Dataset Information

Pangenomic type III effector database of the plant pathogenic Ralstonia spp.

ABSTRACT: Background:The bacterial plant pathogenic Ralstonia species belong to the beta-proteobacteria class and are soil-borne pathogens causing vascular bacterial wilt disease, affecting a wide range of plant hosts. These bacteria form a heterogeneous group considered as a "species complex" gathering three newly defined species. Like many other Gram negative plant pathogens, Ralstonia pathogenicity relies on a type III secretion system, enabling bacteria to secrete/inject a large repertoire of type III effectors into their plant host cells. Type III-secreted effectors (T3Es) are thought to participate in generating a favorable environment for the pathogen (countering plant immunity and modifying the host metabolism and physiology). Methods:Expert genome annotation, followed by specific type III-dependent secretion, allowed us to improve our Hidden-Markov-Model and Blast profiles for the prediction of type III effectors. Results:We curated the T3E repertoires of 12 plant pathogenic Ralstonia strains, representing a total of 12 strains spread over the different groups of the species complex. This generated a pangenome repertoire of 102 T3E genes and 16 hypothetical T3E genes. Using this database, we scanned for the presence of T3Es in the 155 available genomes representing 140 distinct plant pathogenic Ralstonia strains isolated from different host plants in different areas of the globe. All this information is presented in a searchable database. A presence/absence analysis, modulated by a strain sequence/gene annotation quality score, enabled us to redefine core and accessory T3E repertoires.

SUBMITTER: Sabbagh CRR

PROVIDER: S-EPMC6762002 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Pangenomic type III effector database of the plant pathogenic <i>Ralstonia</i> spp.

Sabbagh Cyrus Raja Rubenstein CRR Carrere Sebastien S Lonjon Fabien F Vailleau Fabienne F Macho Alberto P AP Genin Stephane S Peeters Nemo N

PeerJ 20190806

<h4>Background</h4>The bacterial plant pathogenic <i>Ralstonia</i> species belong to the beta-proteobacteria class and are soil-borne pathogens causing vascular bacterial wilt disease, affecting a wide range of plant hosts. These bacteria form a heterogeneous group considered as a "species complex" gathering three newly defined species. Like many other Gram negative plant pathogens, <i>Ralstonia</i> pathogenicity relies on a type III secretion system, enabling bacteria to secrete/inject a large ...[more]

PMID: 31579561

Similar Datasets

Project description:The plant pathogen Ralstonia solanacearum possesses two genes encoding a trehalose-6-phosphate synthase (TPS), an enzyme of the trehalose biosynthetic pathway. One of these genes, named ripTPS, was found to encode a protein with an additional N-terminal domain which directs its translocation into host plant cells through the type 3 secretion system. RipTPS is a conserved effector in the R. solanacearum species complex, and homologues were also detected in other bacterial plant pathogens. Functional analysis of RipTPS demonstrated that this type 3 effector synthesizes trehalose-6-phosphate and identified residues essential for this enzymatic activity. Although trehalose-6-phosphate is a key signal molecule in plants that regulates sugar status and carbon assimilation, the disruption of ripTPS did not alter the virulence of R. solanacearum on plants. However, heterologous expression assays showed that this effector specifically elicits a hypersensitive-like response on tobacco that is independent of its enzymatic activity and is triggered by the C-terminal half of the protein. Recognition of this effector by the plant immune system is suggestive of a role during the infectious process.Ralstonia solanacearum, the causal agent of bacterial wilt disease, infects more than two hundred plant species, including economically important crops. The type III secretion system plays a major role in the pathogenicity of this bacterium, and approximately 70 effector proteins have been shown to be translocated into host plant cells. This study provides the first description of a type III effector endowed with a trehalose-6-phosphate synthase enzymatic activity and illustrates a new mechanism by which the bacteria may manipulate the plant metabolism upon infection. In recent years, trehalose-6-phosphate has emerged as an essential signal molecule in plants, connecting plant metabolism and development. The finding that a bacterial pathogen could induce the production of trehalose-6-phosphate in plant cells further highlights the importance of this metabolite in multiple aspects of the molecular physiology of plants.

Project description:UNLABELLED:The plant pathogen Ralstonia solanacearum uses a large repertoire of type III effector proteins to succeed in infection. To clarify the function of effector proteins in host eukaryote cells, we expressed effectors in yeast cells and identified seven effector proteins that interfere with yeast growth. One of the effector proteins, RipAY, was found to share homology with the ChaC family proteins that function as ?-glutamyl cyclotransferases, which degrade glutathione (GSH), a tripeptide that plays important roles in the plant immune system. RipAY significantly inhibited yeast growth and simultaneously induced rapid GSH depletion when expressed in yeast cells. The in vitro GSH degradation activity of RipAY is specifically activated by eukaryotic factors in the yeast and plant extracts. Biochemical purification of the yeast protein identified that RipAY is activated by thioredoxin TRX2. On the other hand, RipAY was not activated by bacterial thioredoxins. Interestingly, RipAY was activated by plant h-type thioredoxins that exist in large amounts in the plant cytosol, but not by chloroplastic m-, f-, x-, y- and z-type thioredoxins, in a thiol-independent manner. The transient expression of RipAY decreased the GSH level in plant cells and affected the flg22-triggered production of reactive oxygen species (ROS) and expression of pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) marker genes in Nicotiana benthamiana leaves. These results indicate that RipAY is activated by host cytosolic thioredoxins and degrades GSH specifically in plant cells to suppress plant immunity. IMPORTANCE:Ralstonia solanacearum is the causal agent of bacterial wilt disease of plants. This pathogen injects virulence effector proteins into host cells to suppress disease resistance responses of plants. In this article, we report a biochemical activity of R. solanacearum effector protein RipAY. RipAY can degrade GSH, a tripeptide that plays important roles in the plant immune system, with its ?-glutamyl cyclotransferase activity. The high GSH degradation activity of RipAY is considered to be a good weapon for this bacterium to suppress plant immunity. However, GSH also plays important roles in bacterial tolerance to various stresses and growth. Interestingly, RipAY has an excellent safety mechanism to prevent unwanted firing of its enzyme activity in bacterial cells because RipAY is specifically activated by host eukaryotic thioredoxins. This study also reveals a novel host plant protein acting as a molecular switch for effector activation.

Project description:The type III secretion system is required for virulence of many pathogenic bacteria. Bacterial effector proteins delivered into target host cells by this system modulate host signaling pathways and processes in a manner that promotes infection. Here, we define the activity of the effector protein OspB of the human pathogen Shigella spp., the etiological agent of shigellosis and bacillary dysentery. Using the yeast Saccharomyces cerevisiae as a model organism, we show that OspB sensitizes cells to inhibition of TORC1, the central regulator of growth and metabolism. In silico analyses reveal that OspB bears structural homology to bacterial cysteine proteases that target mammalian cell processes, and we define a conserved cysteine-histidine catalytic dyad required for OspB function. Using yeast genetic screens, we identify a crucial role for the arginine N-degron pathway in the yeast growth inhibition phenotype and show that inositol hexakisphosphate is an OspB cofactor. We find that a yeast substrate for OspB is the TORC1 component Tco89p, proteolytic cleavage of which generates a C-terminal fragment that is targeted for degradation via the arginine N-degron pathway; processing and degradation of Tco89p is required for the OspB phenotype. In all, we demonstrate that the Shigella T3SS effector OspB is a cysteine protease and decipher its interplay with eukaryotic cell processes. IMPORTANCE Shigella spp. are important human pathogens and among the leading causes of diarrheal mortality worldwide, especially in children. Virulence depends on the Shigella type III secretion system (T3SS). Definition of the roles of the bacterial effector proteins secreted by the T3SS is key to understanding Shigella pathogenesis. The effector protein OspB contributes to a range of phenotypes during infection, yet the mechanism of action is unknown. Here, we show that S. flexneri OspB possesses cysteine protease activity in both yeast and mammalian cells, and that enzymatic activity of OspB depends on a conserved cysteine-histidine catalytic dyad. We determine how its protease activity sensitizes cells to TORC1 inhibition in yeast, finding that OspB cleaves a component of yeast TORC1, and that the degradation of the C-terminal cleavage product is responsible for OspB-mediated hypersensitivity to TORC1 inhibitors. Thus, OspB is a cysteine protease that depends on a conserved cysteine-histidine catalytic dyad.

Dataset Information

Pangenomic type III effector database of the plant pathogenic Ralstonia spp.

Publications

Pangenomic type III effector database of the plant pathogenic <i>Ralstonia</i> spp.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets