The Arabidopsis NPR1 Protein Is a Receptor for the Plant Defense Hormone Salicylic Acid

Wu, Yue; Zhang, Di; Chu, Jee Yan; Boyle, Patrick; Wang, Yong; Brindle, Ian D.; Luca, Vincenzo De; Després, Charles

doi:10.1016/j.celrep.2012.05.008

Cited by 729 publications

(603 citation statements)

References 45 publications

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“…Recently, the mechanism of SA perception has been identified and the SA action mode has been established to transcriptionally regulate a number of genes, including those related to plant immunity (33,(39)(40)(41). Here, we found an effect of SA interference on the BFA-sensitive endocytic recycling of PM proteins that occurs probably at the level of the endocytic coat protein clathrin and does not involve transcriptional regulation.…”

Section: Discussionmentioning

confidence: 65%

Salicylic acid interferes with clathrin-mediated endocytic protein trafficking

Tejos

Beck

et al. 2013

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

104

117

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Removal of cargos from the cell surface via endocytosis is an efficient mechanism to regulate activities of plasma membrane (PM)-resident proteins, such as receptors or transporters. Salicylic acid (SA) is an important plant hormone that is traditionally associated with pathogen defense. Here, we describe an unanticipated effect of SA on subcellular endocytic cycling of proteins. Both exogenous treatments and endogenously enhanced SA levels repressed endocytosis of different PM proteins. The SA effect on endocytosis did not involve transcription or known components of the SA signaling pathway for transcriptional regulation. SA likely targets an endocytic mechanism that involves the coat protein clathrin, because SA interfered with the clathrin incidence at the PM and clathrin-deficient mutants were less sensitive to the impact of SA on the auxin distribution and root bending during the gravitropic response. By contrast, SA did not affect the ligand-induced endocytosis of the FLAGELLIN SENSING2 (FLS2) receptor during pathogen responses. Our data suggest that the established SA impact on transcription in plant immunity and the nontranscriptional effect of SA on clathrin-mediated endocytosis are independent mechanisms by which SA regulates distinct aspects of plant physiology.

show abstract

Section: Discussionmentioning

confidence: 65%

Salicylic acid interferes with clathrin-mediated endocytic protein trafficking

Tejos

Beck

et al. 2013

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

104

117

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“…The PP pathway is also a source for SA biosynthesis [122]. Moreover, potential homologs for the SA receptor Nonexpressor of PR genes 1 (NPR1) [123], were reported for all land plants [113] and the putative NPR1 homolog of P. patens can partially complement defense signaling-associated phenotypes of the Arabidopsis npr1 mutant [124]. As for ET, recent studies showed that streptophyte algae produce, sense and respond to ET [112,115], but these studies did not dissect the role of ET as a hormone involved in defense.…”

Section: Evolution Of Phytohormone Defense Networkmentioning

confidence: 99%

On plant defense signaling networks and early land plant evolution

Vries

Dahlen

Gould

et al. 2018

Communicative & Integrative Biology

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All land plants must cope with phytopathogens. Algae face pathogens, too, and it is reasonable to assume that some of the strategies for dealing with pathogens evolved prior to the origin of embryophytes – plant terrestrialization simply changed the nature of the plant-pathogen interactions. Here we highlight that many potential components of the angiosperm defense toolkit are i) found in streptophyte algae and non-flowering embryophytes and ii) might be used in non-flowering plant defense as inferred from published experimental data. Nonetheless, the common signaling networks governing these defense responses appear to have become more intricate during embryophyte evolution. This includes the evolution of the antagonistic signaling pathways of jasmonic and salicylic acid, multiple independent expansions of resistance genes, and the evolution of resistance gene-regulating microRNAs. Future comparative studies will illuminate which modules of the streptophyte defense signaling network constitute the core and which constitute lineage- and/or environment-specific (peripheral) signaling circuits.

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“…SA is an effective signaling molecule, and only micromolar concentrations are required for these effects inside plant cells (Raskin et al, 1987;Wu et al, 2012). The basal level of SA can vary between species and even within the same plant family (Raskin et al, 1990).…”

Section: Low Concentrations Of Sa Increase Sqr Activitymentioning

confidence: 99%

“…However, as these enzymes are not classical transcription regulators, they are unlikely to directly regulate gene expression. Recently, there is clear evidence for NON-EXPRESSOR OF PATHOGENESIS-RELATED GENES1 (NPR1), NPR3, and NPR4 acting together as SA receptors based on their binding properties, direct role in defense gene expression, and their impact on disease resistance (Fu et al, 2012;Wu et al, 2012). However, studies beyond defense responses have shown an involvement of SA in thermotolerance and drought resistance combined with an induction of mitochondrial ROS production (Nie et al, 2015;Okuma et al, 2014).…”

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confidence: 99%

Salicylic Acid-Dependent Plant Stress Signaling via Mitochondrial Succinate Dehydrogenase

et al. 2017

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Mitochondria are known for their role in ATP production and generation of reactive oxygen species, but little is known about the mechanism of their early involvement in plant stress signaling. The role of mitochondrial succinate dehydrogenase (SDH) in salicylic acid (SA) signaling was analyzed using two mutants: disrupted in stress response1 (dsr1), which is a point mutation in SDH1 identified in a loss of SA signaling screen, and a knockdown mutant (sdhaf2) for SDH assembly factor 2 that is required for FAD insertion into SDH1. Both mutants showed strongly decreased SA-inducible stress promoter responses and low SDH maximum capacity compared to wild type, while dsr1 also showed low succinate affinity, low catalytic efficiency, and increased resistance to SDH competitive inhibitors. The SA-induced promoter responses could be partially rescued in sdhaf2, but not in dsr1, by supplementing the plant growth media with succinate. Kinetic characterization showed that low concentrations of either SA or ubiquinone binding site inhibitors increased SDH activity and induced mitochondrial H 2 O 2 production. Both dsr1 and sdhaf2 showed lower rates of SA-dependent H 2 O 2 production in vitro in line with their low SA-dependent stress signaling responses in vivo. This provides quantitative and kinetic evidence that SA acts at or near the ubiquinone binding site of SDH to stimulate activity and contributes to plant stress signaling by increased rates of mitochondrial H 2 O 2 production, leading to part of the SA-dependent transcriptional response in plant cells.

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The Arabidopsis NPR1 Protein Is a Receptor for the Plant Defense Hormone Salicylic Acid

Cited by 729 publications

References 45 publications

Salicylic acid interferes with clathrin-mediated endocytic protein trafficking

Salicylic acid interferes with clathrin-mediated endocytic protein trafficking

On plant defense signaling networks and early land plant evolution

Salicylic Acid-Dependent Plant Stress Signaling via Mitochondrial Succinate Dehydrogenase

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