RD19, an<i>Arabidopsis</i>Cysteine Protease Required for RRS1-R–Mediated Resistance, Is Relocalized to the Nucleus by the<i>Ralstonia solanacearum</i>PopP2 Effector

Bernoux, Maud; Timmers, Ton; Jauneau, Alain; Brière, Christian; Wit, P.J.G.M. de; Marco, Yves; Deslandes, Laurent

doi:10.1105/tpc.108.058685

Cited by 186 publications

(174 citation statements)

References 96 publications

(120 reference statements)

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“…HopI1 joins a growing list of pathogen effectors that induce and/or recruit host target proteins to a specific subcellular compartment (4,27,28). We don't know the specific importance of the induction of cytHsp70 accumulation and recruitment to chloroplasts in response to HopI1.…”

Section: Discussionmentioning

confidence: 99%

Pseudomonas syringae hijacks plant stress chaperone machinery for virulence

Jeleńska

Hal²,

Greenberg³

2010

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

150

131

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Plant heat shock protein Hsp70 is the major target of HopI1, a virulence effector of pathogenic Pseudomonas syringae. Hsp70 is essential for the virulence function of HopI1. HopI1 directly binds Hsp70 through its C-terminal J domain and stimulates Hsp70 ATP hydrolysis activity in vitro. In plants, HopI1 forms large complexes in association with Hsp70 and induces and recruits cytosolic Hsp70 to chloroplasts, the site of HopI1 localization. Deletion of a central P/Q-rich repeat region disrupts HopI1 virulence but not Hsp70 interactions or association with chloroplasts. Thus, HopI1 must not only bind Hsp70 through its J domain, but likely actively affects Hsp70 activity and/or specificity. At high temperature, HopI1 is dispensable for P. syringae pathogenicity, unless excess Hsp70 is provided. A working hypothesis is that Hsp70 has a defense-promoting activity(s) that HopI1 or high temperature can subvert. Enhanced susceptibility of Hsp70-depleted plants to nonpathogenic strains of P. syringae supports a defense-promoting role for Hsp70.T o cause a successful infection, many plant pathogenic bacteria use a type III secretion system through which dozens of different effector proteins are injected into plant cells (1). Pseudomonas syringae, a type III-requiring pathogen, causes disease on foliage and fruits of diverse plants. Some P. syringae effectors can restrict host range and/or disease potential, rendering the pathogen "avirulent," when they are recognized by a plant's defense machinery (2). However, in many cases, effectors suppress plant immune responses (1, 3). These virulence effectors are of intense interest, because their study not only gives insight into pathogenic mechanisms, but they can be used to identify previously unknown defense components (1, 4, 5) whose engineering may lead to novel approaches for creating disease-resistant plants.The P. syringae pv. maculicola ES4326 (Pma) HopI1 effector, a J protein (i.e., one that contains a J domain) suppresses accumulation of the defense regulator salicylic acid (SA) and related plant defenses (6). HopI1 localizes to chloroplasts where SA is synthesized (7) and also affects thylakoid stack structure within chloroplasts (6). HopI1-expressing plants can rescue the virulence defect of PmaΔhopI1 bacteria, indicating that HopI1 exerts its effects from within plant cells. All pathogenic P. syringae examined have a HopI1 allele with a conserved 190-amino acid N-terminal region of unknown function, a middle region with variable numbers of P/Q-rich 37/38 amino acid repeats (1-6) and a conserved 70-amino acid J domain. Several alleles with different repeat numbers can complement the virulence defect of PmaΔhopI1, indicating they all function similarly (6).The J domain of HopI1 provides a clue to HopI1's possible mechanism of action. J proteins bind Hsp70 through the J domain and stimulate Hsp70's ATP hydrolysis activity as well as other activities such as de novo folding of client proteins, intervening when proteins are improperly folded-often during stress conditions...

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Section: Discussionmentioning

confidence: 99%

Pseudomonas syringae hijacks plant stress chaperone machinery for virulence

Jeleńska

Hal²,

Greenberg³

2010

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

150

131

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“…However, the exact physiological function of the nuclear EhCP4 is not clear. At least five cysteine proteinases in higher eukaryotic cells have been shown to have nuclear localization: a cathepsin L isoform missing its regular signal peptide (48,49), a cathepsin B-like cysteine proteinase (50), cathepsin F (51), mouse cathepsin 7 (52), and a plant papain-like cysteine proteinase RD19 (53). These enzymes regulate events such as DNA replication, chromatin assembly, activation or deactivation of transcription factors, and cell cycle-related proteins.…”

Section: Discussionmentioning

confidence: 99%

A Novel Entamoeba histolytica Cysteine Proteinase, EhCP4, Is Key for Invasive Amebiasis and a Therapeutic Target

Nora

Schneider

et al. 2010

Journal of Biological Chemistry

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Entamoeba histolytica cysteine proteinases (EhCPs) play a key role in disrupting the colonic epithelial barrier and the innate host immune response during invasion of E. histolytica, the protozoan cause of human amebiasis. EhCPs are encoded by 50 genes, of which ehcp4 (ehcp-a4) is the most up-regulated during invasion and colonization in a mouse cecal model of amebiasis. Up-regulation of ehcp4 in vivo correlated with our finding that co-culture of E. histolytica trophozoites with mucin-producing T84 cells increased ehcp4 expression up to 6-fold. We have expressed recombinant EhCP4, which was autocatalytically activated at acidic pH but had highest proteolytic activity at neutral pH. In contrast to the other amebic cysteine proteinases characterized so far, which have a preference for arginine in the P2 position, EhCP4 displayed a unique preference for valine and isoleucine at P2. This preference was confirmed by homology modeling, which revealed a shallow, hydrophobic S2 pocket. Endogenous EhCP4 localized to cytoplasmic vesicles, the nuclear region, and perinuclear endoplasmic reticulum (ER). Following co-culture with colonic cells, EhCP4 appeared in acidic vesicles and was released extracellularly. A specific vinyl sulfone inhibitor, WRR605, synthesized based on the substrate specificity of EhCP4, inhibited the recombinant enzyme in vitro and significantly reduced parasite burden and inflammation in the mouse cecal model. The unique expression pattern, localization, and biochemical properties of EhCP4 could be exploited as a potential target for drug design.

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“…A host protein, the Cys protease RD19, directly interacts with PopP2. In the presence of PopP2, the RD19 protein changes its localization from the putative prevacuolar vesicles to the nucleus (Bernoux et al, 2008). A GFP-fused version of the Arabidopsis resistance protein RRS1-R could not be detected in the absence of PopP2 (its cognate elicitor), but when RRS1-R was coexpressed with PopP2, both colocalized in the nucleus (Deslandes et al, 2003).…”

Section: Rx1 Is Activated In the Cytoplasmic Compartmentmentioning

confidence: 99%

Nucleocytoplasmic Distribution Is Required for Activation of Resistance by the Potato NB-LRR Receptor Rx1 and Is Balanced by Its Functional Domains

Slootweg¹,

Roosien²,

et al. 2010

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The Rx1 protein, as many resistance proteins of the nucleotide binding-leucine-rich repeat (NB-LRR) class, is predicted to be cytoplasmic because it lacks discernable nuclear targeting signals. Here, we demonstrate that Rx1, which confers extreme resistance to Potato virus X, is located both in the nucleus and cytoplasm. Manipulating the nucleocytoplasmic distribution of Rx1 or its elicitor revealed that Rx1 is activated in the cytoplasm and cannot be activated in the nucleus. The coiled coil (CC) domain was found to be required for accumulation of Rx1 in the nucleus, whereas the LRR domain promoted the localization in the cytoplasm. Analyses of structural subdomains of the CC domain revealed no autonomous signals responsible for active nuclear import. Fluorescence recovery after photobleaching and nuclear fractionation indicated that the CC domain binds transiently to large complexes in the nucleus. Disruption of the Rx1 resistance function and protein conformation by mutating the ATP binding phosphate binding loop in the NB domain, or by silencing the cochaperone SGT1, impaired the accumulation of Rx1 protein in the nucleus, while Rx1 versions lacking the LRR domain were not affected in this respect. Our results support a model in which interdomain interactions and folding states determine the nucleocytoplasmic distribution of Rx1.

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RD19, anArabidopsisCysteine Protease Required for RRS1-R–Mediated Resistance, Is Relocalized to the Nucleus by theRalstonia solanacearumPopP2 Effector

Cited by 186 publications

References 96 publications

Pseudomonas syringae hijacks plant stress chaperone machinery for virulence

Pseudomonas syringae hijacks plant stress chaperone machinery for virulence

A Novel Entamoeba histolytica Cysteine Proteinase, EhCP4, Is Key for Invasive Amebiasis and a Therapeutic Target

Nucleocytoplasmic Distribution Is Required for Activation of Resistance by the Potato NB-LRR Receptor Rx1 and Is Balanced by Its Functional Domains

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