Pattern-Triggered Immunity Alters the Transcriptional Regulation of Virulence-Associated Genes and Induces the Sulfur Starvation Response in <i>Pseudomonas syringae</i> pv. <i>tomato</i> DC3000

Lovelace, Amelia H.; Smith, Amy M.; Kvitko, Brian H.

doi:10.1094/mpmi-01-18-0008-r

Cited by 48 publications

(73 citation statements)

References 58 publications

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“…In addition, RpoS participates in the protection of cellular macromolecules 18 , modulation of metabolism, virulence, and changes in cell envelope and morphology 11 . The overexpression of RpoS suggests that bacteria enter a stationary phase-like state upon stress conditions, as reported previously 44 . This is further supported by the observed significant lack of growth of bacteria under CIP treatment of various concentrations.…”

Section: Discussionsupporting

confidence: 83%

“…We detected a concentration-dependent reduction of growth rate as the CIP concentration was increased, similar to another study with CIP in P. aeruginosa 12 . We then employed RNA-Seq analysis to investigate the influence of a sub-inhibitory CIP concentration on the gene expression of PaeAG1 and its relationship with the bacterial growth, similar to recent studies in P. aeruginosa 76 , 77 and other bacteria 16 , 44 , 78 – 81 . Differential expression analysis (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…Thus, to understand or to infer mechanisms associated with the transcriptional response, it is possible to build gene regulatory networks either using databases or based on co-expression data 39 , 42 , 43 . These networks allow to gain insight into response to stress conditions 44 , leading to the identification of gene clusters or even hub genes as candidate biomarkers or modulators with potential to become key therapeutic targets 43 , 45 .…”

Section: Introductionmentioning

confidence: 99%

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Transcriptomic determinants of the response of ST-111 Pseudomonas aeruginosa AG1 to ciprofloxacin identified by a top-down systems biology approach

Molina-Mora

Chinchilla-Montero

Chavarría-Azofeifa

et al. 2020

Sci Rep

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Pseudomonas aeruginosa is an opportunistic pathogen that thrives in diverse environments and causes a variety of human infections. Pseudomonas aeruginosa AG1 (PaeAG1) is a high-risk sequence type 111 (ST-111) strain isolated from a Costa Rican hospital in 2010. PaeAG1 has both blaVIM-2 and blaIMP-18 genes encoding for metallo-β-lactamases, and it is resistant to β-lactams (including carbapenems), aminoglycosides, and fluoroquinolones. Ciprofloxacin (CIP) is an antibiotic commonly used to treat P. aeruginosa infections, and it is known to produce DNA damage, triggering a complex molecular response. In order to evaluate the effects of a sub-inhibitory CIP concentration on PaeAG1, growth curves using increasing CIP concentrations were compared. We then measured gene expression using RNA-Seq at three time points (0, 2.5 and 5 h) after CIP exposure to identify the transcriptomic determinants of the response (i.e. hub genes, gene clusters and enriched pathways). Changes in expression were determined using differential expression analysis and network analysis using a topdown systems biology approach. A hybrid model using database-based and co-expression analysis approaches was implemented to predict gene-gene interactions. We observed a reduction of the growth curve rate as the sub-inhibitory cip concentrations were increased. in the transcriptomic analysis, we detected that over time CIP treatment resulted in the differential expression of 518 genes, showing a complex impact at the molecular level. The transcriptomic determinants were 14 hub genes, multiple gene clusters at different levels (associated to hub genes or as co-expression modules) and 15 enriched pathways. Down-regulation of genes implicated in several metabolism pathways, virulence elements and ribosomal activity was observed. in contrast, amino acid catabolism, RpoS factor, proteases, and phenazines genes were up-regulated. Remarkably, > 80 resident-phage genes were up-regulated after CIP treatment, which was validated at phenomic level using a phage plaque assay. thus, reduction of the growth curve rate and increasing phage induction was evidenced as the CIP concentrations were increased. In summary, transcriptomic and network analyses, as well as the growth curves and phage plaque assays provide evidence that PaeAG1 presents a complex, concentration-dependent response to sub-inhibitory CIP exposure, showing pleiotropic effects at the systems level. Manipulation of these determinants, such as phage genes, could be used to gain

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Section: Discussionsupporting

confidence: 83%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Transcriptomic determinants of the response of ST-111 Pseudomonas aeruginosa AG1 to ciprofloxacin identified by a top-down systems biology approach

Molina-Mora

Chinchilla-Montero

Chavarría-Azofeifa

et al. 2020

Sci Rep

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“…The bacteria undergo extensive transcriptional reprograming to express virulence genes and other functions needed for growth in plant tissue. These transcriptional changes occur in response to conditions in the plant host tissues (45,49,(56)(57)(58) and are coordinated through a sophisticated network of sensors and regulators that are only partially characterized (45,46,48,(59)(60)(61)(62)(63). Studies focused on control of expression and production of the factors necessary for virulence have been particularly fruitful, such as those describing T3SS and the effectors translocated into plant cells.…”

Section: Discussionmentioning

confidence: 99%

Pseudomonas syringae AlgU Downregulates Flagellin Gene Expression, Helping Evade Plant Immunity

Bao

Wei

et al. 2020

J Bacteriol

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Flagella power bacterial movement through liquids and over surfaces to access or avoid certain environmental conditions, ultimately increasing a cell’s probability of survival and reproduction. In some cases, flagella and chemotaxis are key virulence factors enabling pathogens to gain entry and attach to suitable host tissues. However, flagella are not always beneficial; both plant and animal immune systems have evolved receptors to sense the proteins that make up flagellar filaments as signatures of bacterial infection. Microbes poorly adapted to avoid or counteract these immune functions are unlikely to be successful in host environments, and this selective pressure has driven the evolution of diverse and often redundant pathogen compensatory mechanisms. We tested the role of AlgU, the Pseudomonas extracytoplasmic function sigma factor σE/σ22 ortholog, in regulating flagellar expression in the context of Pseudomonas syringae-plant interactions. We found that AlgU is necessary for downregulating bacterial flagellin expression in planta and that this results in a corresponding reduction in plant immune elicitation. This AlgU-dependent regulation of flagellin gene expression is beneficial to bacterial growth in the course of plant infection, and eliminating the plant’s ability to detect flagellin makes this AlgU-dependent function irrelevant for bacteria growing in the apoplast. Together, these results add support to an emerging model in which P. syringae AlgU functions at a key control point that serves to optimize the expression of bacterial functions during host interactions, including minimizing the expression of immune elicitors and concomitantly upregulating beneficial virulence functions. IMPORTANCE Foliar plant pathogens, like Pseudomonas syringae, adjust their physiology and behavior to facilitate host colonization and disease, but the full extent of these adaptations is not known. Plant immune systems are triggered by bacterial molecules, such as the proteins that make up flagellar filaments. In this study, we found that during plant infection, AlgU, a gene expression regulator that is responsive to external stimuli, downregulates expression of fliC, which encodes the flagellin protein, a strong elicitor of plant immune systems. This change in gene expression and resultant change in behavior correlate with reduced plant immune activation and improved P. syringae plant colonization. The results of this study demonstrate the proximate and ultimate causes of flagellar regulation in a plant-pathogen interaction.

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“…In planta transcriptome analysis was also reported in D. dadantii infecting A. thaliana using microarray . Recently, RNA sequencing (RNA‐seq) approaches were applied to profile in planta transcriptomes of Xanthomonas axonopodis infecting bean , and Pto infecting A. thaliana . RNA‐seq profiling of wild‐type and mutant strains of Pto in a variety of A. thaliana immune compromised mutants revealed the global impact of PTI and ETI and phytohormone signaling pathways on bacterial gene expression .…”

Section: Impacts Of Plants On Bacterial Virulence Networkmentioning

confidence: 99%

Molecular networks in plant–pathogen holobiont

2018

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Edited by Wilhelm JustPlant immune receptors enable detection of a multitude of microbes including pathogens. The recognition of microbes activates various plant signaling pathways, such as those mediated by phytohormones. Over the course of coevolution with microbes, plants have expanded their repertoire of immune receptors and signaling components, resulting in highly interconnected plant immune networks. These immune networks enable plants to appropriately respond to different types of microbes and to coordinate immune responses with developmental programs and environmental stress responses. However, the interconnectivity in plant immune networks is exploited by microbial pathogens to promote pathogen fitness in plants. Analogous to plant immune networks, virulence-related pathways in bacterial pathogens are also interconnected. Accumulating evidence implies that some plant-derived compounds target bacterial virulence networks. Thus, the plant immune and bacterial virulence networks intimately interact with each other. Here, we highlight recent insights into the structures of the plant immune and bacterial virulence networks and the interactions between them. We propose that small molecules derived from plants and/or bacterial pathogens connect the two molecular networks, forming supernetworks in the plant-bacterial pathogen holobiont.

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Pattern-Triggered Immunity Alters the Transcriptional Regulation of Virulence-Associated Genes and Induces the Sulfur Starvation Response in Pseudomonas syringae pv. tomato DC3000

Cited by 48 publications

References 58 publications

Transcriptomic determinants of the response of ST-111 Pseudomonas aeruginosa AG1 to ciprofloxacin identified by a top-down systems biology approach

Transcriptomic determinants of the response of ST-111 Pseudomonas aeruginosa AG1 to ciprofloxacin identified by a top-down systems biology approach

Pseudomonas syringae AlgU Downregulates Flagellin Gene Expression, Helping Evade Plant Immunity

Molecular networks in plant–pathogen holobiont

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