1887

Abstract

produces the exopolysaccharide alginate, a copolymer of mannuronic and guluronic acid. Although alginate has been isolated from plants infected by , the signals and timing of alginate gene expression have not been described. In this study, an  : :  transcriptional fusion, designated pDCalgDP, was constructed and used to monitor alginate gene expression in host and non-host plants inoculated with pv. tomato DC3000. When leaves of susceptible collard plants were spray-inoculated with DC3000(pDCalgDP), was activated within 72 h post-inoculation (p.i.) and was associated with the development of water-soaked lesions. In leaves of the susceptible tomato cv. Rio Grande-, activity was lower than in collard and was not associated with water-soaking. The expression of was also monitored in leaves of tomato cv. Rio Grande-, which is resistant to pv. tomato DC3000. Within 12 h p.i., a microscopic hypersensitive response (micro-HR) was observed in Rio Grande- leaves spray-inoculated with pv. tomato DC3000(pDCalgDP). As the HR progressed, histochemical staining indicated that individual bacterial cells on the surface of resistant tomato leaves were expressing . These results indicate that is expressed in both susceptible (e.g. collard, tomato) and resistant (Rio Grande-) host plants. The expression of in an incompatible host–pathogen interaction was further explored by monitoring transcriptional activity in leaves of tobacco, which is not a host for pv. tomato. In tobacco inoculated with DC3000(pDCalgDP), an HR was evident within 12 h p.i., and expression was evident within 8-12 h p.i. However, when tobacco was inoculated with an mutant of DC3000, the HR did not occur and expression was substantially lower. These results suggest that signals that precede the HR may stimulate alginate gene expression in . Histochemical staining with nitro blue tetrazolium indicated that the superoxide anion () is a signal for activation . This study indicates that is expressed when attempts to colonize both susceptible and resistant plant hosts.

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2003-05-01
2019-11-15
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References

  1. Alexeyev, M. F. ( 1995; ). Three kanamycin resistance gene cassettes with different polylinkers. BioTechniques 18, 52–55.
    [Google Scholar]
  2. Alfano, J. R. & Collmer, A. ( 1996; ). Bacterial pathogens in plants: life up against the wall. Plant Cell 8, 1683–1698.[CrossRef]
    [Google Scholar]
  3. Baker, J. C. & Orlandi, E. W. ( 1995; ). Active oxygen in plant pathogenesis. Annu Rev Phytopathol 33, 299–321.[CrossRef]
    [Google Scholar]
  4. Bender, C. L., Young, S. A. & Mitchell, R. E. ( 1991; ). Conservation of plasmid DNA sequences in coronatine producing pathovars of Pseudomonas syringae. Appl Environ Microbiol 57, 993–999.
    [Google Scholar]
  5. Bender, C. L., Alarcón-Chaidez, F. & Gross, D. C. ( 1999; ). Pseudomonas syringae phytotoxins: mode of action, regulation and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev 63, 266–292.
    [Google Scholar]
  6. Beyer, W. F. & Fridovich, I. ( 1987; ). Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal Biochem 161, 559–566.[CrossRef]
    [Google Scholar]
  7. Boch, J., Joardar, V., Gao, L., Robertson, T. L., Lim, M. & Kunkel, B. N. ( 2002; ). Identification of Pseudomonas syringae genes that are induced during infection of Arabidopsis thaliana. Mol Microbiol 44, 73–88.[CrossRef]
    [Google Scholar]
  8. Cabral, D. A., Loh, B. A. & Speert, D. P. ( 1987; ). Mucoid Pseudomonas aeruginosa resists nonopsonic phagocytosis by human neutrophils and macrophages. Pediatr Res 22, 429–431.[CrossRef]
    [Google Scholar]
  9. Chandra, S., Martin, G. B. & Low, P. S. ( 1996; ). The Pto kinase mediates a signaling pathway leading to the oxidative burst in tomato. Proc Natl Acad Sci U S A 93, 13393–13397.[CrossRef]
    [Google Scholar]
  10. Charkowski, A. O., Huang, H. C. & Collmer, A. ( 1997; ). Altered localization of HrpZ in Pseudomonas syringae pv. syringae hrp mutants suggests that different components of the type III secretion pathway control protein translocation across the inner and outer membranes of gram-negative bacteria. J Bacteriol 179, 3866–3874.
    [Google Scholar]
  11. Collmer, A., Badel, J. L., Charkowski, A. O. & 8 other authors ( 2000; ). Pseudomonas syringae Hrp type III secretion system and effector proteins. Proc Natl Acad Sci U S A 97, 8770–8777.[CrossRef]
    [Google Scholar]
  12. Deng, W. L., Preston, G., Collmer, A., Chang, C. J. & Huang, H. C. ( 1998; ). Characterization of the hrpC and hrpRS operons of Pseudomonas syringae pathovars syringae, tomato, and glycinea and analysis of the ability of hrpF, hrpG, hrcC, hrpT, and hrpV mutants to elicit the hypersensitive response and disease in plants. J Bacteriol 180, 4523–4531.
    [Google Scholar]
  13. Doke, N. ( 1983; ). Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol Plant Pathol 23, 345–357.[CrossRef]
    [Google Scholar]
  14. Fakhr, M. K., Peñaloza-Vázquez, A., Chakrabarty, A. M. & Bender, C. L. ( 1999; ). Regulation of alginate biosynthesis in Pseudomonas syringae pv. syringae. J Bacteriol 181, 3478–3485.
    [Google Scholar]
  15. Fett, W. F. & Dunn, M. F. ( 1989; ). Exopolysaccharides produced by phytopathogenic Pseudomonas syringae pathovars in infected leaves of susceptible hosts. Plant Physiol 89, 5–9.[CrossRef]
    [Google Scholar]
  16. Figurski, D. & Helinski, D. R. ( 1979; ). Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A 76, 1648–1652.[CrossRef]
    [Google Scholar]
  17. Flor, H. H. ( 1971; ). Current status of the gene-for-gene concept. Annu Rev Phytopathol 9, 275–296.[CrossRef]
    [Google Scholar]
  18. Fryer, M. J., Oxborough, K., Mullineaux, P. M. & Baker, N. R. ( 2002; ). Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53, 1249–1254.[CrossRef]
    [Google Scholar]
  19. Galán, J. E. & Collmer, A. C. ( 1999; ). Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284, 1322–1328.[CrossRef]
    [Google Scholar]
  20. Grant, J. J., Yun, B. W. & Loake, G. J. ( 2000; ). Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. Plant J 24, 569–582.[CrossRef]
    [Google Scholar]
  21. Gross, M. & Rudolph, K. ( 1987; ). Studies on the extracellular polysaccharides (EPS) produced in vitro by Pseudomonas phaseolicola. I. Indications for a polysaccharide resembling alginic acid in seven P. syringae pathovars. J Phytopathol 118, 276–287.[CrossRef]
    [Google Scholar]
  22. Heath, M. C. ( 2000; ). Hypersensitive response-related death. Plant Mol Biol 44, 321–334.[CrossRef]
    [Google Scholar]
  23. Hirano, S. S. & Upper, C. D. ( 2000; ). Bacteria in the Leaf ecosystem with emphasis on Pseudomonas syringae – a pathogen, ice nucleus and epiphyte. Microbiol Mol Biol Rev 64, 624–653.[CrossRef]
    [Google Scholar]
  24. Hugouvieux, V., Barber, C. E. & Daniels, M. J. ( 1998; ). Entry of Xanthomonas campestris pv. campestris into hydathodes of Arabidopsis thaliana leaves: a system for studying early infection events in bacterial pathogenesis. Mol Plant–Microbe Interact 11, 537–543.[CrossRef]
    [Google Scholar]
  25. Hutcheson, S. W. ( 1999; ). The hrp cluster of Pseudomonas syringae: a pathogenicity island encoding a type III protein translocation complex? In Pathogenicity Islands and Other Mobile Virulence Elements, pp. 309–329. Edited by J. B. Kaper & J. Harker. Washington, DC: American Society for Microbiology.
  26. Jin, Q. & He, S. Y. ( 2001; ). Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science 294, 2556–2558.[CrossRef]
    [Google Scholar]
  27. Jones, J. D. G. & Gutterson, N. ( 1987; ). An efficient mobilizable cosmid vector, pRK7813, and its use in a rapid method for marker exchange in Pseudomonas fluorescens strain HV37a. Gene 61, 299–306.[CrossRef]
    [Google Scholar]
  28. Kado, C. I. & Liu, S. T. ( 1981; ). Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol 145, 1365–1373.
    [Google Scholar]
  29. Keane, P. J., Kerr, A. & New, P. B. ( 1970; ). Crown gall of stone fruit. II. Identification and nomenclature of Agrobacterium isolates. Aust J Biol Sci 23, 585–595.
    [Google Scholar]
  30. Keith, R. C. ( 2002; ). Expression of alginate in response to environmental stress and plant signals. MSc thesis, Oklahoma State University.
  31. Keith, L. M. W. & Bender, C. L. ( 1999; ). AlgT (σ 22) controls alginate production and tolerance to environmental stress in Pseudomonas syringae. J Bacteriol 181, 7176–7184.
    [Google Scholar]
  32. Kidambi, S. P., Sundin, G. W., Palmer D. A., Chakrabarty, A. M. & Bender, C. L. ( 1995; ). Copper as a signal for alginate synthesis in Pseudomonas syringae pv. syringae. Appl Environ Microbiol 61, 2172–2179.
    [Google Scholar]
  33. Levine, A., Tenhaken, R., Dixon, R. & Lamb, C. ( 1994; ). H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583–593.[CrossRef]
    [Google Scholar]
  34. Lyczak, J. B., Cannon, C. L. & Pier, G. B. ( 2002; ). Lung infections associated with cystic fibrosis. Clin Microbiol Rev 15, 194–222.[CrossRef]
    [Google Scholar]
  35. Martin, G. B., Brommonschenkel, S. H., Chunwongse, J., Frary, A., Ganal, M. W., Spivey, R., Wu, T., Earle, E. D. & Tanksley, S. D. ( 1993; ). Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262, 1432–1436.[CrossRef]
    [Google Scholar]
  36. Mathee, K., Ciofu, O., Sternberg, C. & 9 other authors ( 1999; ). Mucoid conversion of Pseudomonas aeruginosa by hydrogen peroxide: a mechanism for virulence activation in the cystic fibrosis lung. Microbiology 145, 1349–1357.[CrossRef]
    [Google Scholar]
  37. Miller, J. H. ( 1972; ). Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  38. Moore, R. A., Starratt, A. N., Ma, S.-W., Morris, V. L. & Cuppels, D. A. ( 1989; ). Identification of a chromosomal region required for biosynthesis of the phytotoxin coronatine by Pseudomonas syringae pv. tomato. Can J Microbiol 35, 910–917.[CrossRef]
    [Google Scholar]
  39. Osman, S. F., Fett, W. F. & Fishman, M. L. ( 1986; ). Exopolysaccharides of the phytopathogen Pseudomonas syringae pv. glycinea. J Bacteriol 166, 66–71.
    [Google Scholar]
  40. Peñaloza-Vázquez, A. & Bender, C. L. ( 1998; ). Characterization of CorR, a transcriptional activator which is required for biosynthesis of the phytotoxin coronatine. J Bacteriol 180, 6252–6259.
    [Google Scholar]
  41. Peñaloza-Vázquez, A., Kidambi, S. P., Chakrabarty, A. M. & Bender, C. L. ( 1997; ). Characterization of the alginate biosynthetic gene cluster in Pseudomonas syringae. pv. syringae. J Bacteriol 179, 4464–4472.
    [Google Scholar]
  42. Plotnikova, J. M., Rahme, L. G. & Ausubel, F. M. ( 2000; ). Pathogenesis of the human opportunistic pathogen Pseudomonas aeruginosa PA14 in Arabidopsis. Plant Physiol 124, 1766–1774.[CrossRef]
    [Google Scholar]
  43. Rahme, L. G., Mindronos, M. N. & Panopoulos, N. J. ( 1992; ). Plant and environmental sensory signals control the expression of hrp genes in Pseudomonas syringae pv. phaseolicola. J Bacteriol 174, 3499–3507.
    [Google Scholar]
  44. Rahme, L. G., Stevens, E. J., Wolfort, S. F., Shao, J., Tompkins, R. G. & Ausubel, F. M. ( 1995; ). Common virulence factors for bacterial pathogenicity in plants and animals. Science 268, 1899–1902.[CrossRef]
    [Google Scholar]
  45. Rich, J. J., Kinscherf, T. G., Kitten, T. & Willis, D. K. ( 1994; ). Genetic evidence that the gacA gene encodes the cognate response regulator for the lemA sensor in Pseudomonas syringae. J Bacteriol 176, 7468–7475.
    [Google Scholar]
  46. Rudolph, K. W. E., Gross, M., Ebrahim-Nesbat, F. & 8 other authors ( 1994; ). The role of extracellular polysaccharides as virulence factors for phytopathogenic pseudomonads and xanthomonads. In Molecular Mechanisms for Bacterial Virulence, pp. 357–378. Edited by C. I. Kado & J. H. Cross. Dordrecht: Kluwer.
  47. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  48. Schaad, N. W. ( 1988; ). Laboratory Guide for Identification of Plant Pathogenic Bacteria. St Paul: American Phytopathological Society Press.
  49. Segal, A. W. & Abo, A. ( 1993; ). The biochemical basis of the NADPH oxidase of phagocytes. Trends Biochem Sci 18, 43–47.[CrossRef]
    [Google Scholar]
  50. Sessa, G. & Martin, G. B. ( 2000; ). Signal recognition and transduction mediated by the tomato Pto kinase: a paradigm of innate immunity in plants. Microbes Infect 13, 1591–1597.
    [Google Scholar]
  51. Shinabarger, D., Berry, A., May, T. B., Rothmel, R., Fialho, A. & Chakrabarty, A. M. ( 1991; ). Purification and characterization of phosphomannose isomerase-guanosine diphospho-d-mannose pyrophosphorylase. A bifunctional enzyme in the alginate biosynthetic pathway of Pseudomonas aeruginosa. J Biol Chem 266, 2080–2088.
    [Google Scholar]
  52. Simpson, J. A., Smith, S. E. & Dean, R. T. ( 1988; ). Alginate inhibition of the uptake of Pseudomonas aeruginosa by macrophages. J Gen Microbiol 134, 29–36.
    [Google Scholar]
  53. Simpson, J. A., Smith, S. E. & Dean, R. T. ( 1989; ). Scavenging by alginate of free radicals released by macrophages. Free Radic Biol Med 6, 347–353.[CrossRef]
    [Google Scholar]
  54. Staskawicz, B. J., Mudgett, M. B., Dangl, J. L. & Galan, J. E. ( 2001; ). Common and contrasting themes of plant and animal diseases. Science 292, 2285–2289.[CrossRef]
    [Google Scholar]
  55. van Dijk, K., Fouts, D. E., Rehm, A. H., Hill, A. R., Collmer, A. & Alfano, J. R. ( 1999; ). The Avr (effector) proteins HrmA (HopPsyA) and AvrPto are secreted in culture from Pseudomonas syringae pathovars via the Hrp (type III) protein secretion system in a temperature- and pH-sensitive manner. J Bacteriol 181, 4790–4797.
    [Google Scholar]
  56. Venisse, J.-S., Gullner, G. & Brisset, M.-N. ( 2001; ). Evidence for the involvement of an oxidative stress in the initiation of infection of pear by Erwinia amylovora. Plant Physiol 125, 2164–2172.[CrossRef]
    [Google Scholar]
  57. Wang, X., Alarcón-Chaidez, F., Peñaloza-Vázquez, A. & Bender, C. L. ( 2002; ). Differential regulation of coronatine biosynthesis in Pseudomonas syringae pv. tomato DC3000 and P. syringae pv. glycinea PG4180. Physiol Mol Plant Pathol 60, 111–120.[CrossRef]
    [Google Scholar]
  58. Wei, W., Plovanich-Jones, A., Deng, W.-L., Jin, Q.-L., Collmer, A., Huang, H.-C. & He, S. Y. ( 2000; ). The gene coding for the Hrp pilus structural protein is required for type III secretion of Hrp and Avr proteins in Pseudomonas syringae pv. tomato. Proc Natl Acad Sci U S A 97, 2247–2252.[CrossRef]
    [Google Scholar]
  59. Wojtaszek, P. ( 1997; ). Oxidative burst: an early plant response to pathogen infection. Biochem J 322, 681–692.
    [Google Scholar]
  60. Wozniak, D. J. & Ohman, D. E. ( 1994; ). Transcriptional analysis of the Pseudomonas aeruginosa genes algR, algB and algD reveals a hierarchy of alginate gene expression, which is modulated by algT. J Bacteriol 176, 6007–6014.
    [Google Scholar]
  61. Xiao, Y., Lu, Y., Heu, S. & Hutcheson, S. W. ( 1992; ). Organization and environmental regulation of the Pseudomonas syringae pv. syringae 61 hrp cluster. J Bacteriol 174, 1734–1741.
    [Google Scholar]
  62. Yu, J., Peñaloza-Vázquez, A., Chakrabarty, A. M. & Bender, C. L. ( 1999; ). Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Mol Microbiol 33, 712–720.[CrossRef]
    [Google Scholar]
  63. Yuan, J. & He, S. Y. ( 1996; ). The Pseudomonas syringae Hrp regulation and secretion system controls the production and secretion of multiple extracellular proteins. J Bacteriol 178, 6399–6402.
    [Google Scholar]
  64. Zhao, Y., Damicone, J. P., Demezas, D. H., Rangaswamy, V. & Bender, C. L. ( 2000; ). Bacterial leaf spot of leafy crucifers in Oklahoma caused by Pseudomonas syringae pv. maculicola. Plant Dis 84, 1015–1020.[CrossRef]
    [Google Scholar]
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