Journal of Microbiology

The Microbiological Society of Korea (한국미생물학회)
권호 표지

The Endophyte Curtobacterium flaccumfaciens Reduces Symptoms Caused by Xylella fastidiosa in Catharanthus roseus

  • Lacava, Paulo Teixeira (Department of Genetics, Escola Superior de Agricultura 'Luiz de Queiroz', University of Sao Paulo) ;
  • Li, Wenbin (U.S. Department of Agriculture, Animal and Plant Health Inspection Service) ;
  • Araujo, Welington Luiz (Department of Genetics, Escola Superior de Agricultura 'Luiz de Queiroz', University of Sao Paulo) ;
  • Azevedo, Joao Lucio (Department of Genetics, Escola Superior de Agricultura 'Luiz de Queiroz', University of Sao Paulo) ;
  • Hartung, John Stephen (U.S. Department of Agriculture-Agricultural Research Service (USDA-ARS), Fruit Laboratory)
  • Published : 2007.10.30
Download PDF
⟨ Previous Next ⟩

Abstract

Citrus variegated chlorosis (CVC) is a disease of the sweet orange [Citrus sinensis (L.)], which is caused by Xylella fastidiosa subsp. pauca, a phytopathogenic bacterium that has been shown to infect all sweet orange cultivars. Sweet orange trees have been occasionally observed to be infected by Xylella fastidiosa without evidencing severe disease symptoms, whereas other trees in the same grove may exhibit severe disease symptoms. The principal endophytic bacterial species isolated from such CVC-asymptomatic citrus plants is Curtobacterium flaccumfaciens. The Madagascar periwinkle [Citrus sinensis (L.)] is a model plant which has been used to study X. fastidiosa in greenhouse environments. In order to characterize the interactions of X. fastidiosa and C. flaccumfaciens, periwinkle plants were inoculated separately with C. flaccumfaciens, X. fastidiosa, and both bacteria together. The number of flowers produced by the plants, the heights of the plants, and the exhibited disease symptoms were evaluated. PCR-primers for C. flaccumfaciens were designed in order to verify the presence of this endophytic bacterium in plant tissue, and to complement an existing assay for X. fastidiosa. These primers were capable of detecting C. flaccumfaciens in the periwinkle in the presence of X. fastidiosa. X. fastidiosa induced stunting and reduced the number of flowers produced by the periwinkle. When C. flaccumfaciens was inoculated together with X. fastidiosa, no stunting was observed. The number of flowers produced by our doubly- inoculated plants was an intermediate between the number produced by the plants inoculated with either of the bacteria separately. Our data indicate that C. flaccumfaciens interacted with X. fastidiosa in C. roseus, and reduced the severity of the disease symptoms induced by X. fastidiosa. Periwinkle is considered to be an excellent experimental system by which the interaction of C. flaccumfaciens and other endophytic bacteria with X. fastidiosa can be studied.

Keywords

References

  1. Andreote, F.D., M.J.M. Gullo, A.O.S. Lima, W. Maccheroni, Jr., J.L. Azevedo, and W.L. Araujo. 2004. Impact of genetically modified Enterobacter cloacae on indigenous endophytic community of Citrus sinensis seedlings. J. Microbiol. 42, 169-173
  2. Andreote, F.D., P.T. Lacava, C.S. Gai, W.L. Araújo, W. Maccheroni, Jr., L.S. Van Overbeek, J.D. Van Elsas, and J.L. Azevedo. 2006. Model plants for studying the interaction between Methylobacterium mesophilicum and Xylella fastidiosa. Can. J. Microbiol. 52, 419-426 https://doi.org/10.1139/W05-142
  3. Araujo, W.L., W. Maccheroni, Jr., C.I. Aguilar-Vildoso, P.A.V. Barroso, H.O. Saridakis, and J.L. Azevedo. 2001. Variability and interactions between endophytic bacteria and fungi isolated from leaf tissues of citrus rootstocks. Can. J. Microbiol. 47, 229-236 https://doi.org/10.1139/cjm-47-3-229
  4. Araujo, W.L., J. Marcon, W. Maccheroni, Jr., J.D. Van Elsas, J.W.L. Van Vuurde, and J.L. Azevedo. 2002. Diversity of endophytic bacterial populations and their interaction with Xylella fastidiosa in citrus plants. Appl. Environ. Microbiol. 68, 4906-4914 https://doi.org/10.1128/AEM.68.10.4906-4914.2002
  5. Bent, E. and C.P. Chanway. 1998. The growth-promoting effects of a bacterial endophyte on lodgepole pine are partially inhibited by the presence of other rhizobacteria. Can. J. Microbiol. 44, 980-988 https://doi.org/10.1139/cjm-44-10-980
  6. Chanway, C.P. 1997. Inoculation of tree roots with plant growth promoting soil bacteria: an emerging technology for reforestation. Forest Sci. 43, 99-112
  7. Cursino, L. 2005. Ph. D. thesis. University of Sao Paulo, Piracicaba, Sao Paulo, Brazil
  8. Davis, M.J., W.J. French, and N.W. Schaad. 1981. Axenic culture of the bacteria associated with phony disease of peach and plum leaf scald. Curr. Microbiol. 6, 309-314 https://doi.org/10.1007/BF01566883
  9. Della Coletta, F.H., M.A. Takita, A.A. De Souza, C.I. Aguilar- Vildoso, and M.A. Machado. 2001. Differentiation of strains of Xylella fastidiosa by a variable number of tandem repeat analysis. Appl. Environ. Microbiol. 67, 4091-4095 https://doi.org/10.1128/AEM.67.9.4091-4095.2001
  10. Duijff, B.J., V. Gianinazzi-Pearson, and P. Lemanceau. 1997. Involvement of the outer membrane lipopolysaccharides in the endophytic colonization of tomato roots by biocontrol Pseudomonas fluorescens strain WCS417r. New Phytol. 135, 325-344 https://doi.org/10.1046/j.1469-8137.1997.00646.x
  11. Elbeltagy, A., K. Nishioka, H. Suzuki, Y.I. Sato, H. Morisaki, H. Mitsui, and K. Minamisawa. 2000. Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci. Plant Nutr. 46, 617-629 https://doi.org/10.1080/00380768.2000.10409127
  12. Freitag, J.H. 1951. Host range of the Pierce's disease virus of grapes as determined by insect transmission. Phytopathology 41, 920-934
  13. Freitag, J.H. and N.W. Frazier. 1954. Natural infectivity of leafhopper vectors of Pierce's disease virus of grape in California. Phytopathology 44, 7-11
  14. Hallmann, J., A. Quadt-Hallman, W.F. Mahaffee, and J.W. Kloepper 1997. Bacterial endophytes in agricultural crops. Can. J. Microbiol. 43, 895-914 https://doi.org/10.1139/m97-131
  15. Hartung, J.S., J. Beretta, R.H. Brlansky, J. Spisso, and R.F. Lee. 1994. Citrus variegated chlorosis bacterium: axenic culture, pathogenicity, and serological relationships with other strains of Xylella fastidiosa. Phytopathology 84, 591-597 https://doi.org/10.1094/Phyto-84-591
  16. Heuer, H., K. Hartung, G. Wieland, I. Kramer, and K. Smalla 1999. Polynucleotide probes that target a hypervariable region of 16S rRNA genes to identify bacterial isolates corresponding to bands of community fingerprints. Appl. Environ. Microbiol. 65, 1045-1049
  17. Hopkins, D.L. and A.H. Purcell. 2002. Xylella fastidiosa: Cause of Pierce's disease of grapevine and other emergent diseases. Plant Dis. 86, 1056-1066 https://doi.org/10.1094/PDIS.2002.86.10.1056
  18. Jagoueix, S., J.M. Bove, and M. Garnier. 1997. Comparison of the 16S/23S ribosomal intergenic regions of 'Candidatus Liberobacter asiaticum' and 'Candidatus Liberobacter africanum', the two species associated with citrus huanglongbing (greening) disease. Int. J. Syst. Bacteriol. 47, 224-227 https://doi.org/10.1099/00207713-47-1-224
  19. Krishnamurthy, K. and S.S. Gnanamanickam. 1997. Biological control of sheath blight of rice: induction of systemic resistance in rice by plant-associated Pseudomonas spp. Curr. Sci. 72, 331-334
  20. Lacava, P.T., W.L. Araujo, J. Marcon, W. Maccheroni, Jr., and J.L. Azevedo. 2004. Interaction between endophytic bacteria from citrus plants and the phytopathogenic bacterium Xylella fastidiosa, causal agent of citrus variegated chlorosis. Lett. Appl. Microbiol. 39, 55-59 https://doi.org/10.1111/j.1472-765X.2004.01543.x
  21. Lacava, P.T., W.L. Araujo, and J.L. Azevedo. 2007. Evaluation of endophytic colonization of Citrus sinensis and Catharanthus roseus seedlings by endophytic bacteria. J. Microbiol. 45, 11-14
  22. Lacava, P.T., W.B. Li, W.L. Araujo, J.L. Azevedo, and J.S. Hartung. 2006. Rapid, specific and quantitative assays for the detection of the endophytic bacterium Methylobacterium mesophilicum in plants. J. Microbiol. Methods 65, 535-541 https://doi.org/10.1016/j.mimet.2005.09.015
  23. Lazarovits, G. and J. Nowak. 1997. Rhizobacteria for improvement of plant growth and establishment. Hort. Sci. 32, 188-192
  24. Leu, L.S. and C.C. Su. 1993. Isolation, cultivation and pathogenicity of Xylella fastidiosa, the causal bacterium of pear leaf scorch disease in Taiwan. Plant Dis. 77, 642-646 https://doi.org/10.1094/PD-77-0642
  25. Li, W.B., L.C. Donadio, M.J.G. Beretta, V. Rossetti, and O.R. Sempionato. 1997. Practical methods of resistance evaluation of citrus varieties to citrus variegated chlorosis, p. 276-279. In Proceedings of the International Society of Citriculture. Sun City, South Africa. May 12-17, 1996. International Society of Citriculture, Nelspruit, South Africa
  26. Li, W.B., W.D. Pria, Jr., D.C. Teixeira, V.S. Miranda, A.J. Ayres, C.F. Franco, M.G. Costa, C.-X. He, P.I. Costa, and J.S. Hartung. 2001. Coffee leaf scorch caused by a strain of Xylella fastidiosa from citrus. Plant Dis. 85, 501-505 https://doi.org/10.1094/PDIS.2001.85.5.501
  27. Li, W.B., W.D. Pria, Jr., P.T. Lacava, X. Qin, and J.S. Hartung. 2003. Presence of Xylella fastidiosa in sweet orange fruit and seeds and its transmission to seedlings. Phytopathology 93, 953-958 https://doi.org/10.1094/PHYTO.2003.93.8.953
  28. M'Piga, P., R.R. Belanger, T.C. Paulitz, and N. Benhamou 1997. Increased resistance to Fusarium oxysporum f. sp. radicis- licopersici in tomato plants treated with the endophytic bacterium Pseudomonas fluorescens strain 63-28. Physiol. Mol. Plant Pathol. 50, 301-320 https://doi.org/10.1006/pmpp.1997.0088
  29. Monteiro, P.B., J. Renaudin, S. Jagoueix-Eveillard, A.J. Ayres, M. Garnier, and J.M. Bove. 2001. Madagascar periwinkle (Catharanthus roseus): an experimental host plant for the citrus strain of Xylella fastidiosa. Plant Dis. 85, 246-251 https://doi.org/10.1094/PDIS.2001.85.3.246
  30. Pillay, V.J. and J. Nowak. 1997. Inoculum density, temperature and genotype effects on in vitro growth promotion and epiphytic and endophytic colonization of tomato (Lycopersicum esculentum L.) seedlings inoculated with a pseudomonad bacterium. Can. J. Microbiol. 43, 354-361 https://doi.org/10.1139/m97-049
  31. Pooler, M.R. and J.S. Hartung. 1995. Specific PCR detection and identification of Xylella fastidiosa strains causing citrus variegated chlorosis. Curr. Microbiol. 31, 377-381 https://doi.org/10.1007/BF00294703
  32. Raupach, G.S. and J.W. Kloepper. 1998. Mixtures of plant growthpromoting rhizobacteria enhance biological control of multiple cucumber pathogens. Phytopathology 88, 1158-1164 https://doi.org/10.1094/PHYTO.1998.88.11.1158
  33. Sanderlin, R.S. and K.I. Heyderich-Alger. 2000. Evidence that Xylella fastidiosa can cause leaf scorch disease of pecan. Plant Dis. 84, 1282-1286 https://doi.org/10.1094/PDIS.2000.84.12.1282
  34. Sanderlin, R.S. and R.A. Melanson. 2006. Transmission of Xylella fastidiosa through pecan rootstock. HortScience 41, 1455-1456
  35. Schaad, N.W., E. Postnikova, G. Lacy, M. Fatmi, and C.-J. Chang. 2004. Xylella fastidiosa subspecies: X. fastidiosa subsp. piercei, subsp. nov., X. fastidiosa subsp. multiplex, subsp. nov., X. fastidiosa subsp. pauca, subsp. nov.. Syst. Appl. Microbiol. 27, 290-300 https://doi.org/10.1078/0723-2020-00263
  36. Sharma, V.K. and J. Nowak. 1998. Enhancement of verticillium wilt resistance in tomato transplants by in vitro co-culture of seedlings with a plant growth promoting rhizobacteria (Pseudomonas sp. strain PsNJ). Can. J. Microbiol. 44, 528-536 https://doi.org/10.1139/cjm-44-6-528
  37. Steel, R.G.D. and J.H. Torrie. 1980. Principles and procedures of statistics: a biometrical approach. McGraw-Hill, Toronto, Ontario, Canada
  38. Sturz, A.V., B.R. Christie, and B.G. Matheson. 1998. Association of bacterial endophyte populations from red clover and potato crops with potential for beneficial allelopathy. Can. J. Microbiol. 44, 162-167 https://doi.org/10.1139/cjm-44-2-162
  39. Sturz, A.V. and B.G. Matheson. 1996. Populations of endophytic bacteria which influence host-resistance to Erwinia-induced bacterial soft rot in tubers. Plant Soil 184, 265-271 https://doi.org/10.1007/BF00010455
  40. Tor, M., S.H. Mantel, and C. Ainsworth. 1992. Endophytic bacteria expressing beta-glucuronidase cause false positives in transformation of dioscorea species. Plant Cell Rep. 11, 452-456
  41. Wells, J.M., B.C. Raju, H.-Y. Hung, W.G. Weisburg, L. Mandelco- Paul, and D.J. Brenner 1987. Xylella fastidiosa gen. nov., sp. nov: Gram-negative, xylem limited, fastidious plant bacteria related to Xanthomonas spp. Int. J. System. Bacteriol. 37, 136-143 https://doi.org/10.1099/00207713-37-2-136
  42. Zinnier, D.K., P. Lambrecht, N.B. Harris, Z. Feng, D. Kuczmarski, P. Higley, C.A. Ishimaru, A. Arunakumari, R.G. Barletta, and A.K. Vidaver. 2002. Isolation and characterization of endophytic colonizing bacteria from agronomic crops and prairie plants. Appl. Environ. Microbiol. 68, 2198-2208 https://doi.org/10.1128/AEM.68.5.2198-2208.2002