Hierarchy and Roles of Pathogen-Associated Molecular Pattern-Induced Responses in <i>Nicotiana benthamiana</i>

Segonzac, Cécile; Feike, Doreen; Giménez-Ibáñez, Selena; Hann, Dagmar R.; Zipfel, Cyril; Rathjen, John P.

doi:10.1104/pp.110.171249

Cited by 190 publications

(220 citation statements)

References 88 publications

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“…Together, these results suggest that IOS1 is required for full MPK activation, but not for the ROS burst after MAMP perception. This observation is consistent with these responses being uncoupled (Segonzac et al, 2011;Xu et al, 2014a). However, since we do not provide a kinetic analysis, we cannot exclude a slower or faster MPK response in ios1 mutants or OE lines, respectively.…”

Section: Ios1 Modulates Several Early Pti Responsessupporting

confidence: 68%

Retraction

2015

The Plant Cell

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The authors of the above article request that it be retracted from The Plant Cell and issue the following statement:After publication of the article, we discovered irregularities and inappropriate data manipulation in Figure 6C produced by the first author Ching-Wei Chen from the Zimmerli laboratory. Specifically, the same blot image improperly appears twice in Figure 6, once in Figure 6A corresponding to the IP: a-GFP blot for FLS2-GFP and again in Figure 6C as IP: a-GFP for CERK1-GFP. We repeated these experiments but found that the original results associated with Figure 6C could not be replicated and instead suggest the potential for interaction between IOS1 and CERK1 in vivo in Nicotiana benthamiana. This raises questions about some of the conclusions of the article, and we feel the best course of action is to retract the article. We believe a major conclusion of the article remains unaffected, namely, that IOS1 is involved in the regulation of flg22-and elf18-triggered responses. However, we cannot rule out an additional role for IOS1 in mediating signaling by CERK1. We are undertaking follow-up experiments to verify the major findings and clarify the role of IOS1 in plant immunity signaling.www.plantcell.org/cgi/doi/10.1105/tpc.15.00374The Plant Cell, Vol. 27: 1563, May 2015 Plasma membrane-localized pattern recognition receptors (PRRs) such as FLAGELLIN SENSING2 (FLS2), EF-TU RECEPTOR (EFR), and CHITIN ELICITOR RECEPTOR KINASE1 (CERK1) recognize microbe-associated molecular patterns (MAMPs) to activate pattern-triggered immunity (PTI). A reverse genetics approach on genes responsive to the priming agent b-aminobutyric acid (BABA) revealed IMPAIRED OOMYCETE SUSCEPTIBILITY1 (IOS1) as a critical PTI player. Arabidopsis thaliana ios1 mutants were hypersusceptible to Pseudomonas syringae bacteria. Accordingly, ios1 mutants showed defective PTI responses, notably delayed upregulation of the PTI marker gene FLG22-INDUCED RECEPTOR-LIKE KINASE1, reduced callose deposition, and mitogen-activated protein kinase activation upon MAMP treatment. Moreover, Arabidopsis lines overexpressing IOS1 were more resistant to bacteria and showed a primed PTI response. In vitro pull-down, bimolecular fluorescence complementation, coimmunoprecipitation, and mass spectrometry analyses supported the existence of complexes between the membrane-localized IOS1 and BRASSINOSTEROID INSENSITIVE1-ASSOCIATED KINASE1 (BAK1)-dependent PRRs FLS2 and EFR, as well as with the BAK1-independent PRR CERK1. IOS1 also associated with BAK1 in a ligand-independent manner and positively regulated FLS2-BAK1 complex formation upon MAMP treatment. In addition, IOS1 was critical for chitinmediated PTI. Finally, ios1 mutants were defective in BABA-induced resistance and priming. This work reveals IOS1 as a novel regulatory protein of FLS2-, EFR-, and CERK1-mediated signaling pathways that primes PTI activation. INTRODUCTIONPlants possess multilayered recognition systems that detect pathogens at various stages of infection and proliferation. Recognition of m...

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Section: Ios1 Modulates Several Early Pti Responsessupporting

confidence: 68%

Retraction

2015

The Plant Cell

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“…Importantly, we observed ligand-induced internalization of PEPR1 and FLS2 after heterologous expression in Nicotiana benthamiana leaves (Fig. 1C), a suitable model plant for studying MAMP-triggered immune responses (14). In both Arabidopsis and N. benthamiana, PEPR1-YFP fusion proteins were present at the plasma membrane and relocalized into vesicles upon pep1 elicitation ( Fig.…”

Section: Resultsmentioning

confidence: 89%

Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases

Mbengue

Bourdais

Gervasi

et al. 2016

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

181

213

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Sensing of potential pathogenic bacteria is of critical importance for immunity. In plants, this involves plasma membrane-resident pattern recognition receptors, one of which is the FLAGELLIN SENSING 2 (FLS2) receptor kinase. Ligand-activated FLS2 receptors are internalized into endosomes. However, the extent to which these spatiotemporal dynamics are generally present among pattern recognition receptors (PRRs) and their regulation remain elusive. Using live-cell imaging, we show that at least three other receptor kinases associated with plant immunity, PEP RECEPTOR 1/2 (PEPR1/2) and EF-TU RECEPTOR (EFR), internalize in a ligand-specific manner. In all cases, endocytosis requires the coreceptor BRI1-ASSOCIATED KINASE 1 (BAK1), and thus depends on receptor activation status. We also show the internalization of liganded FLS2, suggesting the transport of signaling competent receptors. Trafficking of activated PRRs requires clathrin and converges onto the same endosomal vesicles that are also shared with the hormone receptor BRASSINOSTERIOD INSENSITIVE 1 (BRI1). Importantly, clathrin-dependent endocytosis participates in plant defense against bacterial infection involving FLS2-mediated stomatal closure and callose deposition, but is uncoupled from activation of the flagellin-induced oxidative burst and MAP kinase signaling. In conclusion, immunity mediated by pattern recognition receptors depends on clathrin, a critical component for the endocytosis of signaling competent receptors into a common endosomal pathway.pattern-triggered immunity | clathrin | FLS2 | PEPR1 | EFR

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“…NbRBOHB-derived ROS play a positive role in plant immunity against several plant pathogens including fungi, bacteria, and viruses (5)(6)(7)(8). Therefore, we first expected that RCNMV replication proteins would be recognized by RBOHs to trigger ROS production to inhibit viral infection, or that RCNMV replication proteins act as a suppressor of RBOHs to counteract RBOHmediated antiviral immunity.…”

Section: Resultsmentioning

confidence: 99%

“…Plant NADPH oxidase, termed RBOHs (respiratory burst oxidase homologs), localize at the plasma membrane (PM) and intracellular compartments including the Golgi apparatus (2,3) and play a key role in ROS production upon the perception of environmental stresses (4). In Nicotiana benthamiana, an RBOHB (NbRBOHB) plays important roles in ROS production triggered by microbe-associated molecular patterns (MAMPs), such as bacterial flagellin and fungal chitin, and facilitates plant immunity against biotrophic pathogens including an oomycete pathogen Phytophthola infestance and tobacco mosaic virus (5)(6)(7)(8). RBOH activity is tightly and coordinately regulated posttranslationally [e.g., activation by Ca 2+ , phosphatidic acid (PA), G proteins, or protein kinases] (9-12).…”

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confidence: 99%

Harnessing host ROS-generating machinery for the robust genome replication of a plant RNA virus

Hyodo

Hashimoto

Kuchitsu

et al. 2017

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

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As sessile organisms, plants have to accommodate to rapid changes in their surrounding environment. Reactive oxygen species (ROS) act as signaling molecules to transduce biotic and abiotic stimuli into plant stress adaptations. It is established that a respiratory burst oxidase homolog B of Nicotiana benthamiana (NbRBOHB) produces ROS in response to microbe-associated molecular patterns to inhibit pathogen infection. Plant viruses are also known as causative agents of ROS induction in infected plants; however, the function of ROS in plant-virus interactions remains obscure. Here, we show that the replication of red clover necrotic mosaic virus (RCNMV), a plant positive-strand RNA [(+)RNA] virus, requires NbRBOHB-mediated ROS production. The RCNMV replication protein p27 plays a pivotal role in this process, redirecting the subcellular localization of NbRBOHB and a subgroup II calcium-dependent protein kinase of N. benthamiana (NbCDPKiso2) from the plasma membrane to the p27-containing intracellular aggregate structures. p27 also induces an intracellular ROS burst in an RBOH-dependent manner. NbCDPKiso2 was shown to be an activator of the p27-triggered ROS accumulations and to be required for RCNMV replication. Importantly, this RBOH-derived ROS is essential for robust viral RNA replication. The need for RBOHderived ROS was demonstrated for the replication of another (+) RNA virus, brome mosaic virus, suggesting that this characteristic is true for plant (+)RNA viruses. Collectively, our findings revealed a hitherto unknown viral strategy whereby the host ROS-generating machinery is diverted for robust viral RNA replication.positive-strand RNA virus | viral RNA replication | reactive oxygen species | respiratory burst oxidase homolog | calcium-dependent protein kinase P lants have evolved complicated and sophisticated strategies to survive environmental changes. The rapid generation of reactive oxygen species (ROS) is one of the hallmarks of plant responses to various biotic and abiotic stresses (1). Plant NADPH oxidase, termed RBOHs (respiratory burst oxidase homologs), localize at the plasma membrane (PM) and intracellular compartments including the Golgi apparatus (2, 3) and play a key role in ROS production upon the perception of environmental stresses (4). In Nicotiana benthamiana, an RBOHB (NbRBOHB) plays important roles in ROS production triggered by microbe-associated molecular patterns (MAMPs), such as bacterial flagellin and fungal chitin, and facilitates plant immunity against biotrophic pathogens including an oomycete pathogen Phytophthola infestance and tobacco mosaic virus (5-8). RBOH activity is tightly and coordinately regulated posttranslationally [e.g., activation by Ca 2+ , phosphatidic acid (PA), G proteins, or protein kinases] (9-12). It has recently been shown that receptor-like cytoplasmic kinases and calciumdependent protein kinases (CDPKs) regulate RBOHs activity via direct phosphorylation or through modulating regulators of RBOHs during recognition of MAMPs via corresponding surface-loca...

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Hierarchy and Roles of Pathogen-Associated Molecular Pattern-Induced Responses in Nicotiana benthamiana

Cited by 190 publications

References 88 publications

Retraction

Retraction

Clathrin-dependent endocytosis is required for immunity mediated by pattern recognition receptor kinases

Harnessing host ROS-generating machinery for the robust genome replication of a plant RNA virus

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