Mechanisms of Nuclear Suppression of Host Immunity by Effectors from the Arabidopsis Downy Mildew Pathogen Hyaloperonospora arabidopsidis (Hpa)

Caillaud, Marie‐Cécile; Wirthmueller, Lennart; Fabro, Georgina; Piquerez, Sophie J. M.; Asai, Shuji; Ishaque, Naveed; Jones, Jonathan D. G.

doi:10.1101/sqb.2012.77.015115

Cited by 19 publications

(17 citation statements)

References 73 publications

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“…A significant number of host-targeted pathogen effector proteins localize entirely to host cell nuclei, indicating active nuclear import or passive diffusion through the NPC and sequestration in the nucleus (Deslandes and Rivas, 2011; Caillaud et al, 2012a,b). Generally, nuclear localization correlates with NLS motifs in the primary sequence suggesting that these effectors exploit the host cell’s nuclear import machinery for nuclear translocation.…”

Section: Hold On Tight - Nuclear Pathogen Effectors and The Importin-mentioning

confidence: 99%

Hop-on hop-off: importin-α-guided tours to the nucleus in innate immune signaling

Wirthmueller¹,

Roth²,

Banfield³

et al. 2013

Front. Plant Sci.

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Nuclear translocation of immune regulatory proteins and signal transducers is an essential process in animal and plant defense signaling against pathogenic microbes. Import of proteins containing a nuclear localization signal (NLS) into the nucleus is mediated by nuclear transport receptors termed importins, typically dimers of a cargo-binding α-subunit and a β-subunit that mediates translocation through the nuclear pore complex. Here, we review recent reports of importin-α cargo specificity and mutant phenotypes in plant- and animal–microbe interactions. Using homology modeling of the NLS-binding cleft of nine predicted Arabidopsis α-importins and analyses of their gene expression patterns, we discuss functional redundancy and specialization within this transport receptor family. In addition, we consider how pathogen effector proteins that promote infection by manipulating host cell nuclear processes might compete with endogenous cargo proteins for nuclear uptake.

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Section: Hold On Tight - Nuclear Pathogen Effectors and The Importin-mentioning

confidence: 99%

Hop-on hop-off: importin-α-guided tours to the nucleus in innate immune signaling

Wirthmueller¹,

Roth²,

Banfield³

et al. 2013

Front. Plant Sci.

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“…During invasion of host cells haustoria become enveloped by a highly modified host‐derived membrane, the extrahaustorial membrane (EHM), which separates the haustorium from the host cytoplasm. The EHM provides a pivotal interface for the uptake of nutrients and water from the host and for the delivery of effector proteins secreted by the fungus to manipulate host cells (Bozkurt et al ., ; Caillaud et al ., ). The EHM is continuous with the plant plasma membrane but has a markedly different structure and composition.…”

Section: Introductionmentioning

confidence: 97%

The powdery mildew resistance protein RPW8.2 is carried on VAMP721/722 vesicles to the extrahaustorial membrane of haustorial complexes

et al. 2014

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Plants employ multiple cell-autonomous defense mechanisms to impede pathogenesis of microbial intruders. Previously we identified an exocytosis defense mechanism in Arabidopsis against pathogenic powdery mildew fungi. This pre-invasive defense mechanism depends on the formation of ternary protein complexes consisting of the plasma membrane-localized PEN1 syntaxin, the adaptor protein SNAP33 and closely sequence-related vesicle-resident VAMP721 or VAMP722 proteins. The Arabidopsis thaliana resistance to powdery mildew 8.2 protein (RPW8.2) confers disease resistance against powdery mildews upon fungal entry into host cells and is specifically targeted to the extrahaustorial membrane (EHM), which envelops the haustorial complex of the fungus. However, the secretory machinery involved in trafficking RPW8.2 to the EHM is unknown. Here we report that RPW8.2 is transiently located on VAMP721/722 vesicles, and later incorporated into the EHM of mature haustoria. Resistance activity of RPW8.2 against the powdery mildew Golovinomyces orontii is greatly diminished in the absence of VAMP721 but only slightly so in the absence of VAMP722. Consistent with this result, trafficking of RPW8.2 to the EHM is delayed in the absence of VAMP721. These findings implicate VAMP721/722 vesicles as key components of the secretory machinery for carrying RPW8.2 to the plant-fungal interface. Quantitative fluorescence recovery after photobleaching suggests that vesicle-mediated trafficking of RPW8.2-yellow fluorescent protein (YFP) to the EHM occurs transiently during early haustorial development and that lateral diffusion of RPW8.2-YFP within the EHM exceeds vesicle-mediated replenishment of RPW8.2-YFP in mature haustoria. Our findings imply the engagement of VAMP721/722 in a bifurcated trafficking pathway for pre-invasive defense at the cell periphery and post-invasive defense at the EHM.

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“…Analyses of the subcellular localization of several of these so-called RXLR effectors showed that they can be found in various subcellular compartments (Caillaud et al, 2012a). Each effector seems to have its own specific destination, presumably in the close vicinity of its host target that needs to be modified or (in)activated to suppress host immunity (Caillaud et al, 2012b).…”

Section: Introductionmentioning

confidence: 99%

Immune activation mediated by the late blight resistance protein R1 requires nuclear localization of R1 and the effector AVR1

Berg

Govers

et al. 2015

New Phytologist

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SummaryResistance against oomycete pathogens is mainly governed by intracellular nucleotide-binding leucine-rich repeat (NLR) receptors that recognize matching avirulence (AVR) proteins from the pathogen, RXLR effectors that are delivered inside host cells. Detailed molecular understanding of how and where NLR proteins and RXLR effectors interact is essential to inform the deployment of durable resistance (R) genes.Fluorescent tags, nuclear localization signals (NLSs) and nuclear export signals (NESs) were exploited to determine the subcellular localization of the potato late blight protein R1 and the Phytophthora infestans RXLR effector AVR1, and to target these proteins to the nucleus or cytoplasm.Microscopic imaging revealed that both R1 and AVR1 occurred in the nucleus and cytoplasm, and were in close proximity. Transient expression of NLS-or NES-tagged R1 and AVR1 in Nicotiana benthamiana showed that activation of the R1-mediated hypersensitive response and resistance required localization of the R1/AVR1 pair in the nucleus. However, AVR1-mediated suppression of cell death in the absence of R1 was dependent on localization of AVR1 in the cytoplasm. Balanced nucleocytoplasmic partitioning of AVR1 seems to be a prerequisite.Our results show that R1-mediated immunity is activated inside the nucleus with AVR1 in close proximity and suggest that nucleocytoplasmic transport of R1 and AVR1 is tightly regulated.

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Mechanisms of Nuclear Suppression of Host Immunity by Effectors from the Arabidopsis Downy Mildew Pathogen Hyaloperonospora arabidopsidis (Hpa)

Cited by 19 publications

References 73 publications

Hop-on hop-off: importin-α-guided tours to the nucleus in innate immune signaling

Hop-on hop-off: importin-α-guided tours to the nucleus in innate immune signaling

The powdery mildew resistance protein RPW8.2 is carried on VAMP721/722 vesicles to the extrahaustorial membrane of haustorial complexes

Immune activation mediated by the late blight resistance protein R1 requires nuclear localization of R1 and the effector AVR1

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