scholarly journals Dual role of auxin in regulating plant defense and bacterial virulence gene expression during Pseudomonas syringae PtoDC3000 pathogenesis

2019 ◽  
Author(s):  
Arnaud T. Djami-Tchatchou ◽  
Gregory A. Harrison ◽  
Chris P. Harper ◽  
Renhou Wang ◽  
Michael J. Prigge ◽  
...  
Keyword(s):  
Gene Expression ◽  
Pseudomonas Syringae ◽  
Bacterial Growth ◽  
Plant Pathogens ◽  
Virulence Gene ◽  
Bacterial Virulence ◽  
Auxin Signaling ◽  
Host Defenses ◽  
In Planta ◽  
Virulence Gene Expression

ABSTRACTModification of host hormone biology is a common strategy used by plant pathogens to promote disease. For example, the bacterial pathogen Pseudomonas syringae strain PtoDC3000 produces the plant hormone auxin (Indole-3-acetic acid, or IAA) to promote PtoDC3000 growth in plant tissue. Previous studies suggest that auxin may promote PtoDC3000 pathogenesis through multiple mechanisms, including both suppression of salicylic acid (SA)-mediated host defenses and via an unknown mechanism that appears to be independent of SA. To test if host auxin signaling is important during pathogenesis, we took advantage of Arabidopsis thaliana lines impaired in either auxin signaling or perception. We found that disruption of auxin signaling in plants expressing an inducible dominant axr2-1 mutation resulted in decreased bacterial growth, demonstrating that host auxin signaling is required for normal susceptibility to PtoDC3000, and this phenotype was dependent on SA-mediated defenses. However, despite exhibiting decreased auxin perception, tir1 afb1 afb4 afb5 quadruple mutant plants lacking four of the six known auxin co-receptors supported increased levels of bacterial growth. This mutant also exhibited elevated IAA levels, suggesting that the increased IAA in these plants may promote PtoDC3000 growth independent of host auxin signaling, perhaps through a direct effect on the pathogen. In support of this, we found that IAA directly impacted the pathogen, by modulating expression of bacterial virulence genes, both in liquid culture and in planta. Thus, in addition to suppressing host defenses, IAA acts as a microbial signaling molecule that regulates bacterial virulence gene expression.

scholarly journals Dual Role of Auxin in Regulating Plant Defense and Bacterial Virulence Gene Expression During Pseudomonas syringae PtoDC3000 Pathogenesis

2020 ◽  
Vol 33 (8) ◽  
pp. 1059-1071 ◽  
Author(s):  
Arnaud T. Djami-Tchatchou ◽  
Gregory A. Harrison ◽  
Chris P. Harper ◽  
Renhou Wang ◽  
Michael J. Prigge ◽  
...  
Keyword(s):  
Gene Expression ◽  
Pseudomonas Syringae ◽  
Bacterial Growth ◽  
Plant Pathogens ◽  
Virulence Gene ◽  
Bacterial Virulence ◽  
Auxin Signaling ◽  
Host Defenses ◽  
In Planta ◽  
Virulence Gene Expression

Modification of host hormone biology is a common strategy used by plant pathogens to promote disease. For example, the bacterial pathogen strain Pseudomonas syringae DC3000 (PtoDC3000) produces the plant hormone auxin (indole-3-acetic acid [IAA]) to promote PtoDC3000 growth in plant tissue. Previous studies suggest that auxin may promote PtoDC3000 pathogenesis through multiple mechanisms, including both suppression of salicylic acid (SA)-mediated host defenses and via an unknown mechanism that appears to be independent of SA. To test if host auxin signaling is important during pathogenesis, we took advantage of Arabidopsis thaliana lines impaired in either auxin signaling or perception. We found that disruption of auxin signaling in plants expressing an inducible dominant axr2-1 mutation resulted in decreased bacterial growth and that this phenotype was suppressed by introducing the sid2-2 mutation, which impairs SA synthesis. Thus, host auxin signaling is required for normal susceptibility to PtoDC3000 and is involved in suppressing SA-mediated defenses. Unexpectedly, tir1 afb1 afb4 afb5 quadruple-mutant plants lacking four of the six known auxin coreceptors that exhibit decreased auxin perception, supported increased levels of bacterial growth. This mutant exhibited elevated IAA levels and reduced SA-mediated defenses, providing additional evidence that auxin promotes disease by suppressing host defense. We also investigated the hypothesis that IAA promotes PtoDC3000 virulence through a direct effect on the pathogen and found that IAA modulates expression of virulence genes, both in culture and in planta. Thus, in addition to suppressing host defenses, IAA acts as a microbial signaling molecule that regulates bacterial virulence gene expression.

scholarly journals Agrobacteria reprogram virulence gene expression by controlled release of host-conjugated signals

2019 ◽  
Vol 116 (44) ◽  
pp. 22331-22340 ◽  
Author(s):  
Chao Wang ◽  
Fuzhou Ye ◽  
Changqing Chang ◽  
Xiaoling Liu ◽  
Jianhe Wang ◽  
...  
Keyword(s):  
Gene Expression ◽  
Salicylic Acid ◽  
Agrobacterium Tumefaciens ◽  
Virulence Gene ◽  
Tumor Formation ◽  
Bacterial Virulence ◽  
In Planta ◽  
Virulence Gene Expression ◽  
Successful Infection ◽  
Plant Metabolite

It is highly intriguing how bacterial pathogens can quickly shut down energy-costly infection machinery once successful infection is established. This study depicts that mutation of repressor SghR increases the expression of hydrolase SghA in Agrobacterium tumefaciens, which releases plant defense signal salicylic acid (SA) from its storage form SA β-glucoside (SAG). Addition of SA substantially reduces gene expression of bacterial virulence. Bacterial vir genes and sghA are differentially transcribed at early and later infection stages, respectively. Plant metabolite sucrose is a signal ligand that inactivates SghR and consequently induces sghA expression. Disruption of sghA leads to increased vir expression in planta and enhances tumor formation whereas mutation of sghR decreases vir expression and tumor formation. These results depict a remarkable mechanism by which A. tumefaciens taps on the reserved pool of plant signal SA to reprogram its virulence upon establishment of infection.

scholarly journals In planta bacterial multi-omics analysis illuminates regulatory principles underlying plant-pathogen interactions

2019 ◽  
Author(s):  
Tatsuya Nobori ◽  
Yiming Wang ◽  
Jingni Wu ◽  
Sara Christina Stolze ◽  
Yayoi Tsuda ◽  
...  
Keyword(s):  
Gene Regulation ◽  
Pseudomonas Syringae ◽  
Protein Level ◽  
Plant Pathogens ◽  
Plant Immunity ◽  
Bacterial Pathogen ◽  
Bacterial Virulence ◽  
In Planta ◽  
Bacterial Gene ◽  
Global Food Security

AbstractUnderstanding how gene expression is regulated in plant pathogens is crucial for pest control and thus global food security. An integrated understanding of bacterial gene regulation in the host is dependent on multi-omic datasets, but these are largely lacking. Here, we simultaneously characterized the transcriptome and proteome of a foliar bacterial pathogen, Pseudomonas syringae, in Arabidopsis thaliana and identified a number of bacterial processes influenced by plant immunity at the mRNA and the protein level. We found instances of both concordant and discordant regulation of bacterial mRNAs and proteins. Notably, the tip component of bacterial type III secretion system was selectively suppressed by the plant salicylic acid pathway at the protein level, suggesting protein-level targeting of the bacterial virulence system by plant immunity. Furthermore, gene co-expression analysis illuminated previously unknown gene regulatory modules underlying bacterial virulence and their regulatory hierarchy. Collectively, the integrated in planta bacterial omics approach provides molecular insights into multiple layers of bacterial gene regulation that contribute to bacterial growth in planta and elucidate the role of plant immunity in controlling pathogens.

Endogenous CO2 may inhibit bacterial growth and induce virulence gene expression in enteropathogenic Escherichia coli

2012 ◽  
Vol 53 (1) ◽  
pp. 49-55 ◽  
Author(s):  
Haydee Martínez ◽  
Thomas Buhse ◽  
Marco Rivera ◽  
P. Parmananda ◽  
Guadalupe Ayala ◽  
...  
Keyword(s):  
Gene Expression ◽  
Escherichia Coli ◽  
Bacterial Growth ◽  
Virulence Gene ◽  
Enteropathogenic Escherichia Coli ◽  
Virulence Gene Expression

scholarly journals Transcriptome landscape of a bacterial pathogen under plant immunity

2018 ◽  
Vol 115 (13) ◽  
pp. E3055-E3064 ◽  
Author(s):  
Tatsuya Nobori ◽  
André C. Velásquez ◽  
Jingni Wu ◽  
Brian H. Kvitko ◽  
James M. Kremer ◽  
...  
Keyword(s):  
Immune Response ◽  
Pseudomonas Syringae ◽  
Bacterial Growth ◽  
Plant Pathogens ◽  
Plant Immunity ◽  
Expression Patterns ◽  
Bacterial Pathogen ◽  
In Planta ◽  
Bacterial Strains ◽  
Bacterial Genes

Plant pathogens can cause serious diseases that impact global agriculture. The plant innate immunity, when fully activated, can halt pathogen growth in plants. Despite extensive studies into the molecular and genetic bases of plant immunity against pathogens, the influence of plant immunity in global pathogen metabolism to restrict pathogen growth is poorly understood. Here, we developed RNA sequencing pipelines for analyzing bacterial transcriptomes in planta and determined high-resolution transcriptome patterns of the foliar bacterial pathogen Pseudomonas syringae in Arabidopsis thaliana with a total of 27 combinations of plant immunity mutants and bacterial strains. Bacterial transcriptomes were analyzed at 6 h post infection to capture early effects of plant immunity on bacterial processes and to avoid secondary effects caused by different bacterial population densities in planta. We identified specific “immune-responsive” bacterial genes and processes, including those that are activated in susceptible plants and suppressed by plant immune activation. Expression patterns of immune-responsive bacterial genes at the early time point were tightly linked to later bacterial growth levels in different host genotypes. Moreover, we found that a bacterial iron acquisition pathway is commonly suppressed by multiple plant immune-signaling pathways. Overexpression of a P. syringae sigma factor gene involved in iron regulation and other processes partially countered bacterial growth restriction during the plant immune response triggered by AvrRpt2. Collectively, this study defines the effects of plant immunity on the transcriptome of a bacterial pathogen and sheds light on the enigmatic mechanisms of bacterial growth inhibition during the plant immune response.

scholarly journals The Tzs Protein and Exogenous Cytokinin Affect Virulence Gene Expression and Bacterial Growth of Agrobacterium tumefaciens

2013 ◽  
Vol 103 (9) ◽  
pp. 888-899 ◽  
Author(s):  
Hau-Hsuan Hwang ◽  
Fong-Jhih Yang ◽  
Tun-Fang Cheng ◽  
Yi-Chun Chen ◽  
Ying-Ling Lee ◽  
...  
Keyword(s):  
Gene Expression ◽  
Agrobacterium Tumefaciens ◽  
Bacterial Growth ◽  
Deletion Mutant ◽  
Virulence Gene ◽  
Protein Accumulation ◽  
Virulence Gene Expression ◽  
Crown Gall Disease ◽  
Wide Range ◽  
Exogenous Cytokinin

The soil phytopathogen Agrobacterium tumefaciens causes crown gall disease in a wide range of plant species. The neoplastic growth at the infection sites is caused by transferring, integrating, and expressing transfer DNA (T-DNA) from A. tumefaciens into plant cells. A trans-zeatin synthesizing (tzs) gene is located in the nopaline-type tumor-inducing plasmid and causes trans-zeatin production in A. tumefaciens. Similar to known virulence (Vir) proteins that are induced by the vir gene inducer acetosyringone (AS) at acidic pH 5.5, Tzs protein is highly induced by AS under this growth condition but also constitutively expressed and moderately upregulated by AS at neutral pH 7.0. We found that the promoter activities and protein levels of several AS-induced vir genes increased in the tzs deletion mutant, a mutant with decreased tumorigenesis and transient transformation efficiencies, in Arabidopsis roots. During AS induction and infection of Arabidopsis roots, the tzs deletion mutant conferred impaired growth, which could be rescued by genetic complementation and supplementing exogenous cytokinin. Exogenous cytokinin also repressed vir promoter activities and Vir protein accumulation in both the wild-type and tzs mutant bacteria with AS induction. Thus, the tzs gene or its product, cytokinin, may be involved in regulating AS-induced vir gene expression and, therefore, affect bacterial growth and virulence during A. tumefaciens infection.

scholarly journals A Combination of Independent Transcriptional Regulators Shapes Bacterial Virulence Gene Expression during Infection

2010 ◽  
Vol 6 (3) ◽  
pp. e1000817 ◽  
Author(s):  
Samuel A. Shelburne ◽  
Randall J. Olsen ◽  
Bryce Suber ◽  
Pranoti Sahasrabhojane ◽  
Paul Sumby ◽  
...  
Keyword(s):  
Gene Expression ◽  
Virulence Gene ◽  
Transcriptional Regulators ◽  
Bacterial Virulence ◽  
Virulence Gene Expression

scholarly journals GABA (γ-Aminobutyric Acid) Uptake Via the GABA Permease GabP Represses Virulence Gene Expression in Pseudomonas syringae pv. tomato DC3000

2016 ◽  
Vol 29 (12) ◽  
pp. 938-949 ◽  
Author(s):  
S. L. McCraw ◽  
D. H. Park ◽  
R. Jones ◽  
M. A. Bentley ◽  
A. Rico ◽  
...  
Keyword(s):  
Gene Expression ◽  
Amino Acid ◽  
Pseudomonas Syringae ◽  
Aminobutyric Acid ◽  
Gaba Uptake ◽  
Acid Uptake ◽  
Natural Setting ◽  
In Planta ◽  
Tomato Dc3000 ◽  
Virulence Gene Expression

The nonprotein amino acid γ-aminobutyric acid (GABA) is the most abundant amino acid in the tomato (Solanum lycopersicum) leaf apoplast and is synthesized by Arabidopsis thaliana in response to infection by the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 (hereafter called DC3000). High levels of exogenous GABA have previously been shown to repress the expression of the type III secretion system (T3SS) in DC3000, resulting in reduced elicitation of the hypersensitive response (HR) in the nonhost plant tobacco (Nicotiana tabacum). This study demonstrates that the GABA permease GabP provides the primary mechanism for GABA uptake by DC3000 and that the gabP deletion mutant ΔgabP is insensitive to GABA-mediated repression of T3SS expression. ΔgabP displayed an enhanced ability to elicit the HR in young tobacco leaves and in tobacco plants engineered to produce increased levels of GABA, which supports the hypothesis that GABA uptake via GabP acts to regulate T3SS expression in planta. The observation that P. syringae can be rendered insensitive to GABA through loss of gabP but that gabP is retained by this bacterium suggests that GabP is important for DC3000 in a natural setting, either for nutrition or as a mechanism for regulating gene expression. [Formula: see text] Copyright © 2016 The Author(s). This is an open access article distributed under the CC BY Attribution 4.0 International license .

scholarly journals Spatial Segregation of Virulence Gene Expression during Acute Enteric Infection with Salmonella enterica serovar Typhimurium

mBio ◽  
2014 ◽  
Vol 5 (1) ◽  
Author(s):  
Richard C. Laughlin ◽  
Leigh A. Knodler ◽  
Roula Barhoumi ◽  
H. Ross Payne ◽  
Jing Wu ◽  
...  
Keyword(s):  
Gene Expression ◽  
Salmonella Enterica ◽  
Virulence Gene ◽  
Bacterial Virulence ◽  
Natural Host ◽  
Host Cells ◽  
Enteric Infection ◽  
Content Type ◽  
Virulence Gene Expression ◽  
Serovar Typhimurium

ABSTRACTTo establish a replicative niche during its infectious cycle between the intestinal lumen and tissue, the enteric pathogenSalmonella entericaserovar Typhimurium requires numerous virulence genes, including genes for two type III secretion systems (T3SS) and their cognate effectors. To better understand the host-pathogen relationship, including early infection dynamics and induction kinetics of the bacterial virulence program in the context of a natural host, we monitored the subcellular localization and temporal expression of T3SS-1 and T3SS-2 using fluorescent single-cell reporters in a bovine, ligated ileal loop model of infection. We observed that the majority of bacteria at 2 h postinfection are flagellated, express T3SS-1 but not T3SS-2, and are associated with the epithelium or with extruding enterocytes. In epithelial cells,S. Typhimurium cells were surrounded by intact vacuolar membranes or present within membrane-compromised vacuoles that typically contained numerous vesicular structures. By 8 h postinfection, T3SS-2-expressing bacteria were detected in the lamina propria and in the underlying mucosa, while T3SS-1-expressing bacteria were in the lumen. Our work identifies for the first time the temporal and spatial regulation of T3SS-1 and -2 expression during an enteric infection in a natural host and provides further support for the concept of cytosolicS. Typhimurium in extruding epithelium as a mechanism for reseeding the lumen.IMPORTANCEThe pathogenic bacteriumSalmonella entericaserovar Typhimurium invades and persists within host cells using distinct sets of virulence genes. Genes fromSalmonellapathogenicity island 1 (SPI-1) are used to initiate contact and facilitate uptake into nonphagocytic host cells, while genes within SPI-2 allow the pathogen to colonize host cells. While many studies have identified bacterial virulence determinants in animal models of infection, very few have focused on virulence gene expression at the single-cell level during anin vivoinfection. To better understand when and where bacterial virulence factors are expressed during an acute enteric infection of a natural host, we infected bovine jejunal-ileal loops withS. Typhimurium cells harboring fluorescent transcriptional reporters for SPI-1 and -2 (PinvFand PssaG, respectively). After a prescribed time of infection, tissue and luminal fluid were collected and analyzed by microscopy. During early infection (≤2 h), bacteria within both intact and compromised membrane-bound vacuoles were observed within the epithelium, with the majority expressing SPI-1. As the infection progressed,S. Typhimurium displayed differential expression of the SPI-1 and SPI-2 regulons, with the majority of tissue-associated bacteria expressing SPI-2 and the majority of lumen-associated bacteria expressing SPI-1. This underscores the finding thatSalmonellavirulence gene expression changes as the pathogen transitions from one anatomical location to the next.

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