Xanthomonas oryzae Pv. oryzicola Response Regulator VemR Is Co-opted by the Sensor Kinase CheA for Phosphorylation of Multiple Pathogenicity-Related Targets

Cai, Lulu; Ma, Wenxiu; Zou, Lifang; Xu, Xiao; Xu, Zhi-Hong; Deng, Chao-Ying; Qian, Wenyuan; Chen, Xiaobin; Chen, Gongyou

doi:10.3389/fmicb.2022.928551

Cited by 6 publications

(5 citation statements)

References 62 publications

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“…In Xcc , HpaS is a membrane-bound histidine kinase sensor that forms a two-component signal transduction system with HrpG and activates HrpG activity by phosphorylation [ 38 ]. In the Xoc RS105 strain, there is a cross-talk between CheA/VemR and HpaS/HrpG-mediated signaling events that coordinate the hrp gene expression [ 39 ]. In addition to HrpG, regulatory factors have been identified in other Xanthomonas spp.…”

Section: Discussionmentioning

confidence: 99%

The Transcriptional Regulator TfmR Directly Regulates Two Pathogenic Pathways in Xanthomonas oryzae pv. oryzicola

Chang,

Ma,

et al. 2024

IJMS

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Xanthomonas oryzae pv. oryzicola (Xoc) is a notorious plant pathogen. Like most bacterial pathogens, Xoc has evolved a complex regulatory network to modulate the expression of various genes related to pathogenicity. Here, we have identified TfmR, a transcriptional regulator belonging to the TetR family, as a key player in the virulence mechanisms of this phytopathogenic bacterium. We have demonstrated genetically that tfmR is involved in the hypersensitive response (HR), pathogenicity, motility and extracellular polysaccharide production of this phytopathogenic bacterium. Our investigations extended to exploring TfmR’s interaction with RpfG and HrpX, two prominent virulence regulators in Xanthomonas species. We found that TfmR directly binds to the promoter region of RpfG, thereby positively regulating its expression. Notably, constitutive expression of RpfG partly reinstates the pathogenicity compromised by TfmR-deletion mutants. Furthermore, our studies revealed that TfmR also exerts direct positive regulation on the expression of the T3SS regulator HrpX. Similar to RpfG, sustained expression of HrpX partially restores the pathogenicity of TfmR-deletion mutants. These findings underscore TfmR’s multifaceted role as a central regulator governing key virulence pathways in Xoc. Importantly, our research sheds light on the intricate molecular mechanisms underlying the regulation of pathogenicity in this plant pathogen.

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Section: Discussionmentioning

confidence: 99%

The Transcriptional Regulator TfmR Directly Regulates Two Pathogenic Pathways in Xanthomonas oryzae pv. oryzicola

Chang,

Ma,

et al. 2024

IJMS

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“…HpaR1 regulates hrp gene expression via hrpG negatively in standard media but positively in plant tissues (An et al, 2011 ). Recently, Zhang et al ( 2020 ) found by ChIP‐seq that in Xcc HrpG could bind to the vemR promoter region in vivo and Cai et al ( 2022 ) showed that in X. oryzae pv. oryzicola the transcription of vemR is repressed by HrpG in nutrient‐rich conditions.…”

Section: Discussionmentioning

confidence: 99%

“…citri and the rice bacterial leaf streak agent Xanthomonas oryzae pv. oryzicola also resulted in a reduction of EPS, motility, virulence, and HR (Cai et al, 2022; Wu et al, 2019). It is possible that the VemR proteins among Xanthomonas species have similar functions.…”

Section: Discussionmentioning

confidence: 99%

Xanthomonas campestris VemR enhances the transcription of the T3SS key regulator HrpX via physical interaction with HrpG

Jisheng

Liu

et al. 2023

Molecular Plant Pathology

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VemR is a response regulator of the two‐component signalling systems (TCSs). It consists solely of a receiver domain. Previous studies have shown that VemR plays an important role in influencing the production of exopolysaccharides and exoenzymes, cell motility, and virulence of Xanthomonas campestris pv. campestris (Xcc). However, whether VemR is involved in the essential pathogenicity determinant type III secretion system (T3SS) is unclear. In this work, we found by transcriptome analysis that VemR modulates about 10% of Xcc genes, which are involved in various cellular processes including the T3SS. Further experiments revealed that VemR physically interacts with numerous proteins, including the TCS sensor kinases HpaS and RavA, and the TCS response regulator HrpG, which directly activates the transcription of HrpX, a key regulator controlling T3SS expression. It has been demonstrated previously that HpaS composes a TCS with HrpG or VemR to control the expression of T3SS or swimming motility, while RavA and VemR form a TCS to control the expression of flagellar genes. Mutation analysis and in vitro transcription assay revealed that phosphorylation might be essential for the function of VemR and phosphorylated VemR could significantly enhance the activation of hrpX transcription by HrpG. We infer that the binding of VemR to HrpG can modulate the activity of HrpG to the hrpX promoter, thereby enhancing hrpX transcription. Although further studies are required to validate this inference and explore the detailed functional mechanism of VemR, our findings provide some insights into the complex regulatory cascade of the HpaS/RavA‐VemR/HrpG‐HrpX signal transduction system in the control of T3SS.

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“…More down-regulated genes function in flagellar assembly (ko02040), bacterial chemotaxis (ko02030) in cellular process, starch and sucrose metabolism (ko00500), and oxidative phosphorylation (ko00190) indicating that B. velezensis 504 CFSs suppress phenotypes associated with chemotaxis, and motility of Xoc RS105, both of which are related to virulence toward host colonization. Genes involved in bacterial chemotaxis ( flhA , flhB , flgC , flgK , flgL , fliC genes and cheA , cheB , cheD ) were downregulated to suppress bacterial flagellar synthesis and chemotactic motility, reducing bacterial pathogenicity ( Cai et al., 2022 ). Down-regulated expression of nineteen genes in the starch and sucrose metabolism pathway could lead to inadequate intracellular energy supply to bacteria, thus affecting normal bacterial growth.…”

Section: Discussionmentioning

confidence: 99%

Antagonistic transcriptome profile reveals potential mechanisms of action on Xanthomonas oryzae pv. oryzicola by the cell-free supernatants of Bacillus velezensis 504, a versatile plant probiotic bacterium

Zhou

et al. 2023

Front. Cell. Infect. Microbiol.

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Bacterial leaf streak (BLS) of rice is a severe disease caused by the bacterial pathogen Xanthomonas oryzae pv. oryzicola (Xoc) that has gradually become the fourth major disease on rice in some rice-growing regions in southern China. Previously, we isolated a Bacillus velezensis strain 504 that exhibited apparent antagonistic activity against the Xoc wild-type strain RS105, and found that B. velezensis 504 was a potential biocontrol agent for BLS. However, the underlying mechanisms of antagonism and biocontrol are not completely understood. Here we mine the genomic data of B. velezensis 504, and the comparative transcriptomic data of Xoc RS105 treated by the cell-free supernatants (CFSs) of B. velezensis 504 to define differentially expressed genes (DEGs). We show that B. velezensis 504 shares over 89% conserved genes with FZB42 and SQR9, two representative model strains of B. velezensis, but 504 is more closely related to FZB42 than SQR9, as well as B. velezensis 504 possesses the secondary metabolite gene clusters encoding the essential anti-Xoc agents difficidin and bacilysin. We conclude that approximately 77% of Xoc RS105 coding sequences are differentially expressed by the CFSs of B. velezensis 504, which significantly downregulates genes involved in signal transduction, oxidative phosphorylation, transmembrane transport, cell motility, cell division, DNA translation, and five physiological metabolisms, as well as depresses an additional set of virulence-associated genes encoding the type III secretion, type II secretion system, type VI secretion system, type IV pilus, lipopolysaccharides and exopolysaccharides. We also show that B. velezensis 504 is a potential biocontrol agent for bacterial blight of rice exhibiting relative control efficiencies over 70% on two susceptible cultivars, and can efficiently antagonize against some important plant pathogenic fungi including Colletotrichum siamense and C. australisinense that are thought to be the two dominant pathogenic species causing leaf anthracnose of rubber tree in Hainan province of China. B. velezensis 504 also harbors some characteristics of plant growth-promoting rhizobacterium such as secreting protease and siderophore, and stimulating plant growth. This study reveals the potential biocontrol mechanisms of B. velezensis against BLS, and also suggests that B. velezensis 504 is a versatile plant probiotic bacterium.

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Xanthomonas oryzae Pv. oryzicola Response Regulator VemR Is Co-opted by the Sensor Kinase CheA for Phosphorylation of Multiple Pathogenicity-Related Targets

Cited by 6 publications

References 62 publications

The Transcriptional Regulator TfmR Directly Regulates Two Pathogenic Pathways in Xanthomonas oryzae pv. oryzicola

The Transcriptional Regulator TfmR Directly Regulates Two Pathogenic Pathways in Xanthomonas oryzae pv. oryzicola

Xanthomonas campestris VemR enhances the transcription of the T3SS key regulator HrpX via physical interaction with HrpG

Antagonistic transcriptome profile reveals potential mechanisms of action on Xanthomonas oryzae pv. oryzicola by the cell-free supernatants of Bacillus velezensis 504, a versatile plant probiotic bacterium

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