Metabolic priming by a secreted fungal effector

Djamei, Armin; Schipper, Kerstin; Rabe, Franziska; Ghosh, Anupama; Vincon, Volker; Kahnt, Jörg; Osorio, Sonia; Tohge, Takayuki; Fernie, Alisdair R.; Feußner, Ivo; Feussner, Kirstin; Meinicke, Peter; Stierhof, York‐Dieter; Schwarz, Heinz; Maček, Boris; Mann, Matthias; Kahmann, Regine

doi:10.1038/nature10454

Cited by 517 publications

(536 citation statements)

References 37 publications

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“…P. syringae type III effectors can alter the accumulation of chorismate-and Phe-derived metabolites (Jelenska et al, 2007;Zhou et al, 2011). U. maydis deploys effectors that suppress SA production (Djamei et al, 2011) and promote anthocyanin production (Tanaka et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

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Perturbation of Maize Phenylpropanoid Metabolism by an AvrE Family Type III Effector fromPantoea stewartii

et al. 2015

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Republic of Korea (S.-M.P., M.G.K.)AvrE family type III effector proteins share the ability to suppress host defenses, induce disease-associated cell death, and promote bacterial growth. However, despite widespread contributions to numerous bacterial diseases in agriculturally important plants, the mode of action of these effectors remains largely unknown. WtsE is an AvrE family member required for the ability of Pantoea stewartii ssp. stewartii (Pnss) to proliferate efficiently and cause wilt and leaf blight symptoms in maize (Zea mays) plants. Notably, when WtsE is delivered by a heterologous system into the leaf cells of susceptible maize seedlings, it alone produces water-soaked disease symptoms reminiscent of those produced by Pnss. Thus, WtsE is a pathogenicity and virulence factor in maize, and an Escherichia coli heterologous delivery system can be used to study the activity of WtsE in isolation from other factors produced by Pnss. Transcriptional profiling of maize revealed the effects of WtsE, including induction of genes involved in secondary metabolism and suppression of genes involved in photosynthesis. Targeted metabolite quantification revealed that WtsE perturbs maize metabolism, including the induction of coumaroyl tyramine. The ability of mutant WtsE derivatives to elicit transcriptional and metabolic changes in susceptible maize seedlings correlated with their ability to promote disease. Furthermore, chemical inhibitors that block metabolic flux into the phenylpropanoid pathways targeted by WtsE also disrupted the pathogenicity and virulence activity of WtsE. While numerous metabolites produced downstream of the shikimate pathway are known to promote plant defense, our results indicate that misregulated induction of phenylpropanoid metabolism also can be used to promote pathogen virulence.

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Section: Discussionmentioning

confidence: 99%

“…Recent work with Ustilago maydis showed that the fungal effector Cmu1 is a chorismate mutase that attenuates SA production in infected maize (Djamei et al, 2011). We hypothesized that WtsE, through its perturbation of phenolic metabolism, might similarly suppress SA accumulation.…”

Section: Metabolic Flux Through the Shikimate Pathway And Pal Activitmentioning

confidence: 99%

Perturbation of Maize Phenylpropanoid Metabolism by an AvrE Family Type III Effector fromPantoea stewartii

et al. 2015

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“…Delivery of effectors into host cells by eukaryotic pathogens has been demonstrated in several plant pathogen systems (7)(8)(9)(10)(11)(12), and, in some cases, fungal and oomycete host-cell translocation can occur in the absence of the pathogen (7,(12)(13)(14)(15)(16), suggesting that a hostencoded transport machinery is responsible for internalization of the effectors. Conserved short N-terminal motifs such as RXLR and LXLFLAK have been identified in oomycete-effector protein families (17), and they have been shown to be both necessary and sufficient for plant-cell entry (9,16,18).…”

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confidence: 99%

Structures of the flax-rust effector AvrM reveal insights into the molecular basis of plant-cell entry and effector-triggered immunity

Williams

Catanzariti

et al. 2013

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

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Fungal and oomycete pathogens cause some of the most devastating diseases in crop plants, and facilitate infection by delivering a large number of effector molecules into the plant cell. AvrM is a secreted effector protein from flax rust (Melampsora lini) that can internalize into plant cells in the absence of the pathogen, binds to phosphoinositides (PIPs), and is recognized directly by the resistance protein M in flax (Linum usitatissimum), resulting in effector-triggered immunity. We determined the crystal structures of two naturally occurring variants of AvrM, AvrM-A and avrM, and both reveal an L-shaped fold consisting of a tandem duplicated four-helix motif, which displays similarity to the WY domain core in oomycete effectors. In the crystals, both AvrM variants form a dimer with an unusual nonglobular shape. Our functional analysis of AvrM reveals that a hydrophobic surface patch conserved between both variants is required for internalization into plant cells, whereas the C-terminal coiled-coil domain mediates interaction with M. AvrM binding to PIPs is dependent on positive surface charges, and mutations that abrogate PIP binding have no significant effect on internalization, suggesting that AvrM binding to PIPs is not essential for transport of AvrM across the plant membrane. The structure of AvrM and the identification of functionally important surface regions advance our understanding of the molecular mechanisms underlying how effectors enter plant cells and how they are detected by the plant immune system. innate immunity | plant cell internalization | plant disease resistance | avirulence protein | lipid binding F ilamentous eukaryotic microbes such as fungi and oomycetes cause devastating diseases in many economically important crop plants, including rice, corn, wheat, soybean, and potato. During infection, oomycetes and biotrophic fungal pathogens establish a physical interaction with their host through specialized feeding structures, known as haustoria, which facilitate secretion of a vast array of effector proteins to overcome plant defenses and promote host colonization (1-3). The effectors are generally highly divergent even among related species, and generally lack similarity to proteins currently available in the databases, making it difficult to predict biological function from sequence alone. Some of the effectors accumulate in the plant intercellular space (apoplast), whereas others are translocated into the host cell. At present, the host targets and virulence mechanisms of fungal and oomycete effectors are poorly understood. A subset of the planttranslocated effectors called avirulence (Avr) proteins are recognized directly or indirectly and with high specificity by plant disease resistance (R) proteins (4-6). This recognition event leads to activation of effector-triggered immunity (ETI), which usually includes rapid localized host cell death at the site of infectiontermed the hypersensitive response (HR)-and results in the plants being immune to pathogen infection.The question of how...

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“…The basic criteria to identify candidate secreted effector proteins are: proteins with a signal peptide (within the initial 60 amino acids at the N-terminus), no trans-membrane domains, small size between 300 to 450 amino acids, and mostly species-specific [32,39,40]. These parameters were those used in the identification of putative P. brassicae effectors in the previously mentioned studies (Table 1).…”

Section: Where and How To Look For Effectors?mentioning

confidence: 99%

Identification of Plasmodiophora brassicae effectors — A challenging goal

et al. 2018

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Clubroot is an economically important disease affecting Brassica plants worldwide. Plasmodiophora brassicae is the protist pathogen associated with the disease, and its soil-borne obligate parasitic nature has impeded studies related to its biology and the mechanisms involved in its infection of the plant host. The identification of effector proteins is key to understanding how the pathogen manipulates the plant’s immune response and the genes involved in resistance. After more than 140 years studying clubroot and P. brassicae, very little is known about the effectors playing key roles in the infection process and subsequent disease progression. Here we analyze the information available for identified effectors and suggest several features of effector genes that can be used in the search for others. Based on the information presented in this review, we propose a comprehensive bioinformatics pipeline for effector identification and provide a list of the bioinformatics tools available for such.

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Metabolic priming by a secreted fungal effector

Cited by 517 publications

References 37 publications

Perturbation of Maize Phenylpropanoid Metabolism by an AvrE Family Type III Effector fromPantoea stewartii

Perturbation of Maize Phenylpropanoid Metabolism by an AvrE Family Type III Effector fromPantoea stewartii

Structures of the flax-rust effector AvrM reveal insights into the molecular basis of plant-cell entry and effector-triggered immunity

Identification of Plasmodiophora brassicae effectors — A challenging goal

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