A Yersinia Effector and a Pseudomonas Avirulence Protein Define a Family of Cysteine Proteases Functioning in Bacterial Pathogenesis

Shao, Feng; Merritt, Peter M.; Bao, Zhao-Qin; Innes, Roger W.; Dixon, Jack E.

doi:10.1016/s0092-8674(02)00766-3

Cited by 413 publications

(400 citation statements)

References 54 publications

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“…In susceptible host plants, expression of type III effectors may induce disease-like symptoms (Kjemtrup et al, 2000). In other plants that carry appropriate resistance genes, expression of type III effectors elicits hypersensitive responses (Gopalan et al, 1996;Leister et al, 1996;van den Ackerveken et al, 1996;Shao et al, 2002). Here, we report that constitutive expression of the nopL gene in planta blocks inducible plant defense responses.…”

Section: Discussionmentioning

confidence: 51%

NopL, an Effector Protein ofRhizobiumsp. NGR234, Thwarts Activation of Plant Defense Reactions

et al. 2004

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Bacterial effector proteins delivered into eukaryotic cells via bacterial type III secretion systems are important virulence factors in plant-pathogen interactions. Type III secretion systems have been found in Rhizobium species that form symbiotic, nitrogen-fixing associations with legumes. One such bacterium, Rhizobium sp. NGR234, secretes a number of type III effectors, including nodulation outer protein L (NopL, formerly y4xL). Here, we show that expression of nopL in tobacco (Nicotiana tabacum) prevents full induction of pathogenesis-related (PR) defense proteins. Transgenic tobacco plants that express nopL and were infected with potato virus Y (necrotic strain 605) exhibited only very low levels of chitinase (class I) and ␤-1,3-glucanase (classes I and III) proteins. Northern-blot analysis indicated that expression of nopL in plant cells suppresses transcription of PR genes. Treatment with ethylene counteracted the effect of NopL on chitinase (class I). Transgenic Lotus japonicus plants that expressed nopL exhibited delayed development and low chitinase levels. In vitro experiments showed that NopL is a substrate for plant protein kinases. Together, these data suggest that NopL, when delivered into the plant cell, modulates the activity of signal transduction pathways that culminate in activation of PR proteins.Plants have evolved many defenses against invading pathogens. Among them are preformed antimicrobial compounds, as well as inducible defense proteins, the so-called pathogenesis-related (PR) proteins (van Loon, 1997). It has been shown, for example, that pathogen-induced chitinases (EC 3.2.1.14) and ␤-1,3-glucanases (EC 3.2.1.39) synergistically lyse fungal cell walls (Mauch et al., 1988). Specific recognition of pathogens often induces a hypersensitive response, which is characterized by an oxidative burst and localized death of the host cells. In most cases, the induction of a hypersensitive response arrests invasion by the pathogen (Dangl and Jones, 2001).Virulence in gram-negative bacteria often depends on proteins injected into eukaryotic cells. Some bacteria elaborate a specialized protein secretion apparatus, the type III secretion system (TTSS). The TTSS exports a set of proteins from the bacteria, some of which are delivered directly into the eukaryotic cells-a process called translocation (Cornelis and van Gijsegem, 2000;Plano et al., 2001). Most translocated type III effectors act on the cytoskeleton or interfere with intracellular signaling cascades of the host cell. Yersinia pestis, for example, injects at least six type III effectors into host cells, where they thwart the signaling machinery of the immune system (Cornelis, 2002). Plant pathogens such as Pseudomonas syringae and Xanthomonas campestris also use TTSSs (Kjemtrup et al., 2000; Lahaye and Bonas, 2001). Mounting evidence suggests that type III effectors translocated into plant cells (Casper-Lindley et al., 2002;Szurek et al., 2002) act as virulence factors in susceptible hosts. One likely function of type III effectors is ...

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Section: Discussionmentioning

confidence: 51%

NopL, an Effector Protein ofRhizobiumsp. NGR234, Thwarts Activation of Plant Defense Reactions

et al. 2004

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“…Bacterial plant pathogens were shown to introduce effectors into the plant cell acting as pathogenicity factors (Abramovitch et al, 2003). The Pseudomonas avirulence protein AvrPphB is a homologue of the Yersinia effector YopT that works as a protease cleaving small G-proteins (Shao et al, 2002). It is imaginable that Bgh also effects the host RAC/ROP-signalling pathways to more easily infect the plant cell.…”

Section: Discussionmentioning

confidence: 99%

Functional analysis of barley RAC/ROP G‐protein family members in susceptibility to the powdery mildew fungus

et al. 2003

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SummarySmall monomeric G-proteins of the plant ras (rat sarcome oncogene product) related C3 botulinum toxin substrate (RAC)/Rho of plants (ROP) family are molecular switches in signal transduction of many cellular processes. RAC/ROPs regulate hormone effects, subcellular gradients of Ca 2 , the organisation of the actin cytoskeleton and the production of reactive oxygen intermediates. Therefore, we followed a genetic bottom-up strategy to study the role of these proteins during the interaction of barley (Hordeum vulgare L.) with the fungal biotrophic pathogen Blumeria graminis f.sp. hordei (Bgh). We identi®ed six barley RAC/ ROP proteins and studied their gene expression. Five out of six Rac/Rop genes were expressed constitutively in the leaf epidermis, which is the site of interaction with Bgh. None of the genes showed enhancement of mRNA abundance after inoculation with Bgh. After microprojectile mediated transformation of single barley epidermal cells with constitutively activated mutant RAC/ROP proteins, we found an RAC/ ROP-speci®c enhancement of pathogen accessibility, tagging HvRACB, HvRAC3 and HvROP6 as host proteins potentially involved in the establishment of susceptibility to Bgh. Confocal laser scanning microscopy (CLSM) of green¯uorescent protein (GFP):HvRAC/ROP-transformed cells revealed varying strengths of plasma membrane association of barley RAC/ROPs. The C-terminal CAAX motif for presumable prenylation or the C-terminal hypervariable region (HVR), respectively, were required for membrane association of the RAC/ROPs. Proper intracellular localisation was essential for HvRACB and HvRAC3 function. Together, our data support the view that different paths of host signal transduction via RAC/ROP G-proteins are involved in processes supporting parasitic entry into epidermal host cells.

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“…Other toxins influence the activity of Rho GTPases by mimicry of endogenous GAP activity, e.g., Yersinia YopE (von PawelRammingen et al 2000), Salmonella SptP (Fu and Galan 1999), Pseudomonas aeruginosa ExoS (Goehring et al 1999) or endogenous GEF activity, e.g., Salmonella SopE (Hardt et al 1998). Finally, it has been shown recently that Rho GTPase were cleaved proteolytically at the C-terminal isoprenylated cysteine by Yersinia YopT and thereby inactivated (Shao et al 2002(Shao et al , 2003.…”

Section: The Targets Of C3-like Exoenzymes Are Molecular Switchesmentioning

confidence: 99%

C3 exoenzymes, novel insights into structure and action of Rho-ADP-ribosylating toxins

Vogelsgesang

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Aktories

2006

Naunyn-Schmied Arch Pharmacol

100

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The family of C3-like exoenzymes comprises seven bacterial ADP-ribosyltransferases of different origin. The common hallmark of these exoenzymes is the selective N-ADP-ribosylation of the low molecular mass GTPbinding proteins RhoA, B, and C and inhibition of signal pathways controlled by Rho GTPases. Therefore, C3-like exoenzymes were applied as pharmacological tools for analyses of cellular functions of Rho protein in numerous studies. Recent structural and functional analyses of C3-like exoenzymes provide detailed information on the molecular mechanisms and functional consequences of ADP-ribosylation catalyzed by these toxins. More recently additional non-enzymatic actions of C3-like ADP-ribosyltransferases have been identified showing that C3 transferases from Clostridium botulinum and Clostridium limosum form a GDI-like complex with the Ras-like low molecular mass GTPase Ral without ADP-ribosylation. These results add novel information on the molecular mode of action(s) of C3-like exoenzymes and are discussed in this review.

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A Yersinia Effector and a Pseudomonas Avirulence Protein Define a Family of Cysteine Proteases Functioning in Bacterial Pathogenesis

Cited by 413 publications

References 54 publications

NopL, an Effector Protein ofRhizobiumsp. NGR234, Thwarts Activation of Plant Defense Reactions

NopL, an Effector Protein ofRhizobiumsp. NGR234, Thwarts Activation of Plant Defense Reactions

Functional analysis of barley RAC/ROP G‐protein family members in susceptibility to the powdery mildew fungus

C3 exoenzymes, novel insights into structure and action of Rho-ADP-ribosylating toxins

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