathogen challenge to induce systemic acquired resistance. It is the only major plant hormone for which the receptor has not been firmly identified. Systemic acquired resistance in Arabidopsis requires the transcription cofactor nonexpresser of PR genes 1 (NPR1), the degradation of which acts as a molecular switch. Here we show that the NPR1 paralogues NPR3 and NPR4 are SA receptors that bind SA with different affinities. NPR3 and NPR4 function as adaptors of the Cullin 3 ubiquitin E3 ligase to mediate NPR1 degradation in an SA-regulated manner. Accordingly, the Arabidopsis npr3 npr4 double mutant accumulates higher levels of NPR1, and is insensitive to induction of systemic acquired resistance. Moreover, this mutant is defective in pathogen effector-triggered programmed cell death and immunity. Our study reveals the mechanism of SA perception in determining cell death and survival in response to pathogen challenge.

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    • "Since sumoylation of NPR1 affects its degradation, we tested the effect of sumoylation on NPR1 interactions with its CUL3 E3 ligase adaptors, NPR3 and NPR4. SA binding to NPR3 promotes interaction with NPR1, while SA binding to NPR4 disrupts binding to NPR1 (Fu et al., 2012). We found that sim3 and S55/59D mutations diminish the SA-dependent interactions between NPR1-NPR3 and NPR1-NPR4 (Figures 5A, 5B, and S4). "
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    ABSTRACT: NPR1, a master regulator of basal and systemic acquired resistance in plants, confers immunity through a transcriptional cascade, which includes transcription activators (e.g., TGA3) and repressors (e.g., WRKY70), leading to the massive induction of antimicrobial genes. How this single protein orchestrates genome-wide transcriptional reprogramming in response to immune stimulus remains a major question. Paradoxically, while NPR1 is essential for defense gene induction, its turnover appears to be required for this function, suggesting that NPR1 activity and degradation are dynamically regulated. Here we show that sumoylation of NPR1 by SUMO3 activates defense gene expression by switching NPR1's association with the WRKY transcription repressors to TGA transcription activators. Sumoylation also triggers NPR1 degradation, rendering the immune induction transient. SUMO modification of NPR1 is inhibited by phosphorylation at Ser55/Ser59, which keeps NPR1 stable and quiescent. Thus, posttranslational modifications enable dynamic but tight and precise control of plant immune responses. Copyright © 2015 Elsevier Inc. All rights reserved.
    Cell host & microbe 08/2015; 18(2):169-82. DOI:10.1016/j.chom.2015.07.005 · 12.33 Impact Factor
    • "F. graminearum disease severity was also higher in the npr1 (nonexpresser of PR genes1) mutant (Makandar et al. 2010), which lacks an active SA-response regulator (Fu and Dong 2013). SA promotes the translocation of NPR1 from the cytosol into the nucleus and also facilitates NPR1 turnover, which is critical for its activity as a transcription coactivator in SA signaling (Fu et al. 2012; Spoel et al. 2009). In agreement with a role for NPR1 in curtailing disease severity, overexpression of NPR1 conferred enhanced resistance against F. graminearum in Arabidopsis (Makandar et al. 2006, 2010). "
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    ABSTRACT: Fusarium graminearum (Fg) causes Fusarium head blight (FHB) disease in wheat and other cereals. Fg also causes disease in Arabidopsis thaliana. In both Arabidopsis and wheat, Fg infection is limited by salicylic acid (SA) signaling. Here we show that in Arabidopsis, the defense regulator EDS1 (ENHANCED DISEASE SUSCEPTIBILITY1) and its interacting partners, PAD4 (PHYTOALEXIN-DEFICIENT4) and SAG101 (SENESCENCE-ASSOCIATED GENE101) promote SA accumulation to curtail Fg infection. Characterization of plants expressing the PAD4 non-interacting eds1L262P indicated that interaction between EDS1 and PAD4 is critical for defense against Fg. A conserved serine in the predicted acyl hydrolase catalytic triad of PAD4, which is not required for defense against bacterial and oomycete pathogens, is also necessary for limiting Fg infection. These results suggest a molecular configuration of PAD4 in Arabidopsis defense against Fg that is different from its defense contribution against other pathogens. We further show that constitutive expression of Arabidopsis PAD4 can enhance FHB resistance in Arabidopsis and wheat. Taken together with previous studies of wheat and Arabidopsis expressing salicylate hydroxylase or the SA response regulator NPR1 (NON-EXPRESSER OF PR GENES1), our results show that exploring fundamental processes in a model plant provides important leads to manipulating crops for improved disease resistance.
    Molecular Plant-Microbe Interactions 04/2015; 28(8). DOI:10.1094/MPMI-04-15-0079-R · 3.94 Impact Factor
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    • "Asterisk indicates a significant difference from the control (Student's t-test; *P < 0.05). Dong, 2002), and its paralogue NPR3 (Fu et al., 2012) were also drastically reduced in WsSQS-vigs plants (Figure 8b). The fact that NPR1 is not required for brassinolide-mediated induction of PR1 expression (Divi et al., 2010) and our observation that BR6OX2, NPR and PR were all down-regulated in SQS-silenced plants point to a brassinosteroid-independent phytosterol-mediated defence signalling, thus affecting biotic stress tolerance. "
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    ABSTRACT: Withania somnifera (L.) Dunal is an important Indian medicinal plant that produces withanolides, which are triterpenoid steroidal lactones having diverse biological activities. To enable fast and efficient functional characterization of genes in this slow-growing and difficult-to-transform plant, a virus-induced gene silencing (VIGS) was established by silencing phytoene desaturase (PDS) and squalene synthase (SQS). VIGS of the gene encoding SQS, which provides precursors for triterpenoids, resulted in significant reduction of squalene and withanolides, demonstrating its application in studying withanolides biosynthesis in W. somnifera leaves. A comprehensive analysis of gene expression and sterol pathway intermediates in WsSQS-vigs plants revealed transcriptional modulation with positive feedback regulation of mevalonate pathway genes, and negative feed-forward regulation of downstream sterol pathway genes including DWF1 (delta-24-sterol reductase) and CYP710A1 (C-22-sterol desaturase), resulting in significant reduction of sitosterol, campesterol and stigmasterol. However, there was little effect of SQS silencing on cholesterol, indicating the contribution of sitosterol, campesterol and stigmasterol, but not of cholesterol, towards withanolides formation. Branch-point oxidosqualene synthases in WsSQS-vigs plants exhibited differential regulation with reduced CAS (cycloartenol synthase) and cycloartenol, and induced BAS (β-amyrin synthase) and β-amyrin. Moreover, SQS silencing also led to the down-regulation of brassinosteroid-6-oxidase-2 (BR6OX2), pathogenesis-related (PR) and nonexpressor of PR (NPR) genes, resulting in reduced tolerance to bacterial and fungal infection as well as to insect feeding. Taken together, SQS silencing negatively regulated sterol and defence-related genes leading to reduced phytosterols, withanolides and biotic stress tolerance, thus implicating the application of VIGS for functional analysis of genes related to withanolides formation in W. somnifera leaves. © 2015 Society for Experimental Biology, Association of Applied Biologists and John Wiley & Sons Ltd.
    Plant Biotechnology Journal 03/2015; doi:10.1111/pbi.12347. DOI:10.1111/pbi.12347 · 5.75 Impact Factor
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