Genetic Modulation of c-di-GMP Turnover Affects Multiple Virulence Traits and Bacterial Virulence in Rice Pathogen Dickeya zeae

Chen, Yu-fan; Lv, Minna; Liao, Lisheng; Gu, Yanfang; Liang, Zhibin; Shi, Zurong; Liu, Shiyin; Zhou, Jianuan; Zhang, Lian-Hui

doi:10.1371/journal.pone.0165979

Cited by 20 publications

(47 citation statements)

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“…B). Our previous study revealed that cell motility of D. zeae EC1 is modulated by the c‐di‐GMP levels in cells, which are controlled by two types of enzymes with opposite functions, i.e., diguanylate cyclases containing GGDEF motif and phosphodiesterases containing EAL or HD‐GYP domain (Chen et al , ). Transcriptome analysis showed that inactivation of vfmH significantly influenced the expression of W909_07580 (GGDEF), W909_11190 (GGDEF), W909_11975 (EAL) and W909_18445 (GGDEF) (Table ), and inactivation of vfmH and vfmE decreased the expression of W909_14945 (GGDEF) and W909_14950 (EAL) (Fig.…”

Section: Resultsmentioning

confidence: 99%

A two‐component regulatory system VfmIH modulates multiple virulence traits in Dickeya zeae

Jiang

et al. 2019

Molecular Microbiology

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Bacterial pathogen Dickeya zeae strain EC1 produces antibiotics-like phytotoxins called zeamines, which are major virulence determinants encoded by the zms gene cluster. In this study, we identified a zeamine-deficient mutant with a Tn5 insertion in a gene designated as vfmI encoding a two-component system (TCS) sensor histidine kinase (HK), which is accompanied by vfmH encoding a response regulator (RR) at the same genetic locus. Domain analysis shows this TCS is analogous to the VfmIH of D. dadantii , with typical characteristics of sensor HK and RR, respectively, and sharing the same operon. Deletion of either vfmI or vfmH resulted in decreased production of zeamines and cell wall degrading enzymes (CWDEs), and alleviated virulence on rice seeds and potato tubers. In D. dadantii 3937, VfmH was shown to bind to the promoters of vfmA and vfmE , while in D. zeae EC1, VfmH could bind to the promoters of vfmA , vfmE and vfmF . RNA-seq analysis of strain EC1 and its vfmH mutant also showed that the TCS positively regulated a range of virulence genes, including zms , T1SS, T2SS, T3SS, T6SS, flagellar and CWDE genes.

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Section: Resultsmentioning

confidence: 99%

A two‐component regulatory system VfmIH modulates multiple virulence traits in Dickeya zeae

Jiang

et al. 2019

Molecular Microbiology

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“…4a ). We then measured the production of cell wall degrading enzymes and extracellular polysaccharides (EPS), which are two categories of virulence factors produced by the rice pathogen D. zeae strain EC1 [ 44 , 59 ]. Results showed that JZL strains produced lower amount of pectate lyases (Pel), polygalacturonases (Peh), proteases (Prt) and cellulases (Cel) than the others, especially hardly any protein degrading zone was visible.…”

Section: Resultsmentioning

confidence: 99%

Dickeya zeae strains isolated from rice, banana and clivia rot plants show great virulence differentials

Chen

et al. 2018

BMC Microbiol

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BackgroundDickeya zeae is the causal agent of maize and rice foot rot diseases, but recently it was also found to infect banana and cause severe losses in China. Strains from different sources showed significant diversity in nature, implying complicated evolution history and pathogenic mechanisms.ResultsD. zeae strains were isolated from soft rot banana plants and ornamental monocotyledonous Clivia miniata. Compared with D. zeae strain EC1 isolated from rice, clivia isolates did not show any antimicrobial activity, produced less extracellular enzymes, had a much narrow host ranges, but released higher amount of extracellular polysaccharides (EPS). In contrast, the banana isolates in general produced more extracellular enzymes and EPS than strain EC1. Furthermore, we provided evidence that the banana D. zeae isolate MS2 produces a new antibiotic/phytotoxin(s), which differs from the zeamine toxins produced by rice pathogen D. zeae strain EC1 genetically and in its antimicrobial potency.ConclusionsThe findings from this study expanded the natural host range of D. zeae and highlighted the genetic and phenotypic divergence of D. zeae strains. Conclusions can be drawn from a series of tests that at least two types of D. zeae strains could cause the soft rot disease of banana, with one producing antimicrobial compound while the other producing none, and the D. zeae clivia strains could only infect monocot hosts. D. zeae strains isolated from different sources have diverse virulence characteristics.Electronic supplementary materialThe online version of this article (10.1186/s12866-018-1300-y) contains supplementary material, which is available to authorized users.

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“…Mutant construction and complementation. The generation of in-frame gene deletion mutants was conducted using the suicide vector pKNG101 and triparental mating, according to a protocol described previously (19). In-frame deletion of the coding regions of the specific GGDEF or EAL domain of three genes, i.e., W909_01375, W909_10355, and W909_16285, was done by the allelic-exchange method (54).…”

Section: Methodsmentioning

confidence: 99%

“…Extracellular enzyme activity assays. The cellulase (Cel), pectate lyase (Pel and Peh), and proteolytic enzyme (Prt) activities were measured using carboxymethyl cellulose sodium, polygalacturonic acid, and skimmed milk as the substrates, respectively, according to methods and conditions described previously (19).…”

Section: Methodsmentioning

confidence: 99%

Systematic Analysis of c-di-GMP Signaling Mechanisms and Biological Functions in Dickeya zeae EC1

Chen

Zhou

et al. 2020

mBio

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Dickeya zeae is an important and aggressive bacterial phytopathogen that can cause substantial economic losses in banana and rice plantations. We previously showed that c-di-GMP signaling proteins (cyclases/phosphodiesterases) in D. zeae strain EC1 play a significant role in the bacterial sessile-to-motile transition. To determine whether there is any synergistic effect among these c-di-GMP signaling proteins, we prepared a series of mutant strains by generating consecutive in-frame deletions of the genes encoding diguanylate cyclases (which make c-di-GMP) and phosphodiesterases (which break down c-di-GMP), respectively, using EC1 as a parental strain. The results showed that the complete deletion of all the putative diguanylate cyclases resulted in significantly increased bacterial motility and abrogated biofilm formation but did not appear to affect pathogenicity and virulence factor production. In contrast, the deletion of all the c-di-GMP phosphodiesterase genes disabled motility and prevented the invasion of EC1 into rice seeds. By measuring the c-di-GMP concentrations and swimming motility of all the mutants, we propose that c-di-GMP controlled swimming behavior through a multitiered program in a c-di-GMP concentration-dependent manner, which could be described as an L-shaped regression curve. These features are quite different from those that have been shown for other bacterial species such as Salmonella and Caulobacter crescentus. Further analysis identified three c-di-GMP signaling proteins, i.e., PDE10355, DGC14945, and PDE14950, that play dominant roles in influencing the global c-di-GMP pool of strain EC1. The findings from this study highlight the complexity and plasticity of c-di-GMP regulatory circuits in different bacterial species. IMPORTANCE Dickeya zeae is the etiological agent of bacterial foot rot disease, which can cause massive economic losses in banana and rice plantations. Genome sequence analysis showed that D. zeae strain EC1 contains multiple c-di-GMP turnover genes, but their roles and regulatory mechanisms in bacterial physiology and virulence remain vague. By generating consecutive in-frame deletion mutants of the genes encoding c-di-GMP biosynthesis and degradation, respectively, we analyzed the individual and collective impacts of these c-di-GMP metabolic genes on the c-di-GMP global pool, bacterial physiology, and virulence. The significance of our study is in identifying the mechanism of c-di-GMP signaling in strain EC1 more clearly, which expands the c-di-GMP regulating patterns in Gram-negative species. The methods and experimental designs in this research will provide a valuable reference for the exploration of the complex c-di-GMP regulation mechanisms in other bacteria.

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Genetic Modulation of c-di-GMP Turnover Affects Multiple Virulence Traits and Bacterial Virulence in Rice Pathogen Dickeya zeae

Cited by 20 publications

References 77 publications

A two‐component regulatory system VfmIH modulates multiple virulence traits in Dickeya zeae

A two‐component regulatory system VfmIH modulates multiple virulence traits in Dickeya zeae

Dickeya zeae strains isolated from rice, banana and clivia rot plants show great virulence differentials

Systematic Analysis of c-di-GMP Signaling Mechanisms and Biological Functions in Dickeya zeae EC1

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