Role of rpfF in virulence and exoenzyme production of Xanthomonas axonopodis pv. glycines, the causal agent of bacterial pustule of soybean.

Ten strains of Xanthomonas axonopodis pv. glycines, the causal agent of bacterial pustule of soybean, which were isolated from various soybean growing regions of Thailand, produced an extracellular diffusible factor (DSF) related to a well-characterized quorum sensing molecule produced by other Xanthomonas spp. Genomic DNA of the 10 strains of X. axonopodis pv. glycines contained rpfF, a gene encoding for the biosynthesis of the DSF in X. campestris pv. campestris. The rpfF gene from one strain of X. axonopodis pv. glycines was fully sequenced, and the 289 aa product is closely related to RpfF of other Xanthomonas spp. (95 to 98% identical). Three independently generated rpfF mutants of X. axonopodis pv. glycines strain No12-2 were defective in the production of a DSF, as expected if rpfF encodes for DSF biosynthesis in X. axonopodis pv. glycines. The rpfF mutants of X. axonopodis pv. glycines exhibited reduced virulence on soybean and produced less than wild-type levels of extracellular polysaccharide and the extracellular enzymes carboxylmethylcellulase, protease, endo-beta-1,4-mannanase, and pectate lyase. Transcripts for three genes that encode for the extracellular enzymes protease, endoglucanase, and pectate lyase were at lower abundance in an rpfF mutant than in the parental strain of X. axonopodis pv. glycines. These results indicate that X. axonopodis pv. glycines produces a diffusible signal related to the DSF of X. campestris pv. campestris, which contributes to virulence and exoenzyme production by this phytopathogenic bacterium.

[1]  S. Lindow,et al.  Living in two worlds: the plant and insect lifestyles of Xylella fastidiosa. , 2008, Annual review of phytopathology.

[2]  Lian-Hui Zhang,et al.  Quorum sensing and virulence regulation in Xanthomonas campestris. , 2008, FEMS microbiology reviews.

[3]  S. Lindow,et al.  A cell–cell signaling sensor is required for virulence and insect transmission of Xylella fastidiosa , 2008, Proceedings of the National Academy of Sciences.

[4]  Karyn L. Newman,et al.  Virulence of plant pathogenic bacteria attenuated by degradation of fatty acid cell-to-cell signaling factors. , 2008, Molecular plant-microbe interactions : MPMI.

[5]  C. Fuqua,et al.  Biofilm formation by plant-associated bacteria. , 2007, Annual review of microbiology.

[6]  J. M. Dow,et al.  Controlled synthesis of the DSF cell–cell signal is required for biofilm formation and virulence in Xanthomonas campestris , 2007, Environmental microbiology.

[7]  K. Winzer,et al.  Look who's talking: communication and quorum sensing in the bacterial world , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[8]  E. Carrilho,et al.  Characterization of a putative Xylella fastidiosa diffusible signal factor by HRGC-EI-MS. , 2007, Journal of mass spectrometry : JMS.

[9]  J. M. Dow,et al.  The HD-GYP domain, cyclic di-GMP signaling, and bacterial virulence to plants. , 2006, Molecular plant-microbe interactions : MPMI.

[10]  Juan E. González,et al.  Messing with Bacterial Quorum Sensing , 2006, Microbiology and Molecular Biology Reviews.

[11]  U. Jenal,et al.  Mechanisms of cyclic-di-GMP signaling in bacteria. , 2006, Annual review of genetics.

[12]  T. Burr,et al.  A Pectate Lyase Homolog, xagP, in Xanthomonas axonopodis pv. glycines Is Associated with Hypersensitive Response Induction on Tobacco. , 2006, Phytopathology.

[13]  I. Pieretti,et al.  High Variation in Pathogenicity of Genetically Closely Related Strains of Xanthomonas albilineans, the Sugarcane Leaf Scald Pathogen, in Guadeloupe. , 2006, Phytopathology.

[14]  C. Ramos,et al.  The HD‐GYP domain of RpfG mediates a direct linkage between the Rpf quorum‐sensing pathway and a subset of diguanylate cyclase proteins in the phytopathogen Xanthomonas axonopodis pv citri , 2006, Molecular microbiology.

[15]  C. Bermejo,et al.  Analysis of the molecular basis of Xanthomonas axonopodis pv. citri pathogenesis in Citrus limon , 2006 .

[16]  J. M. Dow,et al.  Genome scale analysis of diffusible signal factor regulon in Xanthomonas campestris pv. campestris: identification of novel cell–cell communication‐dependent genes and functions , 2006, Molecular microbiology.

[17]  S. Lindow,et al.  Pseudomonas syringae genes induced during colonization of leaf surfaces. , 2005, Environmental microbiology.

[18]  T. Burr,et al.  Aggressiveness of Xanthomonas axonopodis pv. glycines isolates to soybean and hypersensitivity responses by other plants , 2005 .

[19]  Zhijian Yao,et al.  Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris. , 2005, Genome research.

[20]  Lian-Hui Zhang,et al.  Quorum sensing and quorum-quenching enzymes. , 2005, Journal of microbiology.

[21]  Karyn L. Newman,et al.  Cell-cell signaling controls Xylella fastidiosa interactions with both insects and plants. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Lian-Hui Zhang,et al.  A bacterial cell–cell communication signal with cross‐kingdom structural analogues , 2003, Molecular microbiology.

[23]  J. M. Dow,et al.  Genetic and molecular analysis of a cluster of rpf genes involved in positive regulation of synthesis of extracellular enzymes and polysaccharide in Xanthomonas campestris pathovar campestris , 1991, Molecular and General Genetics MGG.

[24]  P. Turner,et al.  Behaviour of the transposons Tn5 and Tn7 in Xanthomonas campestris pv. campestris , 1984, Molecular and General Genetics MGG.

[25]  D. Coplin,et al.  Quorum sensing in plant-pathogenic bacteria. , 2003, Annual review of phytopathology.

[26]  J. M. Dow,et al.  Biofilm dispersal in Xanthomonas campestris is controlled by cell–cell signaling and is required for full virulence to plants , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Bonnie L Bassler,et al.  Small Talk Cell-to-Cell Communication in Bacteria , 2002, Cell.

[28]  R. Sonti,et al.  rpfF mutants of Xanthomonas oryzae pv. oryzae are deficient for virulence and growth under low iron conditions. , 2002, Molecular plant-microbe interactions : MPMI.

[29]  E. C. Teixeira,et al.  Comparison of the genomes of two Xanthomonas pathogens with differing host specificities , 2002, Nature.

[30]  Lian-Hui Zhang,et al.  Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[31]  J. Bewley,et al.  Gel diffusion assays for endo-beta-mannanase and pectin methylesterase can underestimate enzyme activity due to proteolytic degradation: a remedy. , 2002, Analytical biochemistry.

[32]  Lian-Hui Zhang,et al.  Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase , 2001, Nature.

[33]  H. H. Ram,et al.  Soybean disease loss estimates for the top ten soybean-producing counries in 1998 , 2001 .

[34]  J. M. Dow,et al.  A two‐component system involving an HD‐GYP domain protein links cell–cell signalling to pathogenicity gene expression in Xanthomonas campestris , 2000, Molecular microbiology.

[35]  R. Sonti,et al.  Mutants of Xanthomonas oryzae pv. oryzae deficient in general secretory pathway are virulence deficient and unable to secrete xylanase. , 2000, Molecular plant-microbe interactions : MPMI.

[36]  S. Lory Secretion of proteins and assembly of bacterial surface organelles: shared pathways of extracellular protein targeting. , 1998, Current opinion in microbiology.

[37]  J. M. Dow,et al.  A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule , 1997, Molecular microbiology.

[38]  L. D. Ploper,et al.  Soybean Disease Loss Estimates for the Top 10 Soybean Producing Countries in 1994. , 1997, Plant disease.

[39]  S. P. Bradley,et al.  Cloning of a pectate lyase gene from Xanthomonas campestris pv. malvacearum and comparison of its sequence relationship with pel genes of soft-rot Erwinia and Pseudomonas. , 1996, Molecular plant-microbe interactions : MPMI.

[40]  A. Hayward The hosts of Xanthomonas. , 1993 .

[41]  J. M. Dow,et al.  Nucleotide sequence of the engXCA gene encoding the major endoglucanase of Xanthomonas campestris pv. campestris. , 1990, Gene.

[42]  J. M. Dow,et al.  A gene cluster in Xanthomonas campestris pv. campestris required for pathogenicity controls the excretion of polygalacturonate lyase and other enzymes , 1987 .

[43]  J. Neilands,et al.  Universal chemical assay for the detection and determination of siderophores. , 1987, Analytical biochemistry.

[44]  A. Kotoujansky,et al.  Mutants of Erwinia chrysanthemi defective in secretion of pectinase and cellulase , 1984, Journal of bacteriology.

[45]  P. Turner,et al.  Isolation of Mutants of Xanthomonas campestris pv. campestris Showing Altered Pathogenicity , 1984 .

[46]  A. Pühler,et al.  A Broad Host Range Mobilization System for In Vivo Genetic Engineering: Transposon Mutagenesis in Gram Negative Bacteria , 1983, Bio/Technology.

[47]  C. Kado,et al.  Conditions for mutagenesis by N-methyl-N′-nitro-N-nitrosoguanidine and relationships of A. tumefaciens mutants to crown-gall tumor induction , 1972 .

[48]  M. Starr,et al.  Polygalacturonic acid trans-eliminase of Xanthomonas campestris. , 1967, The Biochemical journal.

[49]  T. C. McIlvaine,et al.  A BUFFER SOLUTION FOR COLORIMETRIC COMPARISON , 1921 .