Transcriptional Analysis of the Global Regulatory Networks Active in Pseudomonas syringae during Leaf Colonization

Yu, Xilan; Lund, Steven P.; Greenwald, Jessica W.; Records, Angela H.; Scott, Russell; Nettleton, Dan; Lindow, Steven E.; Gross, Dennis C.; Beattie, Gwyn A.

doi:10.1128/mbio.01683-14

Cited by 62 publications

(104 citation statements)

References 83 publications

(148 reference statements)

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“…This study also found that AlgU-dependent transcription was induced in response to osmotic stress (21), and there is a great deal of overlapping regulation between the osmotic stress stimulon and the algU regulon in P. syringae pv. syringae B728a, suggesting that osmolarity is a key signal for AlgU activation in this pathovar (21,22). But, the role of AlgU may be different in P. syringae pv.…”

supporting

confidence: 54%

“…syringae B728a growing in plants and under a variety of in vitro conditions indicated that AlgU regulates genes for alginate biosynthesis as well as for type VI secretion and oxidative and osmotic stress responses (21). This study also found that AlgU-dependent transcription was induced in response to osmotic stress (21), and there is a great deal of overlapping regulation between the osmotic stress stimulon and the algU regulon in P. syringae pv. syringae B728a, suggesting that osmolarity is a key signal for AlgU activation in this pathovar (21,22).…”

mentioning

confidence: 60%

mentioning

confidence: 99%

“…syringae B728a (21). AlgU has an active role in regulating expression of genes in response to envelope stress on leaf surfaces (21), and AlgU-dependent expression correlates with ROS production in planta (25). P. syringae pathovars produce alginate in planta (26), and there is a positive correlation between the amount of alginate produced and the severity of disease symptoms (27).…”

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confidence: 99%

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AlgU Controls Expression of Virulence Genes in Pseudomonas syringae pv. tomato DC3000

et al. 2016

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Plant-pathogenic bacteria are able to integrate information about their environment and adjust gene expression to provide adaptive functions. AlgU, an extracytoplasmic function (ECF) sigma factor encoded by Pseudomonas syringae, controls expression of genes for alginate biosynthesis and genes involved with resisting osmotic and oxidative stress. AlgU is active while these bacteria are associated with plants, where its presence supports bacterial growth and disease symptoms. We found that AlgU is an important virulence factor for P. syringae pv. tomato DC3000 but that alginate production is dispensable for disease in host plants. This implies that AlgU regulates additional genes that facilitate bacterial pathogenesis. We used transcriptome sequencing (RNA-seq) to characterize the AlgU regulon and chromatin immunoprecipitation sequencing (ChIP-seq) to identify AlgUregulated promoters associated with genes directly controlled by this sigma factor. We found that in addition to genes involved with alginate and osmotic and oxidative stress responses, AlgU regulates genes with known virulence functions, including components of the Hrp type III secretion system, virulence effectors, and the hrpL and hrpRS transcription regulators. These data suggest that P. syringae pv. tomato DC3000 has adapted to use signals that activate AlgU to induce expression of important virulence functions that facilitate survival and disease in plants. IMPORTANCEPlant immune systems produce antimicrobial and bacteriostatic conditions in response to bacterial infection. Plant-pathogenic bacteria are adapted to suppress and/or tolerate these conditions; however, the mechanisms controlling these bacterial systems are largely uncharacterized. The work presented here provides a mechanistic explanation for how P. syringae pv. tomato DC3000 coordinates expression of multiple genetic systems, including those dedicated to pathogenicity, in response to environmental conditions. This work demonstrates the scope of AlgU regulation in P. syringae pv. tomato DC3000 and characterizes the promoter sequence regulated by AlgU in these bacteria. Pseudomonas syringae is a globally dispersed plant-pathogenic bacterium adapted to live in many diverse environments, which in some cases expose bacteria to stresses that can interfere with their growth and survival. Counteracting or tolerating these stresses requires coordinated expression of specific physiologic traits. These responses are controlled by environmental sensing and signal transduction systems that detect information about external conditions and induce changes in transcription. The extracytoplasmic function (ECF) sigma factors are one type of system providing this function in bacteria and are capable of inducing sets of genes (regulons) in response to environmental stimuli (1). ECF sigma factor activity is often controlled by a cytoplasmic membrane-bound anti-sigma factor that forms a complex with the ECF sigma factor (2). Under inducing conditions, the ECF sigma factor is liberated from the anti-...

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supporting

confidence: 54%

mentioning

confidence: 60%

mentioning

confidence: 99%

mentioning

confidence: 99%

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AlgU Controls Expression of Virulence Genes in Pseudomonas syringae pv. tomato DC3000

et al. 2016

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“…There is precedence for such a restricted QS regulon. Only a small subset of genes is activated in the photosynthetic bacterium Rhodopseudomonas palustris (33), as well as in the plant pathogen Pseudomonas syringae (34). This is in stark contrast to the QS systems of Pseudomonas aeruginosa, which regulate hundreds of genes (35,36).…”

Section: Discussionmentioning

confidence: 95%

Quorum Sensing in a Methane-Oxidizing Bacterium

Puri

Schaefer

et al. 2017

J Bacteriol

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Aerobic methanotrophic bacteria use methane as their sole source of carbon and energy and serve as a major sink for the potent greenhouse gas methane in freshwater ecosystems. Dissecting the molecular details of how these organisms interact in the environment may increase our understanding of how they perform this important ecological role. Many bacterial species use quorum sensing (QS) systems to regulate gene expression in a cell density-dependent manner. We have identified a QS system in the genome of Methylobacter tundripaludum, a dominant methane oxidizer in methane enrichments of sediment from Lake Washington (Seattle, WA). We determined that M. tundripaludum produces primarily N-3-hydroxydecanoyl-L-homoserine lactone (3-OH-C 10 -HSL) and that its production is governed by a positive feedback loop. We then further characterized this system by determining which genes are regulated by QS in this methane oxidizer using transcriptome sequencing (RNA-seq) and discovered that this system regulates the expression of a putative nonribosomal peptide synthetase biosynthetic gene cluster. Finally, we detected an extracellular factor that is produced by M. tundripaludum in a QS-dependent manner. These results identify and characterize a mode of cellular communication in an aerobic methane-oxidizing bacterium.IMPORTANCE Aerobic methanotrophs are critical for sequestering carbon from the potent greenhouse gas methane in the environment, yet the mechanistic details of chemical interactions in methane-oxidizing bacterial communities are not well understood. Understanding these interactions is important in order to maintain, and potentially optimize, the functional potential of the bacteria that perform this vital ecosystem function. In this work, we identify a quorum sensing system in the aerobic methanotroph Methylobacter tundripaludum and use both chemical and genetic methods to characterize this system at the molecular level.KEYWORDS methane, methanotroph, quorum sensing, sociomicrobiology, acyl-homoserine lactone, biosynthetic gene cluster A erobic methane-oxidizing bacteria (methanotrophs) are an important component of the carbon cycle that serve to sequester carbon from the potent greenhouse gas methane after it is produced by anaerobic microbial ecosystems (1, 2). Methanotrophs provide a carbon and energy source for communities of organisms that cannot oxidize methane themselves, thereby serving as key supporting species in the environment (3, 4). The methanotroph Methylobacter tundripaludum is a member of the Gammaproteobacteria (type I methanotroph), and it has been repeatedly identified as a dominant member of methane enrichment and stable isotope probing experiments of sediment from Lake Washington, Seattle, WA (3, 5-7). Methylobacter spp. have also been isolated from other geographically distinct regions, including the arctic (8), estuaries (9), and temperate wetlands (10), highlighting the diverse environments inhabited by this genus. We, therefore, use M. tundripaludum as part of a model system for ...

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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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Transcriptional Analysis of the Global Regulatory Networks Active in Pseudomonas syringae during Leaf Colonization

Cited by 62 publications

References 83 publications

AlgU Controls Expression of Virulence Genes in Pseudomonas syringae pv. tomato DC3000

AlgU Controls Expression of Virulence Genes in Pseudomonas syringae pv. tomato DC3000

Quorum Sensing in a Methane-Oxidizing Bacterium

Molecular networks in plant–pathogen holobiont

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