1887

Abstract

Phytoplasmas are plant-pathogenic bacteria that infect many important crops and cause serious economic losses worldwide. However, owing to an inability to culture phytoplasmas, screening of antimicrobials on media is difficult. The only antimicrobials being used to control phytoplasmas are tetracycline-class antibiotics. In this study, we developed an accurate and efficient screening method to evaluate the effects of antimicrobials using an in vitro plant–phytoplasma co-culture system. We tested 40 antimicrobials, in addition to tetracycline, and four of these (doxycycline, chloramphenicol, thiamphenicol and rifampicin) decreased the accumulation of ‘Candidatus (Ca.) Phytoplasma asteris'. The phytoplasma was eliminated from infected plants by the application of both tetracycline and rifampicin. We also compared nucleotide sequences of rRNAs and amino acid sequences of proteins targeted by antimicrobials between phytoplasmas and other bacteria. Since antimicrobial target sequences were conserved among various phytoplasma species, the antimicrobials that decreased accumulation of ‘Ca. P. asteris' may also have been effective against other phytoplasma species. These approaches will provide new strategies for phytoplasma disease management.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000681
2018-06-28
2019-10-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/164/8/1048.html?itemId=/content/journal/micro/10.1099/mic.0.000681&mimeType=html&fmt=ahah

References

  1. Christensen NM, Axelsen KB, Nicolaisen M, Schulz A. Phytoplasmas and their interactions with hosts. Trends Plant Sci 2005;10:526–535 [CrossRef][PubMed]
    [Google Scholar]
  2. Hogenhout SA, Oshima K, Ammar El-D, Kakizawa S, Kingdom HN et al. Phytoplasmas: bacteria that manipulate plants and insects. Mol Plant Pathol 2008;9:403–423 [CrossRef][PubMed]
    [Google Scholar]
  3. Seemüller E, Garnier M, Schneider B. Mycoplasmas of plants and insects. In Razin S, Herrmann R. (editors) Molecular Biology and Pathogenicity of Mycoplasmas USA: Springer; 2002; pp.91–115
    [Google Scholar]
  4. Bertaccini A, Duduk B. Phytoplasma and phytoplasma diseases: a review of recent research. Phytopathol Mediterr 2010;48:355–378
    [Google Scholar]
  5. Chalak L, Elbitar A, Mourad N, Mortada C, Choueiri E. Elimination of grapevine Bois Noir Phytoplasma by tissue culture coupled or not with heat therapy or hot water treatment. Adv Crop Sci Tech 2013;1:107
    [Google Scholar]
  6. Parmessur Y, Aljanabi S, Saumtally S, Dookun-Saumtally A. Sugarcane yellow leaf virus and sugarcane yellows phytoplasma: elimination by tissue culture. Plant Pathol 2002;51:561–566 [CrossRef]
    [Google Scholar]
  7. Wongkaew P, Fletcher J. Sugarcane white leaf phytoplasma in tissue culture: long-term maintenance, transmission, and oxytetracycline remission. Plant Cell Rep 2004;23:426–434 [CrossRef][PubMed]
    [Google Scholar]
  8. McManus PS, Jones AL. Epidemiology and genetic analysis of streptomycin-resistant Erwinia amylovora from Michigan and evaluation of oxytetracycline for control. Phytopathology 1994;84:627–633 [CrossRef]
    [Google Scholar]
  9. McManus PS, Stockwell VO, Sundin GW, Jones AL. Antibiotic use in plant agriculture. Ann Rev Phytopathol 2002;40:443–465
    [Google Scholar]
  10. Ishiie T, Doi Y, Yora K, Asuyama H. Suppressive effects of antibiotics of tetracycline group on symptom development of mulberry dwarf disease. Jpn J Phytopathol 1967;33:267–275 [CrossRef]
    [Google Scholar]
  11. Doi Y, Teranaka M, Yora K, Asuyama H. 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. Jpn J Phytopathol 1967;33:259–266 [CrossRef]
    [Google Scholar]
  12. McCoy RE. Use of tetracycline antibiotics to control yellows diseases. Plant Dis 1982;66:539–542 [CrossRef]
    [Google Scholar]
  13. Zamharir MG. Phytoplasmas associated with almond witches broom disease: an overview. Afr J Microbiol Res 2011;5:6013–6017
    [Google Scholar]
  14. Kaewmanee C, Hanboonsong Y. Evaluation of the efficiency of various treatments used for sugarcane white leaf phytoplasma control. Bull Insectol 2011;64:S197–S198
    [Google Scholar]
  15. Bradel BG, Preil W, Jeske H. Remission of the free-branching pattern of Euphorbia pulcherrima by tetracycline treatment. J Phytopathol 2000;148:587–590 [CrossRef]
    [Google Scholar]
  16. Stockwell VO, Duffy B. Use of antibiotics in plant agriculture. Rev Sci Tech 2012;31:199–210 [CrossRef][PubMed]
    [Google Scholar]
  17. Ferre R, Badosa E, Feliu L, Planas M, Montesinos E et al. Inhibition of plant-pathogenic bacteria by short synthetic cecropin A-melittin hybrid peptides. Appl Environ Microbiol 2006;72:3302–3308 [CrossRef][PubMed]
    [Google Scholar]
  18. Jorgensen JH, Ferraro MJ. Antimicrobial susceptibility testing: a review of general principles and contemporary practices. Clin Infect Dis 2009;49:1749–1755 [CrossRef][PubMed]
    [Google Scholar]
  19. Chiesa S, Prati S, Assante G, Maffi D, Bianco PA. Activity of synthetic and natural compounds for phytoplasma control. Bull Insectol 2007;60:313
    [Google Scholar]
  20. Kaminska M, Sliwa H. Effect of antibiotics on the symptoms of stunting disease of Magnolia liliiflora plants. J Phytopathol 2003;151:59–63 [CrossRef]
    [Google Scholar]
  21. Miyahara K, Matsuzaki M, Tanaka K, Sako N. A new disease of onion caused by mycoplasma-like organism in Japan. Jpn J Phytopathol 1982;48:551–554 [CrossRef]
    [Google Scholar]
  22. Murashige T, Skoog F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 1962;15:473–497 [CrossRef]
    [Google Scholar]
  23. Oshima K, Ishii Y, Kakizawa S, Sugawara K, Neriya Y et al. Dramatic transcriptional changes in an intracellular parasite enable host switching between plant and insect. PLoS One 2011;6:e23242 [CrossRef][PubMed]
    [Google Scholar]
  24. Feng J, Chen X, Wu Y, Liu W, Liang Q et al. Detection and transcript expression of S-RNase gene associated with self-incompatibility in apricot (Prunus armeniaca L.). Mol Biol Rep 2006;33:215–221 [CrossRef][PubMed]
    [Google Scholar]
  25. Namba S, Kato S, Iwanami S, Oyaizu H, Shiozawa H et al. Detection and differentiation of plant-pathogenic mycoplasmalike organisms using polymerase chain reaction. Phytopathology 1993;83:786–791 [CrossRef]
    [Google Scholar]
  26. Jung HY, Sawayanagi T, Kakizawa S, Nishigawa H, Wei W et al. 'Candidatus Phytoplasma ziziphi', a novel phytoplasma taxon associated with jujube witches'-broom disease. Int J Syst Evol Microbiol 2003;53:1037–1041 [CrossRef][PubMed]
    [Google Scholar]
  27. Oshima K, Miyata S, Sawayanagi T, Kakizawa S, Nishigawa H et al. Minimal set of metabolic pathways suggested from the genome of onion yellows phytoplasma. J Gen Plant Pathol 2002;68:225–236 [CrossRef]
    [Google Scholar]
  28. Jung HY, Miyata S, Oshima K, Kakizawa S, Nishigawa H et al. First complete nucleotide sequence and heterologous gene organization of the two rRNA operons in the phytoplasma genome. DNA Cell Biol 2003;22:209–215 [CrossRef][PubMed]
    [Google Scholar]
  29. Nicholas KB, Nicholas Jr HB. GeneDoc: a tool for editing and annotating multiple sequence alignments. Distributed by authors 1997
  30. Demain AL, Elander RP. The β-lactam antibiotics: past, present, and future. Antonie van Leeuwenhoek 1999;75:5–19 [CrossRef][PubMed]
    [Google Scholar]
  31. Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K et al. Loop-mediated isothermal amplification of DNA. Nucleic Acids Res 2000;28:E63 [CrossRef][PubMed]
    [Google Scholar]
  32. Dégrange S, Renaudin H, Charron A, Pereyre S, Bébéar C et al. Reduced susceptibility to tetracyclines is associated in vitro with the presence of 16S rRNA mutations in Mycoplasma hominis and Mycoplasma pneumoniae. J Antimicrob Chemother 2008;61:1390–1392 [CrossRef][PubMed]
    [Google Scholar]
  33. Taylor-Robinson D, Bébéar C. Antibiotic susceptibilities of mycoplasmas and treatment of mycoplasmal infections. J Antimicrob Chemother 1997;40:622–630 [CrossRef][PubMed]
    [Google Scholar]
  34. Floss HG, Yu TW. Rifamycin-mode of action, resistance, and biosynthesis. Chem Rev 2005;105:621–632 [CrossRef][PubMed]
    [Google Scholar]
  35. Gaurivaud P, Laigret F, Bove JM. Insusceptibility of members of the class Mollicutes to rifampin: studies of the Spiroplasma citri RNA polymerase beta-subunit gene. Antimicrob Agents Chemother 1996;40:858–862[PubMed]
    [Google Scholar]
  36. Mohajeri P, Sadri H, Farahani A, Norozi B, Atashi S. Frequency of mutations associated with rifampicin resistance in Mycobacterium tuberculosis strains isolated from patients in West of Iran. Microb Drug Resist 2015;21:315–319 [CrossRef][PubMed]
    [Google Scholar]
  37. Yang B, Koga H, Ohno H, Ogawa K, Fukuda M et al. Relationship between antimycobacterial activities of rifampicin, rifabutin and KRM-1648 and rpoB mutations of Mycobacterium tuberculosis. J Antimicrob Chemother 1998;42:621–628 [CrossRef][PubMed]
    [Google Scholar]
  38. Hansen JL, Ippolito JA, Ban N, Nissen P, Moore PB et al. The structures of four macrolide antibiotics bound to the large ribosomal subunit. Mol Cell 2002;10:117–128 [CrossRef][PubMed]
    [Google Scholar]
  39. Douthwaite S. Functional interactions within 23S rRNA involving the peptidyltransferase center. J Bacteriol 1992;174:1333–1338 [CrossRef][PubMed]
    [Google Scholar]
  40. Ettayebi M, Prasad SM, Morgan EA. Chloramphenicol-erythromycin resistance mutations in a 23S rRNA gene of Escherichia coli. J Bacteriol 1985;162:551–557[PubMed]
    [Google Scholar]
  41. Okazaki N, Narita M, Yamada S, Izumikawa K, Umetsu M et al. Characteristics of macrolide-resistant Mycoplasma pneumoniae strains isolated from patients and induced with erythromycin in vitro. Microbiol Immunol 2001;45:617–620 [CrossRef][PubMed]
    [Google Scholar]
  42. Matsuoka M, Narita M, Okazaki N, Ohya H, Yamazaki T et al. Characterization and molecular analysis of macrolide-resistant Mycoplasma pneumoniae clinical isolates obtained in Japan. Antimicrob Agents Chemother 2004;48:4624–4630 [CrossRef][PubMed]
    [Google Scholar]
  43. Vester B, Douthwaite S. Macrolide resistance conferred by base substitutions in 23S rRNA. Antimicrob Agents Chemother 2001;45:1–12 [CrossRef][PubMed]
    [Google Scholar]
  44. Schlünzen F, Zarivach R, Harms J, Bashan A, Tocilj A et al. Structural basis for the interaction of antibiotics with the peptidyl transferase centre in eubacteria. Nature 2001;413:814–821 [CrossRef][PubMed]
    [Google Scholar]
  45. Wang H, Dzink-Fox JL, Chen M, Levy SB. Genetic characterization of highly fluoroquinolone-resistant clinical Escherichia coli strains from China: role of acrR mutations. Antimicrob Agents Chemother 2001;45:1515–1521 [CrossRef][PubMed]
    [Google Scholar]
  46. Gruson D, Pereyre S, Renaudin H, Charron A, Bébéar C et al. In vitro development of resistance to six and four fluoroquinolones in Mycoplasma pneumoniae and Mycoplasma hominis, respectively. Antimicrob Agents Chemother 2005;49:1190–1193 [CrossRef][PubMed]
    [Google Scholar]
  47. Dickinson M, Hodgetts J. Phytoplasma: methods and protocols. In Dickinson M, Hodgetts J. (editors) Preface UK: Humana Press; 2013
    [Google Scholar]
  48. Shiomi T, Tanaka M, Sawayanagi T, Yamamoto S, Tsuchizaki T et al. A symptomatic mutant of onion yellows phytoplasma derived from a greenhouse-maintained isolate. Jpn J Phytopathol 1998;64:501–505 [CrossRef]
    [Google Scholar]
  49. Wauchope RD, Yeh S, Linders JB, Kloskowski R, Tanaka K et al. Pesticide soil sorption parameters: theory, measurement, uses, limitations and reliability. Pest Manag Sci 2002;58:419–445 [CrossRef][PubMed]
    [Google Scholar]
  50. Wei W, Kakizawa S, Suzuki S, Jung HY, Nishigawa H et al. In planta dynamic analysis of onion yellows phytoplasma using localized inoculation by insect transmission. Phytopathology 2004;94:244–250 [CrossRef][PubMed]
    [Google Scholar]
  51. Acimovic SG. Disease Management in Apples Using Trunk Injection Delivery of Plant Protective Compounds Doctoral dissertation Michigan State University, USA; 2014
    [Google Scholar]
  52. Oshima K, Maejima K, Namba S. Genomic and evolutionary aspects of phytoplasmas. Front Microbiol 2013;4:230 [CrossRef][PubMed]
    [Google Scholar]
  53. Amram E, Mikula I, Schnee C, Ayling RD, Nicholas RA et al. 16S rRNA gene mutations associated with decreased susceptibility to tetracycline in Mycoplasma bovis. Antimicrob Agents Chemother 2015;59:796–802 [CrossRef][PubMed]
    [Google Scholar]
  54. Zhang M, Powell CA, Zhou L, He Z, Stover E et al. Chemical compounds effective against the citrus Huanglongbing bacterium 'Candidatus Liberibacter asiaticus' in planta. Phytopathology 2011;101:1097–1103 [CrossRef][PubMed]
    [Google Scholar]
  55. Zhang M, Guo Y, Powell CA, Doud MS, Yang C et al. Effective antibiotics against 'Candidatus Liberibacter asiaticus' in HLB-affected citrus plants identified via the graft-based evaluation. PLoS One 2014;9:e111032 [CrossRef][PubMed]
    [Google Scholar]
  56. Kemmitt GM, Deboer G, Ouimette D, Iamauti M. Systemic properties of myclobutanil in soybean plants, affecting control of Asian soybean rust (Phakopsora pachyrhizi). Pest Manag Sci 2008;64:1285–1293 [CrossRef][PubMed]
    [Google Scholar]
  57. Wyss P, Bolsinger M. Translocation of pymetrozine in plants. Pest Manag Sci 1997;50:195–202 [CrossRef]
    [Google Scholar]
  58. Chen I, Dubnau D. DNA uptake during bacterial transformation. Nat Rev Microbiol 2004;2:241–249 [CrossRef][PubMed]
    [Google Scholar]
  59. Gutell RR, Larsen N, Woese CR. Lessons from an evolving rRNA: 16S and 23S rRNA structures from a comparative perspective. Microbiol Rev 1994;58:10–26[PubMed]
    [Google Scholar]
  60. Campbell EA, Korzheva N, Mustaev A, Murakami K, Nair S et al. Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 2001;104:901–912 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000681
Loading
/content/journal/micro/10.1099/mic.0.000681
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error