XC_0531 encodes a c-type cytochrome biogenesis protein and is required for pathogenesis in Xanthomonas campestris pv. campestris

Chen, Lei; Wang, Mingpeng; Huang, Li; Zhang, Zhaojie; Liu, Fanghua; Lu, Guang‐Tao

doi:10.1186/s12866-017-1056-9

Cited by 7 publications

(6 citation statements)

References 54 publications

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“…In brief, DsbA protein transfers its disulfide bond to newly synthesized proteins and is reoxidized back to its active oxidized state by DsbB, while DsbC rearranges the misfolded proteins and is maintained in its active state form by DsbD (27,28). Although there is an unexpected diversity in the mechanisms of disulfide bond formation (29,30), the Dsb system appears to have critical roles in copper resistance in various bacterial species (24,25,(31)(32)(33)(34)(35), including Pseudomonas aeruginosa (36), a notorious human pathogen that causes more than 10% infections in most hospitals (37) and is among the microorganisms for which there is an urgent need for novel antibiotics (38).…”

Section: Introductionmentioning

confidence: 99%

A novel copper-sensing two-component system for inducing Dsb gene expression in bacteria

Cao

Chen

et al. 2022

Science Bulletin

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Copper is an essential element for biological systems but becomes toxic when present in excess. In Pseudomonas aeruginosa, an important human pathogen, the resistance to copper requires the induction of dsbDEG operon encoding proteins involved in disulfide-bond formation (Dsb). However, it is unknown how the copper stress induces the transcription of the operon. Here, we report that the exogenous copper induces the transcription of the dsbDEG operon through a new coppersensing two-component system named DsbRS. The dsbRS is divergently transcribed from the dsbDEG operon, and the response regulator DsbR binds to the intergenic region between the operons. In the absence of copper, the sensor kinase DsbS acts as a phosphatase toward DsbR and thus blocks the transcription of the operons.However, in the presence of copper, the metal ion directly binds to the sensor domain of DsbS, for which the Cys82 residue plays a critical role. The copper-binding appears to inhibit the phosphatase activity of DsbS, leading to activation of DsbR.The copper resistance of the dsbRS knock-out mutant was restored by ectopic expression of the dsbDEG operon, confirming the critical role of the operon in the resistance to copper. Strikingly, cognates of dsbRS-dsbDEG pair are widely distributed across eubacteria. Also, a DsbR-binding site, which contains the consensus sequence 5'-TAA-N7-TTAAT-3', is detected in the promoter region of dsbDEG homologs in those species. Thus, regulation of Dsb genes by DsbRS represents a novel mechanism by which bacterial cells cope with copper stress.

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Section: Introductionmentioning

confidence: 99%

A novel copper-sensing two-component system for inducing Dsb gene expression in bacteria

Cao

Chen

et al. 2022

Science Bulletin

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“…Cytochrome c -type biogenesis protein has been reported to protect black rot disease caused by phytopathogenic Xanthomonas campestris pv. campestris from cruciferous crops ( Chen et al., 2017 ); however, the effect of the gene on FHB requires further research. Two proteins, diacylglycerol kinase and alpha-galactosidase, were located near the FHB QTL Qfhb.spa-6A.…”

Section: Discussionmentioning

confidence: 99%

High-density genetic mapping of Fusarium head blight resistance and agronomic traits in spring wheat

et al. 2023

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Fusarium head blight (FHB) has rapidly become a major challenge to successful wheat production and competitive end-use quality in western Canada. Continuous effort is required to develop germplasm with improved FHB resistance and understand how to incorporate the material into crossing schemes for marker-assisted selection and genomic selection. The aim of this study was to map quantitative trait loci (QTL) responsible for the expression of FHB resistance in two adapted cultivars and to evaluate their co-localization with plant height, days to maturity, days to heading, and awnedness. A large doubled haploid population of 775 lines developed from cultivars Carberry and AC Cadillac was assessed for FHB incidence and severity in nurseries near Portage la Prairie, Brandon, and Morden in different years, and for plant height, awnedness, days to heading, and days to maturity near Swift Current. An initial linkage map using a subset of 261 lines was constructed using 634 polymorphic DArT and SSR markers. QTL analysis revealed five resistance QTL on chromosomes 2A, 3B (two loci), 4B, and 5A. A second genetic map with increased marker density was constructed using the Infinium iSelect 90k SNP wheat array in addition to the previous DArT and SSR markers, which revealed two additional QTL on 6A and 6D. The complete population was genotyped, and a total of 6,806 Infinium iSelect 90k SNP polymorphic markers were used to identify 17 putative resistance QTL on 14 different chromosomes. As with the smaller population size and fewer markers, large-effect QTL were detected on 3B, 4B, and 5A that were consistently expressed across environments. FHB resistance QTL were co-localized with plant height QTL on chromosomes 4B, 6D, and 7D; days to heading on 2B, 3A, 4A, 4B, and 5A; and maturity on 3A, 4B, and 7D. A major QTL for awnedness was identified as being associated with FHB resistance on chromosome 5A. Nine small-effect QTL were not associated with any of the agronomic traits, whereas 13 QTL that were associated with agronomic traits did not co-localize with any of the FHB traits. There is an opportunity to select for improved FHB resistance within adapted cultivars by using markers associated with complementary QTL.

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“…We found that some KB-dependent RhpR-regulated genes not only were involved in metabolic pathways but also had certain effects on virulence. In Xanthomonas campestris , the c -type cytochromes contribute to the EPS production and extracellular enzyme activities to enhance virulence ( 54 ). In Staphylococcus aureus , HemB leads to the production of α-hemolysin, protein A, and thermonuclease to maintain virulence ( 55 , 56 ).…”

Section: Discussionmentioning

confidence: 99%

Pseudomonas savastanoi Two-Component System RhpRS Switches between Virulence and Metabolism by Tuning Phosphorylation State and Sensing Nutritional Conditions

Xie

Shao

Zhang

et al. 2019

mBio

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Pseudomonas savastanoi uses a type III secretion system (T3SS) to invade host plants. Our previous studies have demonstrated that a two-component system (TCS), RhpRS, enables P. savastanoi to coordinate the T3SS gene expression, which depends on the phosphorylation state of RhpR under different environmental conditions. Orthologues of RhpRS are distributed in a wide range of bacterial species, indicating a general regulatory mechanism. How RhpRS uses external signals and the phosphorylation state to exercise its regulatory functions remains unknown. We performed chromatin immunoprecipitation sequencing (ChIP-seq) assays to identify the specific binding sites of RhpR and RhpRD70A in either King’s B medium (KB [a T3SS-inhibiting medium]) or minimal medium (MM [a T3SS-inducing medium]). We identified 125 KB-dependent binding sites and 188 phosphorylation-dependent binding sites of RhpR. In KB, RhpR directly and positively regulated cytochrome c550 production (via ccmA) and alcohol dehydrogenase activity (via adhB) but negatively regulated anthranilate synthase activity (via trpG) and protease activity (via hemB). In addition, phosphorylated RhpR (RhpR-P) directly and negatively regulated the T3SS (via hrpR and hopR1), swimming motility (via flhA), c-di-GMP levels (via PSPPH_2590), and biofilm formation (via algD). It positively regulated twitching motility (via fimA) and lipopolysaccharide production (via PSPPH_2653). Our transcriptome sequencing (RNA-seq) analyses identified 474 and 840 new genes that were regulated by RhpR in KB and MM, respectively. We showed nutrient-rich conditions allowed RhpR to directly regulate multiple metabolic pathways of P. savastanoi and phosphorylation enabled RhpR to specifically control virulence and the cell envelope. The action of RhpRS switched between virulence and regulation of multiple metabolic pathways by tuning its phosphorylation and sensing environmental signals in KB, respectively. IMPORTANCE The plant pathogen Pseudomonas savastanoi invades host plants through a type III secretion system, which is strictly regulated by a two-component system called RhpRS. The orthologues of RhpRS are widely distributed in the bacterial kingdom. The master regulator RhpR specifically depends on the phosphorylation state to regulate the majority of the virulence-related genes. Under nutrient-rich conditions, it modulates many important metabolic pathways, which consist of one-fifth of the genome. We propose that RhpRS uses phosphorylation- and nutrition-dependent mechanisms to switch between regulating virulence and metabolism, and this functionality is widely conserved among bacterial species.

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XC_0531 encodes a c-type cytochrome biogenesis protein and is required for pathogenesis in Xanthomonas campestris pv. campestris

Cited by 7 publications

References 54 publications

A novel copper-sensing two-component system for inducing Dsb gene expression in bacteria

A novel copper-sensing two-component system for inducing Dsb gene expression in bacteria

High-density genetic mapping of Fusarium head blight resistance and agronomic traits in spring wheat

Pseudomonas savastanoi Two-Component System RhpRS Switches between Virulence and Metabolism by Tuning Phosphorylation State and Sensing Nutritional Conditions

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