Organization and environmental regulation of the Pseudomonas syringae pv. syringae 61 hrp cluster
10.1128/jb.174.6.1734-1741.1992
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

The ability of Pseudomonas syringae pv. syringae 61 to elicit the hypersensitive response in nonhost plant species has been linked to a cluster of hrp/hrm genes whose expression appears to be environmentally regulated. To understand the genetic organization of this hrp/hrm gene cluster and its expression during the interaction with nonhost plant species better, we constructed a set of chromosomal hrp-uidA fusions in P. syringae pv. syringae 61 by Tn5-gusA1 mutagenesis of the cloned hrp/hrm gene cluster and transferred them into the genome by marker exchange mutagenesis. Complementation analysis employing plasmid-borne Tn5-gusA1 insertions and previously characterized chromosomal TnphoA mutations defined at least eight apparent transcriptional units within the hrp/hrm cluster, several of which were multicistronic. The expression of hrp-uidA fusions in seven of these apparent hrp transcriptional units increased following inoculation into tobacco leaves. Enhanced expression from a representative fusion was detected 1 h after inoculation of tobacco leaves. The induction observed in planta was similar to the levels detected following culture of the bacteria in minimal-salts medium: irrespective of the carbon source. Complex amino acid sources, such as peptone, repressed the expression of P. syringae pv. syringae 61 hrp genes at levels exceeding 0.028%. The results indicate that enhanced expression of hrp genes occurs early in the interaction with nonhost plant species in an apparent response to altered nutritional conditions.

Bibliography

Xiao, Y., Lu, Y., Heu, S., & Hutcheson, S. W. (1992). Organization and environmental regulation of the Pseudomonas syringae pv. syringae 61 hrp cluster. Journal of Bacteriology, 174(6), 1734–1741.

Authors 4
  1. Y Xiao (first)
  2. Y Lu (additional)
  3. S Heu (additional)
  4. S W Hutcheson (additional)
References 55 Referenced 149
  1. Baker , C. J. , N. Mock , M. M. Atkinson , and S. W. Hutcheson . 1990 . Inhibition of the hypersensitive response in tobacco by pectate Iyase digests of cell wall and of polygalacturonic acid . Physiol. Mol. Plant Pathol. 37 : 155 - 167 . (10.1016/0885-5765(90)90008-L) / Physiol. Mol. Plant Pathol. / Inhibition of the hypersensitive response in tobacco by pectate Iyase digests of cell wall and of polygalacturonic acid by Baker C. J. (1990)
  2. Beer S. V. D. W. Bauer X. H. Jiang R. J. Laby B. J. Sneath Z.-M. Wei D. A. Wilcox and C. H. Zumoff. 1991. The hrp gene cluster of Erwinia amylovora p. 53-60. In H. Hennecke and D. P. S. Verma (ed.) Advances in molecular genetics of plant-microbe interactions vol. 1. Kluwer Academic Publishers Dordrecht The Netherlands. (10.1007/978-94-015-7934-6_8)
  3. Bertoni , G. , and D. Mills . 1987 . A simple method to monitor growth of bacterial populations in leaf tissue . Phytopathology 77 : 832 - 835 . (10.1094/Phyto-77-832) / Phytopathology / A simple method to monitor growth of bacterial populations in leaf tissue by Bertoni G. (1987)
  4. Bradford , M. M. 1976 . A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding . Anal. Biochem. 72 : 248 - 254 . (10.1016/0003-2697(76)90527-3) / Anal. Biochem. / A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding by Bradford M. M. (1976)
  5. de Bruin , F. J. , and J. R. Lupski . 1984 . The use of transposon TnS mutagenesis in the rapid generation of correlated physical and genetic maps of DNA segments cloned into multicopy plasmids-a review . Gene 27 : 131 - 149 . (10.1016/0378-1119(84)90135-5) / Gene / The use of transposon TnS mutagenesis in the rapid generation of correlated physical and genetic maps of DNA segments cloned into multicopy plasmids-a review by de Bruin F. J. (1984)
  6. Ditta , G. , S. Stanfield , D. Corbin , and D. R. Helinski . 1980 . Broad host range DNA cloning system for gram negative bacteria: construction of a gene bank of Rhizobium meliloti . Proc. Natl. Acad. Sci. USA 77 : 7347 - 7351 . (10.1073/pnas.77.12.7347) / Proc. Natl. Acad. Sci. USA / Broad host range DNA cloning system for gram negative bacteria: construction of a gene bank of Rhizobium meliloti by Ditta G. (1980)
  7. Dixon , R. A. , and C. Lamb . 1990 . Molecular communication in interactions between plant and microbial pathogens. Annu . Rev. Plant Physiol. 41 : 339 - 367 . / Rev. Plant Physiol. / Molecular communication in interactions between plant and microbial pathogens. Annu by Dixon R. A. (1990)
  8. Dower , W. J. , J. F. Miller , and C. W. Ragsdale . 1988 . High efficiency transformation of Escherichia coli by high voltage electroporation . Nucleic Acids Res. 16 : 6127 - 6145 . (10.1093/nar/16.13.6127) / Nucleic Acids Res. / High efficiency transformation of Escherichia coli by high voltage electroporation by Dower W. J. (1988)
  9. Fellay R. L. G. Rahme M. N. Mindrinos R. D. Frederick A. Pisi and N. J. Panopoulos. 1991. Genes and signals controlling the Pseudomonas syringae pv. phaseolicola-plant interaction p. 45-52. In H. Hennecke and D. P. S. Verma (ed.) Advances in molecular genetics of plant-microbe interactions vol. 1. Kluwer Academic Publishers Dordrecht The Netherlands. (10.1007/978-94-015-7934-6_7)
  10. Hanahan , D. 1983 . Studies on transformation of Escherichia coli with plasmids . J. Mol. Biol. 166 : 557 - 580 . (10.1016/S0022-2836(83)80284-8) / J. Mol. Biol. / Studies on transformation of Escherichia coli with plasmids by Hanahan D. (1983)
  11. Heu , S. , and S. W. Hutcheson . 1991 . Pseudomonas syringae pv. syringae hrplhrm genes encode avirulence functions in P. syringae pv. glycinea race 4 . Phytopathology 81 : 702 - 703 . / Phytopathology / Pseudomonas syringae pv. syringae hrplhrm genes encode avirulence functions in P. syringae pv. glycinea race 4 by Heu S. (1991)
  12. Heu , S. , and S. W. Hutcheson . 1991 . Molecular characterization of the Pseudomonas syringae pv. syringae 61 hrnnA locus . Phytopathology 81 : 1245 . / Phytopathology / Molecular characterization of the Pseudomonas syringae pv. syringae 61 hrnnA locus by Heu S. (1991)
  13. Heu S. Y. Lu and S. W. Hutcheson. Unpublished data.
  14. Huang H.-C. and A. Colimer. Unpublished data.
  15. Huang , H. - C. , S. W. Hutcheson , and A. Collmer . 1991 . Characterization of the hrp cluster from Pseudomonas syringae pv. syringae 61 and TnphoA tagging of genes encoding exported or membrane-spanning Hrp proteins . Mol. Plant-Microbe Interact. 4 : 469 - 476 . (10.1094/MPMI-4-469) / Mol. Plant-Microbe Interact. / Characterization of the hrp cluster from Pseudomonas syringae pv. syringae 61 and TnphoA tagging of genes encoding exported or membrane-spanning Hrp proteins by Huang H. (1991)
  16. Huang , H. - C. , R. Schuurink , T. P. Denny , M. M. Atkinson , C. J. Baker , I. Yucel , S. W. Hutcheson , and A. Collmer . 1988 . Molecular cloning of a Pseudomonas syringae pv. syringae gene cluster that enables Pseudomonasfluorescens to elicit the hypersensitive response in tobacco plants . J. Bacteriol. 170 : 4748 - 4756 . (10.1128/JB.170.10.4748-4756.1988) / J. Bacteriol. / Molecular cloning of a Pseudomonas syringae pv. syringae gene cluster that enables Pseudomonasfluorescens to elicit the hypersensitive response in tobacco plants by Huang H. (1988)
  17. Hutcheson , S. W. , C. J. Baker , and A. Collmer . 1989 . Elicitation of the hypersensitive response by Pseudomonas syringae . Physiol. Plant. 76 : 155 - 163 . (10.1111/j.1399-3054.1989.tb05625.x) / Physiol. Plant. / Elicitation of the hypersensitive response by Pseudomonas syringae by Hutcheson S. W. (1989)
  18. .Hutcheson S. W. S. Heu H. C. Huang T.-H. Li Y. Lu and Y. Xiao. The hrp genes of Pseudomonas syringae: an evaluation of their role in determining nonhost resistance. In D. Bills and S. D. King (ed.) Biotechnology and plant protection: bacterial pathogenesis and plant resistance in press. Butterworths London.
  19. Huynh , T. , D. Dahlbeck , and B. J. Staskawicz . 1989 . Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity . Science 245 : 1374 - 1377 . (10.1126/science.2781284) / Science / Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity by Huynh T. (1989)
  20. Jefferson , R. A. 1987 . Assaying chimeric genes in plants: the GUS gene fusion system . Plant Mol. Biol. Rep. 5 : 387 - 405 . (10.1007/BF02667740) / Plant Mol. Biol. Rep. / Assaying chimeric genes in plants: the GUS gene fusion system by Jefferson R. A. (1987)
  21. Keen , N. T. 1990 . Gene for gene complementarity in plantpathogen interactions. Annu . Rev. Genet. 24 : 447 - 463 . (10.1146/annurev.ge.24.120190.002311) / Rev. Genet. / Gene for gene complementarity in plantpathogen interactions. Annu by Keen N. T. (1990)
  22. Keen N. T. and M. J. Holliday. 1982. Recognition of bacterial pathogens by plants p. 179-220. In M. S. Mount and G. H. Lacy (ed.) Phytopathogenic prokaryotes vol. 2. Academic Press Inc. New York. (10.1016/B978-0-12-509002-5.50018-5)
  23. Keen , N. T. , and B. J. Staskawicz . 1988 . Host range determinants in plant pathogens and symbionts. Annu . Rev. Microbiol. 42 : 421 - 440 . (10.1146/annurev.mi.42.100188.002225) / Rev. Microbiol. / Host range determinants in plant pathogens and symbionts. Annu by Keen N. T. (1988)
  24. . Keppler , L. D. , C. J. Baker , and M. M. Atkinson . 1989 . Active oxygen production during a bacteria-induced hypersensitive reaction in tobacco suspension cells . Phytopathology 79 : 974 - 978 . (10.1094/Phyto-79-974) / Phytopathology / Active oxygen production during a bacteria-induced hypersensitive reaction in tobacco suspension cells by Keppler L. D. (1989)
  25. King , E. O. , M. K. Ward , and D. E. Raney . 1954 . Two simple media for the demonstration of pyocyanin and fluorescein . J. Lab. Clin. Med. 44 : 301 - 307 . / J. Lab. Clin. Med. / Two simple media for the demonstration of pyocyanin and fluorescein by King E. O. (1954)
  26. Klement Z. 1982. Hypersensitivity p. 149-177. In M. S. Mount and G. H. Lacy (ed.) Phytopathogenic prokaryotes vol. 2. Academic Press Inc. New York. (10.1016/B978-0-12-509002-5.50017-3)
  27. Kramer P. J. 1983. Water relations of plants. Academic Press Inc. New York. (10.1016/B978-0-12-425040-6.50005-9)
  28. Li , T. - H. , S. A. Benson , and S. W. Hutcheson . 1992 . Phenotypic expression of the Pseudomonas syringae pv. syringae 61 hrpl hrm gene cluster in Escherichia coli MC4100 requires a functional porin . J. Bacteriol. 174 : 1742 - 1749 . (10.1128/JB.174.6.1742-1749.1992) / J. Bacteriol. / Phenotypic expression of the Pseudomonas syringae pv. syringae 61 hrpl hrm gene cluster in Escherichia coli MC4100 requires a functional porin by Li T. (1992)
  29. Lindgren , P. B. , R. D. Frederick , A. G. Govindarajin , N. J. Panopoulos , B. J. Staskawicz , and S. E. Lindow . 1989 . An ice nucleation reporter gene system: identification of inducible pathogenicity genes in Pseudomonas syningae pv. phaseolicola . EMBO J. 8 : 2990 - 3001 . (10.1002/j.1460-2075.1989.tb03508.x) / EMBO J. / An ice nucleation reporter gene system: identification of inducible pathogenicity genes in Pseudomonas syningae pv. phaseolicola by Lindgren P. B. (1989)
  30. Lindgren , P. B. , N. J. Panopoulos , B. J. Staskawicz , and D. Dahlbeck . 1988 . Genes required for pathogenicity and hypersensitivity are conserved and interchangeable among pathovars of Pseudomonas syringae . Mol. Gen. Genet. 211 : 499 - 506 . (10.1007/BF00425707) / Mol. Gen. Genet. / Genes required for pathogenicity and hypersensitivity are conserved and interchangeable among pathovars of Pseudomonas syringae by Lindgren P. B. (1988)
  31. Lindgren , P. B. , R. C. Peet , and N. J. Panopoulos . 1986 . Gene cluster of Pseudomonas syringae pv. "phaseolicola " controls pathogenicity of bean plants and hypersensitivity on nonhost J. Bacteriol. 168 : 512 - 522 . (10.1128/JB.168.2.512-522.1986) / J. Bacteriol. / Gene cluster of Pseudomonas syringae pv. "phaseolicola by Lindgren P. B. (1986)
  32. Long , S. R. 1989 . Rhizobium genetics. Annu . Rev. Genet. 23 : 483 - 506 . (10.1146/annurev.ge.23.120189.002411) / Rev. Genet. / Rhizobium genetics. Annu by Long S. R. (1989)
  33. Lu Y. and S. W. Hutcheson. Unpublished data.
  34. Maas , R. 1983 . An improved colony hybridization method with significantly increased sensitivity for detection of single genes . Plasmid 10 : 296 - 298 . (10.1016/0147-619X(83)90045-8) / Plasmid / An improved colony hybridization method with significantly increased sensitivity for detection of single genes by Maas R. (1983)
  35. Manoil , C. , and J. Beckwith . 1985 . TnphoA: a transposon probe for protein export signals . Proc. Natl. Acad. Sci. USA 82 : 8129 - 8133 . (10.1073/pnas.82.23.8129) / Proc. Natl. Acad. Sci. USA / TnphoA: a transposon probe for protein export signals by Manoil C. (1985)
  36. Mo , Y. - Y. , and D. C. Gross . 1991 . Plant signal molecules activate the syrB gene, which is required for syringomycin production by Pseudomonas syningae pv. syringae . J. Bacteriol. 173 : 5784 - 5792 . (10.1128/JB.173.18.5784-5792.1991) / J. Bacteriol. / Plant signal molecules activate the syrB gene, which is required for syringomycin production by Pseudomonas syningae pv. syringae by Mo Y. (1991)
  37. Nester E. W. and M. P. Gordon. 1991. Molecular strategies in the interaction between Agrobacterium and its hosts p. 3-9. In H. Hennecke and D. P. S. Verma (ed.) Advances in molecular genetics of plant-microbe interactions vol. 1. Kluwer Academic Publishers Dordrecht The Netherlands. (10.1007/978-94-015-7934-6_1)
  38. Niepold , F. , D. Anderson , and D. Mills . 1985 . Cloning determinants of pathogenesis from Pseudomonas syringae pathovar syringae . Proc. Natl. Acad. Sci. USA 82 : 406 - 410 . (10.1073/pnas.82.2.406) / Proc. Natl. Acad. Sci. USA / Cloning determinants of pathogenesis from Pseudomonas syringae pathovar syringae by Niepold F. (1985)
  39. Perbal B. 1988. A practical guide to molecular cloning 2nd ed. John Wiley & Sons Inc. New York.
  40. Rahme , L. G. , M. N. Mindrinos , and N. J. Panopoulos . 1991 . Genetic and transcriptional organization of the hip cluster of Pseudomonas syringae pv. phaseolicola . J. Bacteriol. 173 : 575 - 586 . (10.1128/JB.173.2.575-586.1991) / J. Bacteriol. / Genetic and transcriptional organization of the hip cluster of Pseudomonas syringae pv. phaseolicola by Rahme L. G. (1991)
  41. Ruvkin , G. B. , and F. M. Ausubel . 1981 . A general method for site-directed mutagenesis in prokaryotes . Nature (London) 289 : 85 - 88 . (10.1038/289085a0) / Nature (London) / A general method for site-directed mutagenesis in prokaryotes by Ruvkin G. B. (1981)
  42. Sambrook J. E. F. Fritsch and T. Maniatis. 1989. Molecular cloning: a laboratory manual 2nd ed. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  43. Sasser , M. 1982 . Inhibition by antibacterial compounds of the hypersensitive reaction induced by Pseudomonas pisi in tobacco . Phytopathology 72 : 1513 - 1517 . (10.1094/Phyto-72-1513) / Phytopathology / Inhibition by antibacterial compounds of the hypersensitive reaction induced by Pseudomonas pisi in tobacco by Sasser M. (1982)
  44. Sharma , S. B. , and E. R. Signor . 1990 . Temporal and spatial regulation of the symbiotic genes of Rhizobium meliloti in planta revealed by transposon TnS-gusA . Genes Dev. 4 : 344 - 356 . (10.1101/gad.4.3.344) / Genes Dev. / Temporal and spatial regulation of the symbiotic genes of Rhizobium meliloti in planta revealed by transposon TnS-gusA by Sharma S. B. (1990)
  45. Shaw , J. J. , and C. I. Kado . 1986 . Development of a Vibrio bioluminescence gene-set to monitor phytopathogenic bacteria during the ongoing disease process in a non-disruptive manner . Bio/Technology 4 : 560 - 564 . / Bio/Technology / Development of a Vibrio bioluminescence gene-set to monitor phytopathogenic bacteria during the ongoing disease process in a non-disruptive manner by Shaw J. J. (1986)
  46. Silhavy T. J. M. L. Berman and L. W. Enquist. 1984. Experiments with gene fusions. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  47. Staskawicz , B. , D. Dahlbeck , N. Keen , and C. Napoli . 1987 . Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea . J. Bacteriol. 169 : 5789 - 5794 . (10.1128/JB.169.12.5789-5794.1987) / J. Bacteriol. / Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea by Staskawicz B. (1987)
  48. Tyree , M. T. , and H. T. Hammel . 1972 . The measurement of turgor pressure and the water relations of plants by the pressure bomb technique . J. Exp. Bot. 23 : 267 - 282 . (10.1093/jxb/23.1.267) / J. Exp. Bot. / The measurement of turgor pressure and the water relations of plants by the pressure bomb technique by Tyree M. T. (1972)
  49. Willis , K. , J. J. Rich , and E. M. Hrabak . 1990 . The hip genes of phytopathogenic bacteria . Mol. Plant-Microbe Interact. 4 : 132 - 138 . (10.1094/MPMI-4-132) / Mol. Plant-Microbe Interact. / The hip genes of phytopathogenic bacteria by Willis K. (1990)
  50. Winins , S. 1990 . Transcriptional induction of an Agrobacterium regulatory gene at tandem promotors by plant-released phenolic compounds, phosphate starvation, and acidic growth media . J. Bacteriol. 172 : 2433 - 2438 . (10.1128/JB.172.5.2433-2438.1990) / J. Bacteriol. / Transcriptional induction of an Agrobacterium regulatory gene at tandem promotors by plant-released phenolic compounds, phosphate starvation, and acidic growth media by Winins S. (1990)
  51. Xiao , Y. , and S. W. Hutcheson . 1991 . Environmental regulation of Pseudomonas synngae pv. synngae 61 hip genes . Phytopathology 81 : 705 . / Phytopathology / Environmental regulation of Pseudomonas synngae pv. synngae 61 hip genes by Xiao Y. (1991)
  52. Xiao , Y. , and S. W. Hutcheson . 1991 . Transcriptional organization and expression of the Pseudomonas syringae pv. syningae 61 hip gene cluster . Phytopathology 81 : 1245 - 1246 . / Phytopathology / Transcriptional organization and expression of the Pseudomonas syringae pv. syningae 61 hip gene cluster by Xiao Y. (1991)
  53. Xiao Y. and S. W. Hutcheson. Unpublished data.
  54. Xiao Y. Y. Lu and S. W. Hutcheson. Unpublished data.
  55. Yucel , I. , Y. Xiao , and S. W. Hutcheson . 1989 . Influence of Pseudomonas synngae culture conditions on initiation of the hypersensitive response of cultured tobacco cells . Appl. Environ. Microbiol. 55 : 1724 - 1729 . (10.1128/AEM.55.7.1724-1729.1989) / Appl. Environ. Microbiol. / Influence of Pseudomonas synngae culture conditions on initiation of the hypersensitive response of cultured tobacco cells by Yucel I. (1989)
Dates
Type When
Created 8 years, 9 months ago (Nov. 4, 2016, 3:52 p.m.)
Deposited 4 years ago (July 29, 2021, 1:49 p.m.)
Indexed 3 weeks, 2 days ago (July 30, 2025, 8:34 p.m.)
Issued 33 years, 5 months ago (March 1, 1992)
Published 33 years, 5 months ago (March 1, 1992)
Published Print 33 years, 5 months ago (March 1, 1992)
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@article{Xiao_1992, title={Organization and environmental regulation of the Pseudomonas syringae pv. syringae 61 hrp cluster}, volume={174}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.174.6.1734-1741.1992}, DOI={10.1128/jb.174.6.1734-1741.1992}, number={6}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Xiao, Y and Lu, Y and Heu, S and Hutcheson, S W}, year={1992}, month=mar, pages={1734–1741} }