Repertoire, unified nomenclature and evolution of the Type III effector gene set in the Ralstonia solanacearum species complex

Peeters, Nemo; Carrère, Sébastien; Anisimova, Maria; Plener, Laure; Cazalé, Anne‐Claire; Genin, Stéphane

doi:10.1186/1471-2164-14-859

Cited by 204 publications

(295 citation statements)

References 69 publications

(147 reference statements)

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“…This hypothesis is in accordance with a polymutant approach in Pst DC3000 which highlighted a consortium of redundant translocators required to promote Pst T3E injection into plant cells (61,62). RipF1, RipW, RipX, RipAB, and RipAM all belong to the R. solanacearum core effectome (11). It will be of particular interest to study more precisely how they take part in the formation of the Hrp translocation apparatus as acces- sory cotranslocators, notably by looking for interactions between them and the HrpY pilin.…”

Section: Discussionsupporting

confidence: 83%

“…3B). These experiments showed that RSp0213 encodes a T3E, which was therefore renamed RipBJ following the proposed nomenclature for R. solanacearum T3Es (11). A ripBJ disruption mutant was generated and used to evaluate the contribution of this effector to pathogenicity on A. thaliana and M. truncatula, and to hypersensitive response (HR) elicitation after infiltration of tobacco leaves.…”

Section: ϫ34mentioning

confidence: 99%

“…solanacearum strains possess large T3E repertoires, with 72 Rips (Ralstonia injected proteins) identified in the model strain GMI1000 (11). Rip delivery through the T3SS is under a fine transcriptional control, orchestrated by the regulatory protein HrpB.…”

mentioning

confidence: 99%

“…The R. solanacearum T3SS transcriptional regulatory system is well described (13), whereas little is known about the post-translational control of Rip delivery. There were 94 Rip genes identified among strains of the R. solanacearum species complex sequenced to date (11). This large repertoire of virulence factors may explain the wide host range of this bacterium.…”

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confidence: 99%

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Comparative Secretome Analysis of Ralstonia solanacearum Type 3 Secretion-Associated Mutants Reveals a Fine Control of Effector Delivery, Essential for Bacterial Pathogenicity

Lonjon

Turner

Henry

et al. 2016

Molecular & Cellular Proteomics

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Ralstonia solanacearum, the causal agent of bacterial wilt, exerts its pathogenicity through more than a hundred secreted proteins, many of them depending directly on the functionality of a type 3 secretion system. To date, only few type 3 effectors have been identified as required for bacterial pathogenicity, notably because of redundancy among the large R. solanacearum effector repertoire. In order to identify groups of effectors collectively promoting disease on susceptible hosts, we investigated the role of putative post-translational regulators in the control of type 3 secretion. A shotgun secretome analysis with label-free quantification using tandem mass spectrometry was performed on the R. solanacearum GMI1000 strain. There were 228 proteins identified, among which a large proportion of type 3 effectors, called Rip (Ralstonia injected proteins). Thanks to this proteomic approach, RipBJ was identified as a new effector specifically secreted through type 3 secretion system and translocated into plant cells. A focused Rip secretome analysis using hpa (hypersensitive response and pathogenicity associated) mutants revealed a fine secretion regulation and specific subsets of Rips with different secretion patterns. We showed that a set of Rips (RipF1, RipW, RipX, RipAB, and RipAM) are secreted in an Hpa-independent manner. We hypothesize that these Rips could be preferentially involved in the first stages of type 3 secretion. In addition, the secretion of about thirty other Rips is controlled by HpaB and HpaG. HpaB, a candidate chaperone was shown to positively control secretion of numerous Rips, whereas HpaG was shown to act as a negative regulator of secretion. To evaluate the impact of altered type 3 effectors secretion on plant pathogenesis, the hpa mutants were assayed on several host plants. HpaB was required for bacterial pathogenicity on multiple hosts whereas HpaG was found to be specifically required for full R. solanacearum pathogenicity on the legume plant Medicago truncatula. Molecular & Cellular Proteomics 15: 10.1074/ mcp.M115.051078, 598-613, 2016.The soil-borne vascular bacterium R. solanacearum is described as one of the most destructive plant pathogenic bacterium worldwide (1), mainly because of its broad host range and wide geographic distribution. Indeed, R. solanacearum attacks more than 250 plant species, distributed in more than 50 botanical families (2). R. solanacearum causes dramatic crop losses, more specifically in the tropics, notably affecting emerging countries. Durable protection strategies against this bacterium are lacking. R. solanacearum penetrates into the plant via the roots, and then colonizes the xylem vessels. The bacterium reaches the aerial parts of the plant, causes wilting symptoms leading to the death of the plant, and will eventually return to the soil, completing the cycle (3). To achieve these first colonization steps, the bacterium uses a molecular syringe called the type 3 secretion system (T3SS), 1 which deFrom the ‡INRA, Laboratoire des Interactions Plantes-...

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Section: Discussionsupporting

confidence: 83%

Section: ϫ34mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Comparative Secretome Analysis of Ralstonia solanacearum Type 3 Secretion-Associated Mutants Reveals a Fine Control of Effector Delivery, Essential for Bacterial Pathogenicity

Lonjon

Turner

Henry

et al. 2016

Molecular & Cellular Proteomics

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“…Individual R. solanacearum strains typically possess around 60 -75 effectors. Effector repertoire comparison revealed a group of 32 core effectors present in 10 of 11 strains (13). To date, only a few R. solanacearum effectors have been assigned molecular functions and targets (14 -16), but most of these effectors remain functionally uncharacterized.…”

mentioning

confidence: 99%

RipAY, a Plant Pathogen Effector Protein, Exhibits Robust γ-Glutamyl Cyclotransferase Activity When Stimulated by Eukaryotic Thioredoxins

Fujiwara

Kawazoe

Ohnishi

et al. 2016

Journal of Biological Chemistry

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The plant pathogenic bacterium Ralstonia solanacearum injects more than 70 effector proteins (virulence factors) into the host plant cells via the needle-like structure of a type III secretion system. The type III secretion system effector proteins manipulate host regulatory networks to suppress defense responses with diverse molecular activities. Uncovering the molecular function of these effectors is essential for a mechanistic understanding of R. solanacearum pathogenicity. However, few of the effectors from R. solanacearum have been functionally characterized, and their plant targets remain largely unknown. Here, we show that the ChaC domain-containing effector RipAY/RSp1022 from R. solanacearum exhibits ␥-glutamyl cyclotransferase (GGCT) activity to degrade the major intracellular redox buffer, glutathione. Heterologous expression of RipAY, but not other ChaC family proteins conserved in various organisms, caused growth inhibition of yeast Saccharomyces cerevisiae, and the intracellular glutathione level was decreased to ϳ30% of the normal level following expression of RipAY in yeast. Although active site mutants of GGCT activity were non-toxic, the addition of glutathione did not reverse the toxicity, suggesting that the toxicity might be a consequence of activity against other ␥-glutamyl compounds. Intriguingly, RipAY protein purified from a bacterial expression system did not exhibit any GGCT activity, whereas it exhibited robust GGCT activity upon its interaction with eukaryotic thioredoxins, which are important for intracellular redox homeostasis during bacterial infection in plants. Our results suggest that RipAY has evolved to sense the host intracellular redox environment, which triggers its enzymatic activity to create a favorable environment for R. solanacearum infection.

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Trophic preferences of the pathogen Ralstonia solanacearum and consequences on its growth in xylem sap

2022

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Ralstonia solanacearum is one of the most destructive pathogens worldwide. In the last 30 years, the molecular mechanisms at the origin of R. solanacearum pathogenicity have been studied in depth. However, the nutrition status of the pathogen once inside the plant has been poorly investigated. Yet, the pathogen needs substrates to sustain a fast‐enough growth, maintain its virulence and subvert the host immunity. This study aimed to explore in‐depth the xylem environment where the pathogen is abundant, and its trophic preferences. First, we determined the composition of tomato xylem sap, where fast multiplication of the pathogen occurs. Then, kinetic growth on single and mixtures of carbon sources in relation to this environment was performed to fully quantify growth. Finally, we calculated the concentration of available metabolites in the xylem sap flux to assess how much it can support bacterial growth in planta . Overall, the study underlines the adaptation of R. solanacearum to the xylem environment and the fact that the pathogen assimilates several substrates at the same time in media composed of several carbon sources. It also provides metrics on key physiological parameters governing the growth of this major pathogen, which will be instrumental in the future to better understand its metabolic behavior during infection.

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Repertoire, unified nomenclature and evolution of the Type III effector gene set in the Ralstonia solanacearum species complex

Cited by 204 publications

References 69 publications

Comparative Secretome Analysis of Ralstonia solanacearum Type 3 Secretion-Associated Mutants Reveals a Fine Control of Effector Delivery, Essential for Bacterial Pathogenicity

Comparative Secretome Analysis of Ralstonia solanacearum Type 3 Secretion-Associated Mutants Reveals a Fine Control of Effector Delivery, Essential for Bacterial Pathogenicity

RipAY, a Plant Pathogen Effector Protein, Exhibits Robust γ-Glutamyl Cyclotransferase Activity When Stimulated by Eukaryotic Thioredoxins

Trophic preferences of the pathogen Ralstonia solanacearum and consequences on its growth in xylem sap

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