1887

Abstract

Phytoplasma asteris’, onion yellows strain (OY), a mildly pathogenic line (OY-M), is a phytopathogenic bacterium transmitted by leafhoppers. OY-M contains two types of plasmids (EcOYM and pOYM), each of which possesses a gene encoding the putative transmembrane protein, ORF3. A non-insect-transmissible line of this phytoplasma (OY-NIM) has the corresponding plasmids (EcOYNIM and pOYNIM), but pOYNIM lacks . Here we show that in OY-M, is transcribed from two putative promoters and that on EcOYNIM, one of the promoter sequences is mutated and the other deleted. We also show by immunohistochemical analysis that ORF3 is not expressed in OY-NIM-infected plants. Moreover, ORF3 protein seems to be preferentially expressed in OY-M-infected insects rather than in plants. We speculate that ORF3 may play a role in the interactions of OY with its insect host.

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2009-06-01
2020-08-14
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References

  1. Bai X., Zhang J., Ewing A., Miller S. A., Jancso Radek A., Shevchenko D. V., Tsukerman K., Walunas T., Lapidus A.. other authors 2006; Living with genome instability: the adaptation of phytoplasmas to diverse environments of their insect and plant hosts. J Bacteriol188:3682–3696
    [Google Scholar]
  2. Berg M., Melcher U., Fletcher J.. 2001; Characterization of Spiroplasma citri adhesion related protein SARP1, which contains a domain of a novel family designated sarpin. Gene275:57–64
    [Google Scholar]
  3. Berho N., Duret S., Renaudin J.. 2006a; Absence of plasmids encoding adhesion-related proteins in non-insect-transmissible strains of Spiroplasma citri . Microbiology152:873–886
    [Google Scholar]
  4. Berho N., Duret S., Danet J. L., Renaudin J.. 2006b; Plasmid pSci6 from Spiroplasma citri GII-3 confers insect transmissibility to the non-transmissible strain S. citri 44. Microbiology152:2703–2716
    [Google Scholar]
  5. Botti S., Bertaccini A.. 2006; Phytoplasma infection through seed transmission: further observations. InAbstracts, 16th International Organization of Mycoplasmology Conference Cambridge, UK p76
    [Google Scholar]
  6. Christensen N. M., Axelsen K. B., Nicolaisen M., Schulz A.. 2005; Phytoplasmas and their interactions with hosts. Trends Plant Sci10:526–535
    [Google Scholar]
  7. Cordova I., Jones P., Harrison N. A., Oropeza C.. 2003; In situ PCR detection of phytoplasma DNA in embryos from coconut palms with lethal yellowing disease. Mol Plant Pathol4:99–108
    [Google Scholar]
  8. Doi Y., Teranaka M., Yora K., Asuyama H.. 1967; Mycoplasma or PLT group-like microorganisms found in the phloem elements of plants infected with mulberry dwarf, potato witches' broom, aster yellows or paulownia witches' broom. Ann Phytopathol Soc Jpn33:259–266
    [Google Scholar]
  9. Duret S., Berho N., Danet J. L., Garnier M., Renaudin J.. 2003; Spiralin is not essential for helicity, motility, or pathogenicity but is required for efficient transmission of Spiroplasma citri by its leafhopper vector Circulifer haematoceps . Appl Environ Microbiol69:6225–6234
    [Google Scholar]
  10. Firrao G., Garcia-Chapa M., Marzachì C.. 2007; Phytoplasmas: genetics, diagnosis and relationships with the plant and insect host. Front Biosci12:1353–1375
    [Google Scholar]
  11. Fraser C. M., Gocayne J. D., White O., Adams M. D., Clayton R. A., Fleischmann R. D., Bult C. J., Kerlavage A. R., Sutton G.. other authors 1995; The minimal gene complement of Mycoplasma genitalium . Science270:397–403
    [Google Scholar]
  12. Grimm D., Tilly K., Byram R., Stewart P. E., Krum J. G., Bueschel D. M., Schwan T. G., Policastro P. F., Elias A. F., Rosa P. A.. 2004; Outer-surface protein C of the Lyme disease spirochete: a protein induced in ticks for infection of mammals. Proc Natl Acad Sci U S A101:3142–3147
    [Google Scholar]
  13. Gruber T. M., Gross C. A.. 2003; Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol57:441–466
    [Google Scholar]
  14. Hogenhout S. A., Oshima K., Ammar el-D., Kakizawa S., Kingdom H. N., Namba S.. 2008; Phytoplasmas: bacteria that manipulate plants and insects. Mol Plant Pathol9:403–423
    [Google Scholar]
  15. Hovius J. W., van Dam A. P., Fikrig E.. 2007; Tick–host–pathogen interactions in Lyme borreliosis. Trends Parasitol23:434–438
    [Google Scholar]
  16. Jung H. Y., Miyata S., Oshima K., Kakizawa S., Nishigawa H., Wei W., Suzuki S., Ugaki M., Hibi T., Namba S.. 2003; First complete nucleotide sequence and heterologous gene organization of the two rRNA operons in the phytoplasma genome. DNA Cell Biol22:209–215
    [Google Scholar]
  17. Kakizawa S., Oshima K., Kuboyama T., Nishigawa H., Jung H. Y., Sawayanagi T., Tsuchizaki T., Miyata S., Ugaki M., Namba S.. 2001; Cloning and expression analysis of phytoplasma protein translocation genes. Mol Plant Microbe Interact14:1043–1050
    [Google Scholar]
  18. Kakizawa S., Oshima K., Nishigawa H., Jung H. Y., Wei W., Suzuki S., Tanaka M., Miyata S., Ugaki M., Namba S.. 2004; Secretion of immunodominant membrane protein from onion yellows phytoplasma through the Sec protein-translocation system in Escherichia coli . Microbiology150:135–142
    [Google Scholar]
  19. Khan A. J., Botti S., Al-Subhi A. M., Zaidi M. A., Altosaar I., Alma A., Bertaccini A.. 2003; Molecular characterization of the 16S rRNA gene of phytoplasmas detected in two leafhopper species associated with alfalfa plants infected with witches' broom in Oman. Phytopathol Mediterr42:257–267
    [Google Scholar]
  20. Killiny N., Castroviejo M., Saillard C.. 2005; Spiroplasma citri spiralin acts in vitro as a lectin binding to glycoproteins from its insect vector Circulifer haematoceps . Phytopathology95:541–548
    [Google Scholar]
  21. Killiny N., Batailler B., Foissac X., Saillard C.. 2006; Identification of a Spiroplasma citri hydrophilic protein associated with insect transmissibility. Microbiology152:1221–1230
    [Google Scholar]
  22. Kube M., Schneider B., Kuhl H., Dandekar T., Heitmann K., Migdoll A. M., Reinhardt R., Seemüller E.. 2008; The linear chromosome of the plant-pathogenic mycoplasma ‘ Candidatus Phytoplasma mali’. BMC Genomics9:306
    [Google Scholar]
  23. Kuboyama T., Huang C. C., Lu X., Sawayanagi T., Kanazawa T., Kagami T., Matsuda I., Tsuchizaki T., Namba S.. 1998; A plasmid isolated from phytopathogenic onion yellows phytoplasma and its heterogeneity in the pathogenic phytoplasma mutant. Mol Plant Microbe Interact11:1031–1037
    [Google Scholar]
  24. Lee I. M., Davis R. E., Gundersen-Rindal D. E.. 2000; Phytoplasma: phytopathogenic mollicutes. Annu Rev Microbiol54:221–255
    [Google Scholar]
  25. Liefting L. W., Shaw M. E., Kirkpatrick B. C.. 2004; Sequence analysis of two plasmids from the phytoplasma beet leafhopper-transmitted virescence agent. Microbiology150:1809–1817
    [Google Scholar]
  26. Liefting L. W., Andersen M. T., Lough T. J., Beever R. E.. 2006; Comparative analysis of the plasmids from two isolates of “ Candidatus Phytoplasma australiense”. Plasmid56:138–144
    [Google Scholar]
  27. Mulligan M. E., Hawley D. K., Entriken R., McClure W. R.. 1984; Escherichia coli promoter sequences predict in vitro RNA polymerase selectivity. Nucleic Acids Res12:789–800
    [Google Scholar]
  28. Neelakanta G., Li X., Pal U., Liu X., Beck D. S., DePonte K., Fish D., Kantor F. S., Fikrig E.. 2007; Outer surface protein B is critical for Borrelia burgdorferi adherence and survival within Ixodes ticks. PLoS Pathog3:e33
    [Google Scholar]
  29. Nishigawa H., Miyata S., Oshima K., Sawayanagi T., Komoto A., Kuboyama T., Matsuda I., Tsuchizaki T., Namba S.. 2001; In planta expression of a protein encoded by the extrachromosomal DNA of a phytoplasma and related to geminivirus replication proteins. Microbiology147:507–513
    [Google Scholar]
  30. Nishigawa H., Oshima K., Kakizawa S., Jung H. Y., Kuboyama T., Miyata S., Ugaki M., Namba S.. 2002a; Evidence of intermolecular recombination between extrachromosomal DNAs in phytoplasma: a trigger for the biological diversity of phytoplasma?. Microbiology148:1389–1396
    [Google Scholar]
  31. Nishigawa H., Oshima K., Kakizawa S., Jung H. Y., Kuboyama T., Miyata S., Ugaki M., Namba S.. 2002b; A plasmid from a non-insect-transmissible line of a phytoplasma lacks two open reading frames that exist in the plasmid from the wild-type line. Gene298:195–201
    [Google Scholar]
  32. Nishigawa H., Oshima K., Miyata S., Ugaki M., Namba S.. 2003; Complete set of extrachromosomal DNAs from three pathogenic lines of onion yellows phytoplasma and use of PCR to differentiate each line. J Gen Plant Pathol69:194–198
    [Google Scholar]
  33. Oshima K., Kakizawa S., Nishigawa H., Kuboyama T., Miyata S., Ugaki M., Namba S.. 2001a; A plasmid of phytoplasma encodes a unique replication protein having both plasmid- and virus-like domains: clue to viral ancestry or result of virus/plasmid recombination?. Virology285:270–277
    [Google Scholar]
  34. Oshima K., Shiomi T., Kuboyama T., Sawayanagi T., Nishigawa H., Kakizawa S., Miyata S., Ugaki M., Namba S.. 2001b; Isolation and characterization of derivative lines of the onion yellows phytoplasma that do not cause stunting or phloem hyperplasia. Phytopathology91:1024–1029
    [Google Scholar]
  35. Oshima K., Kakizawa S., Nishigawa H., Jung H. Y., Wei W., Suzuki S., Arashida R., Nakata D., Miyata S.. other authors 2004; Reductive evolution suggested from the complete genome sequence of a plant-pathogenic phytoplasma. Nat Genet36:27–29
    [Google Scholar]
  36. Pal U., Yang X., Chen M., Bockenstedt L. K., Anderson J. F., Flavell R. A., Norgard M. V., Fikrig E.. 2004; OspC facilitates Borrelia burgdorferi invasion of Ixodes scapularis salivary glands. J Clin Invest113:220–230
    [Google Scholar]
  37. Purcell A. H.. 1982; Insect vector relationships with prokaryotic plant pathogens. Annu Rev Phytopathol20:397–417
    [Google Scholar]
  38. Shiomi T., Tanaka M., Wakiya H., Zenbayashi R.. 1996; Occurrence of welsh onion yellows. Ann Phytopathol Soc Jpn62:258–260
    [Google Scholar]
  39. Sorensen K. I., Baker K. E., Kelln R. A., Neuhard J.. 1993; Nucleotide pool-sensitive selection of the transcriptional start site in vivo at the Salmonella typhimurium pyrC and pyrD promoters. J Bacteriol175:4137–4144
    [Google Scholar]
  40. Stewart P. E., Byram R., Grimm D., Tilly K., Rosa P. A.. 2005; The plasmids of Borrelia burgdorferi : essential genetic elements of a pathogen. Plasmid53:1–13
    [Google Scholar]
  41. Suzuki S., Oshima K., Kakizawa S., Arashida R., Jung H. Y., Yamaji Y., Nishigawa H., Ugaki M., Namba S.. 2006; Interaction between the membrane protein of a pathogen and insect microfilament complex determines insect-vector specificity. Proc Natl Acad Sci U S A103:4252–4257
    [Google Scholar]
  42. Thomas C. M.. 2004; Evolution and population genetics of bacterial plasmids. In Plasmid Biology pp509–528 Edited by Funnell B. E., Phillips G. J. Washington, DC: American Society for Microbiology;
  43. Tran-Nguyen L. T. T., Gibb K. S.. 2006; Extrachromosomal DNA isolated from tomato big bud and Candidatus Phytoplasma australiense phytoplasma strains. Plasmid56:153–166
    [Google Scholar]
  44. Vivian A., Murillo J., Jackson R. W.. 2001; The roles of plasmids in phytopathogenic bacteria: mobile arsenals?. Microbiology147:763–780
    [Google Scholar]
  45. Wade J. T., Roa D. C., Grainger D. C., Hurd D., Busby S. J., Struhl K., Nudler E.. 2006; Extensive functional overlap between sigma factors in Escherichia coli . Nat Struct Mol Biol13:806–814
    [Google Scholar]
  46. Wagner L. A., Weiss R. B., Driscoll R., Dunn D. S., Gesteland R. F.. 1990; Transcriptional slippage occurs during elongation at runs of adenine or thymine in Escherichia coli . Nucleic Acids Res18:3529–3535
    [Google Scholar]
  47. Webb D. R., Bonfiglioli R. G., Carraro L., Osler R. H., Symons R. H.. 1999; Oligonucleotides as hybridization probes to localize phytoplasmas in host plants and insect vectors. Phytopathology89:894–901
    [Google Scholar]
  48. Weiner J., Herrmann R., Browning G. F.. 2000; Transcription in Mycoplasma pneumoniae . Nucleic Acids Res28:4488–4496
    [Google Scholar]
  49. Weintraub P. G., Beanland L.. 2006; Insect vectors of phytoplasmas. Annu Rev Entomol51:91–111
    [Google Scholar]
  50. Wilson H. R., Chan P. T., Turnbough C. L. Jr. 1987; Nucleotide sequence and expression of the pyrC gene of Escherichia coli K-12. J Bacteriol169:3051–3058
    [Google Scholar]
  51. Wilson H. R., Archer C. D., Liu J. K., Turnbough C. L. Jr. 1992; Translational control of pyrC expression mediated by nucleotide-sensitive selection of transcriptional start sites in Escherichia coli . J Bacteriol174:514–524
    [Google Scholar]
  52. Xiong X. F., Reznikoff W. S.. 1993; Transcriptional slippage during the transcription initiation process at a mutant lac promoter in vivo . J Mol Biol231:569–580
    [Google Scholar]
  53. Yang X. F., Pal U., Alani S. M., Fikrig E., Norgard M. V.. 2004; Essential role for OspA/B in the life cycle of the Lyme disease spirochete. J Exp Med199:641–648
    [Google Scholar]
  54. Ye F., Melcher U., Fletcher J.. 1997; Molecular characterization of a gene encoding a membrane protein of Spiroplasma citri . Gene189:95–100
    [Google Scholar]
  55. Yu J., Wayadande A. C., Fletcher J.. 2000; Spiroplasma citri surface protein P89 implicated in adhesion to cells of the vector, Circulifer tenellus . Phytopathology90:716–722
    [Google Scholar]
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