Regulons of Three Pseudomonas syringae pv. tomato DC3000 Iron Starvation Sigma Factors

Markel, Eric; Butcher, Bronwyn G.; Myers, Christopher R.; Stodghill, Paul; Cartinhour, Sam; Swingle, Bryan

doi:10.1128/aem.02801-12

Cited by 11 publications

(11 citation statements)

References 21 publications

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“…It is known that the genome of DC3000 contains 15 sigma factors, including 10 extracytoplasmic function (ECF) sigma factors (Oguiza et al 2005). These ECF sigma factors are involved in regulating T3SS gene expression (HrpL), iron transport systems (PvdS, PSPTO1203, PSPTO1209, PSPTO1286, and PSPTO0444), outer membrane modifications (SigX and AlgU), as well as unknown functions (PSPTO1043 and PSPTO4224) (Markel et al 2011(Markel et al , 2013Oguiza et al 2005). In addition, the DC3000 genome encodes over 12% of the genes required for rapid adaptation to diverse environments during epiphytic growth and pathogenesis (Buell et al 2003).…”

Section: Discussionmentioning

confidence: 99%

The Stringent Response Mediated by (p)ppGpp Is Required for Virulence ofPseudomonas syringaepv.tomatoand Its Survival on Tomato

Chatnaparat

Zhong

Korban

et al. 2015

MPMI

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The hypersensitive response and pathogenicity (hrp) type III secretion system (T3SS) is a key pathogenicity factor in Pseudomonas syringae pv. tomato DC3000 (DC3000). In this study, the role of the second messenger (p)ppGpp on virulence and survival of DC3000 was investigated. Results have demonstrated that (p)ppGpp-deficient mutant (ppGpp(0)) of DC3000 exhibited lower levels of expression of the T3SS and genes of other virulence traits, such as coronatine toxin. The ppGpp(0) mutant of DC3000 was greatly impaired in causing disease and in growth in planta. Furthermore, (p)ppGpp was required for swarming motility, pyoverdine production, the oxidative stress response, as well as γ-amino butyric acid utilization. Screening of amino acids, major signals in activation of ppGpp biosynthesis, revealed that promoter activities of the avrPto gene could be either activated or suppressed by various amino acids in a ppGpp-dependent or -independent manner. Moreover, the ppGpp(0) mutant exhibited increased cell size and decreased survival on plant surfaces. Altogether, these findings indicate that ppGpp acts as an internal signal that regulates the T3SS as well as other virulence factors in pseudomonads and suggest that bacterial pathogens utilize intracellular messengers to sense environmental and nutritional signals for rapid, precise, and reversible control of their pathogenesis and survival.

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Section: Discussionmentioning

confidence: 99%

The Stringent Response Mediated by (p)ppGpp Is Required for Virulence ofPseudomonas syringaepv.tomatoand Its Survival on Tomato

Chatnaparat

Zhong

Korban

et al. 2015

MPMI

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“…Five P. syringae pv. tomato DC3000 ECF sigma factors are dedicated to iron homeostasis and control expression of genes related to siderophore biosynthesis and/or uptake (3)(4)(5)(6). The remaining five are classified as stress response ECF sigma factors based on sequence similarity to sigma factors encoded by other bacteria (3).…”

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confidence: 99%

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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“…A recent study by Markel et al [65] used ChlP-seq to investigate the regulons in P. syringae pv. tomato DC3000 associated with ECF sigma factors encoded by PSPTO_0444, PSPTO_1209, and PSPTO_1286, which are orthologous to the ecf6 , ecf5 and ecf7 genes of B728a, respectively.…”

Section: Discussionmentioning

confidence: 99%

“…Likewise, we observed that the ECF7 sigma factor, which is orthologous to PSPTO_1286, regulated a heme oxygenase (Psyr_1104) and FecA-receptor (Psyr_1105) in B728a (Table 4). The regulon associated with PSPTO_1209 was somewhat larger and included the type VI protein secretion system, an OmpA-family protein, and a helicase family protein in addition to a FecA-like receptor [65]. Ferric uptake regulator binding sites (Fur box) were identified upstream of FecA-like receptor genes [65], [66], which shows the importance of iron regulation on expression of these sigma factors and their downstream regulon targets.…”

Section: Discussionmentioning

confidence: 99%

“…The regulon associated with PSPTO_1209 was somewhat larger and included the type VI protein secretion system, an OmpA-family protein, and a helicase family protein in addition to a FecA-like receptor [65]. Ferric uptake regulator binding sites (Fur box) were identified upstream of FecA-like receptor genes [65], [66], which shows the importance of iron regulation on expression of these sigma factors and their downstream regulon targets. Consequently, it is likely that Fur controls expression of the FecI-like sigma factors and their associated regulons in B728a as has been previously demonstrated in DC3000 [65], [66].…”

Section: Discussionmentioning

confidence: 99%

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Characterization of Five ECF Sigma Factors in the Genome of Pseudomonas syringae pv. syringae B728a

et al. 2013

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Pseudomonas syringae pv. syringae B728a, a bacterial pathogen of bean, utilizes large surface populations and extracellular signaling to initiate a fundamental change from an epiphytic to a pathogenic lifestyle. Extracytoplasmic function (ECF) sigma (σ) factors serve as important regulatory factors in responding to various environmental signals. Bioinformatic analysis of the B728a genome revealed 10 ECF sigma factors. This study analyzed deletion mutants of five previously uncharacterized ECF sigma factor genes in B728a, including three FecI-type ECF sigma factors (ECF5, ECF6, and ECF7) and two ECF sigma factors placed in groups ECF11 and ECF18. Transcriptional profiling by qRT-PCR analysis of ECF sigma factor mutants was used to measure expression of their associated anti-sigma and outer membrane receptor proteins, and expression of genes associated with production of extracellular polysaccharides, fimbriae, glycine betaine and syringomycin. Notably, the B728aΔecf7 mutant displayed reduced swarming and had decreased expression of CupC fimbrial genes. Growth and pathogenicity assays, using a susceptible bean host, revealed that none of the tested sigma factor genes are required for in planta growth and lesion formation.

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Regulons of Three Pseudomonas syringae pv. tomato DC3000 Iron Starvation Sigma Factors

Cited by 11 publications

References 21 publications

The Stringent Response Mediated by (p)ppGpp Is Required for Virulence ofPseudomonas syringaepv.tomatoand Its Survival on Tomato

The Stringent Response Mediated by (p)ppGpp Is Required for Virulence ofPseudomonas syringaepv.tomatoand Its Survival on Tomato

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

Characterization of Five ECF Sigma Factors in the Genome of Pseudomonas syringae pv. syringae B728a

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