Virulence analysis and gene expression profiling of the pigment-deficient mutant of<i>Xanthomonas oryzae</i>pathovar<i>oryzae</i>

Park, Youngjin; Song, Eun-Sung; Noh, Tae-Hwan; Kim, Hyungtae; Yang, Kap‐Seok; Hahn, Jang-Ho; Kang, Hee‐Wan; Lee, Byoung-Moo

doi:10.1111/j.1574-6968.2009.01793.x

Cited by 12 publications

(9 citation statements)

References 22 publications

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“…oryzae is a rod-shaped, gram-negative bacterium (Nino-Liu et al 2006). Disruption of xanthomonadin biosynthesis led to a virulence deficiency in a previous study (Goel et al 2001;Park et al 2009;Song et al 2011). X. oryzae pv.…”

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confidence: 99%

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The Rice Bacterial Pathogen Xanthomonas oryzae pv. oryzae Produces 3-Hydroxybenzoic Acid and 4-Hydroxybenzoic Acid via XanB2 for Use in Xanthomonadin, Ubiquinone, and Exopolysaccharide Biosynthesis

Zhou¹,

Huang²,

Wang³

et al. 2013

MPMI

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Xanthomonas oryzae pv. oryzae, the causal agent of rice bacterial blight, produces membrane-bound yellow pigments, referred to as xanthomonadins. Xanthomonadins protect the pathogen from photodamage and host-induced perioxidation damage. They are also required for epiphytic survival and successful host plant infection. Here, we show that XanB2 encoded by PXO_3739 plays a key role in xanthomonadin and coenzyme Q8 biosynthesis in X. oryzae pv. oryzae PXO99A. A xanB2 deletion mutant exhibits a pleiotropic phenotype, including xanthomonadin deficiency, producing less exopolysaccharide (EPS), lower viability and H2O2 resistance, and lower virulence. We further demonstrate that X. oryzae pv. oryzae produces 3-hydroxybenzoic acid (3-HBA) and 4-hydroxybenzoic acid (4-HBA) via XanB2. 3-HBA is associated with xanthomonadin biosynthesis while 4-HBA is mainly used as a precursor for coenzyme Q (CoQ)8 biosynthesis. XanB2 is the alternative source of 4-HBA for CoQ8 biosynthesis in PXO99A. These findings suggest that the roles of XanB2 in PXO99A are generally consistent with those in X. campestris pv. campestris. The present study also demonstrated that X. oryzae pv. oryzae PXO99A has evolved several specific features in 3-HBA and 4-HBA signaling. First, our results showed that PXO99A produces less 3-HBA and 4-HBA than X. campestris pv. campestris and this is partially due to a degenerated 4-HBA efflux pump. Second, PXO99A has evolved unique xanthomonadin induction patterns via 3-HBA and 4-HBA. Third, our results showed that 3-HBA or 4-HBA positively regulates the expression of gum cluster to promote EPS production in PXO99A. Taken together, the results of this study indicate that XanB2 is a key metabolic enzyme linking xanthomonadin, CoQ, and EPS biosynthesis, which are collectively essential for X. oryzae pv. oryzae pathogenesis.

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confidence: 99%

“…oryzae strains PXO99A, HB21, and KACC10331 He et al 2011). Moreover, mutations in genes involved in the shikimate pathway lead to deficiency in pigments (Goel et al 2001;Park et al 2009;Song et al 2011). oryzae strains PXO99A, KACC10331, and MAFF 311018 (He et al 2011).…”

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confidence: 99%

The Rice Bacterial Pathogen Xanthomonas oryzae pv. oryzae Produces 3-Hydroxybenzoic Acid and 4-Hydroxybenzoic Acid via XanB2 for Use in Xanthomonadin, Ubiquinone, and Exopolysaccharide Biosynthesis

Zhou¹,

Huang²,

Wang³

et al. 2013

MPMI

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“…Pigments, in general, can play a role in virulence in bacterial pathogens (20,34,37). Specifically, a carotenoid pigment called staphyloxanthin is a known virulence factor for S. aureus and is even referred to as its "golden coat" (14).…”

Section: Figmentioning

confidence: 99%

Biological Role of Pigment Production for the Bacterial Phytopathogen Pantoea stewartii subsp. stewartii

Mohammadi

Burbank

Roper

2012

Appl Environ Microbiol

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Pantoea stewartii subsp. stewartii, the causal agent of Stewart's wilt of sweet corn, produces a yellow carotenoid pigment. A nonpigmented mutant was selected from a bank of mutants generated by random transposon mutagenesis. The transposon insertion site was mapped to the crtB gene, encoding a putative phytoene synthase, an enzyme involved in the early steps of carotenoid biosynthesis. We demonstrate here that the carotenoid pigment imparts protection against UV radiation and also contributes to the complete antioxidant pathway of P. stewartii. Moreover, production of this pigment is regulated by the EsaI/EsaR quorumsensing system and significantly contributes to the virulence of the pathogen in planta. P antoea stewartii subsp. stewartii (formerly Erwinia stewartii) is a yellow-pigmented, Gram-negative bacterial phytopathogen that causes a severe disease of sweet corn (Zea mays) called Stewart's wilt. The bacterium is introduced into the plant by its insect vector, the corn flea beetle (Chaetocnema pulicaria), where it colonizes both the apoplast and the xylem. Following systemic colonization of the plant, the bacteria exit the leaf tissue as a visible, yellow bacterial ooze. It is the preferential colonization of the xylem that blocks water flow in the plant and leads to the characteristic wilting associated with the disease. The type III secretion system, stewartan exopolysaccharide production, flagellum-based motility, and one host cell wall-degrading enzyme have been implicated as important pathogenicity or virulence factors for P. stewartii, but little is known about the biological role of the characteristic yellow pigment produced by P. stewartii (4,10,11,22,35).Carotenoids are among the most diverse natural products; they are synthesized by many organisms, including animals, plants, and microorganisms, and absorb light in the 400-to 550-nm range, which gives them their yellow-orange color (5). Several Erwinia species, which are close relatives of P. stewartii, produce yellow carotenoid pigments and possess a conserved carotenoid biosynthesis operon consisting of the genes crtE, crtX, crtY, crtI, and crtB in map order. Phytoene synthase, encoded by crtB, is the enzyme for the first step in carotenoid biogenesis, and mutations in crtB render a nonpigmented phenotype (36, 40, 52). More specifically, the P. stewartii genome contains a conserved carotenoid biosynthesis operon found in Erwinia spp., where crtE encodes geranylgeranyl pyrophosphate synthase, crtX encodes 3-hydroxy-␤-carotene glycosylase, crtY encodes lycopene cyclase, and crtI encodes phytoene dehydrogenase (43, 46). The crtB gene encodes phytoene synthase, which converts geranylgeranyl pyrophosphate to phytoene, an early step in the biosynthesis of ␤-carotene (41). Zeaxanthin diglucoside, a derivative of ␤-carotene, is the typical carotenoid produced by Erwinia spp. (2), and because of the high homology to the carotenoid biosynthetic operon in other Erwinia spp., we speculate that the P. stewartii likely produces zeaxanthin diglucoside or a cl...

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“…While 3‐HBA is involved in the biosynthesis of yellow pigments called xanthomonadins (Figure ), production of 4‐HBA forms the committed step in the biosynthesis of coenzyme Q (CoQ) 8 (Zhou, Wang, et al , ). Interestingly, both xanthomonadins and CoQ are associated with epiphytic survival, protection against oxidative damage, and virulence in Xoo (Goel et al , ; Park et al , ; Zhou, Huang, et al , ).…”

Section: Resultsmentioning

confidence: 99%

Genome‐scale metabolic reconstruction and in silico analysis of the rice leaf blight pathogen, Xanthomonas oryzae

Koduru

Kim

Mohanty

et al. 2020

Molecular Plant Pathology

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Xanthomonas oryzae pv. oryzae (Xoo) is a vascular pathogen that causes leaf blight in rice, leading to severe yield losses. Since the usage of chemical control methods has not been very promising for the future disease management, it is of high importance to systematically gain new insights about Xoo virulence and pathogenesis, and devise effective strategies to combat the rice disease. To do this, we reconstructed a genome‐scale metabolic model of Xoo (iXOO673) and validated the model predictions using culture experiments. Comparison of the metabolic architecture of Xoo and other plant pathogens indicated that the Entner–Doudoroff pathway is a more common feature in these bacteria than previously thought, while suggesting some of the unique virulence mechanisms related to Xoo metabolism. Subsequent constraint‐based flux analysis allowed us to show that Xoo modulates fluxes through gluconeogenesis, glycogen biosynthesis, and degradation pathways, thereby exacerbating the leaf blight in rice exposed to nitrogenous fertilizers, which is remarkably consistent with published experimental literature. Moreover, model‐based interrogation of transcriptomic data revealed the metabolic components under the diffusible signal factor regulon that are crucial for virulence and survival in Xoo. Finally, we identified promising antibacterial targets for the control of leaf blight in rice by using gene essentiality analysis.

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Virulence analysis and gene expression profiling of the pigment-deficient mutant ofXanthomonas oryzaepathovaroryzae

Cited by 12 publications

References 22 publications

The Rice Bacterial Pathogen Xanthomonas oryzae pv. oryzae Produces 3-Hydroxybenzoic Acid and 4-Hydroxybenzoic Acid via XanB2 for Use in Xanthomonadin, Ubiquinone, and Exopolysaccharide Biosynthesis

The Rice Bacterial Pathogen Xanthomonas oryzae pv. oryzae Produces 3-Hydroxybenzoic Acid and 4-Hydroxybenzoic Acid via XanB2 for Use in Xanthomonadin, Ubiquinone, and Exopolysaccharide Biosynthesis

Biological Role of Pigment Production for the Bacterial Phytopathogen Pantoea stewartii subsp. stewartii

Genome‐scale metabolic reconstruction and in silico analysis of the rice leaf blight pathogen, Xanthomonas oryzae

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