Skip to main content
Log in

Isolation and Characterization of Putative Endophytic Bacteria Antagonistic to Phoma tracheiphila and Verticillium albo-atrum

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

A collection of 200 bacterial isolates recovered from citrus plants (Citrus limon, Citrus sinensis, and Citrus reticulata), Medicago truncatula and Laurus nobilis, was established. In vitro screening indicated that 28 isolates exhibited an inhibitory activity against the vascular pathogens Phoma tracheiphila and Verticillium albo-atrum. Isolates were screened according to their hydrolytic activities, plant growth-promoting bacteria (PGPB) abilities, as well as for the presence of nonribosomal peptide synthetase (NRPS) genes responsible of the lipopeptide biosynthesis. The results were positive for 16 isolates which exhibited at least two PGPB activities and a single NRPS gene. Genetic diversity of the selected isolates was studied using random amplified polymorphic DNA (RAPD) and repetitive element PCR (REP) tools that showed clustering of strains into three major groups (I, II, and III) (i, ii, and iii), respectively. Clustering was further confirmed by the 16S rDNA sequencing that assigned nine isolates to Bacillus velezensis, four isolates to Bacillus methyltrophicus, one isolate to Bacillus amyloliquefaciens, and two isolates to Bacillus mojavensis. Organ-bacterial genotype interaction as well as positive correlation with NRPS genes are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Agrios, G. N. (2005). Plant pathology (5th ed.). USA: Elsevier Academic Press.

    Google Scholar 

  2. Perrotta, G., & Graniti, A. (1988). In I. M. Smith, J. Dunez, R. A. Lelliot, D. H. Phillips, & S. A. Archer (Eds.), European handbook of plant diseases: Phoma tracheiphila (pp. 396–398). Oxford: Blackwell Scientific Publications.

    Google Scholar 

  3. Erwin, J. A. G. (1973). Australasian Plant Pathology Society Newsletter, 2, 18.

    Article  Google Scholar 

  4. Klosterman, S. J., Atallah, Z. K., Vallad, G. E., & Subbarao, K. V. (2009). Annual Review of Phytopathology, 47, 39–62.

    Article  CAS  Google Scholar 

  5. Ben, C., Toueni, M., Montanari, S., Tardin, M. C., Fervel, M., Negahi, A., Saint-Pierre, L., Mathieu, G., Gras, M. C., Noël, D., Prospéri, J. M., Pilet-Nayel, M. L., Baranger, A., Huguet, T., Julier, B., Rickauer, M., & Gentzbittel, L. (2013). Journal of Experimental Botany, 64, 317–332.

    Article  CAS  Google Scholar 

  6. Thanassoulopoulos, C. C., and Manos, B. D. (1992). Proc Int Citrus Congr 7th Acireale International Society of Citriculture, Italy

  7. Fravel, D. R., Lewis, J. A., & Chittams, J. L. (1995). Phytopathology, 85, 165–68.

    Article  Google Scholar 

  8. Nagtzaam, M. P. M., Bollen, G. J., & Termorshuizen, A. J. (1998). Journal of Phytopathology, 146, 165–73.

    Article  CAS  Google Scholar 

  9. Spink, D. S., & Rowe, R. C. (1989). Plant Disease, 73, 230–36.

    Article  Google Scholar 

  10. Grasso, S., & Tirrò, A. (1982). Tecnica Agricola, 3, 1–10.

    Google Scholar 

  11. Paradies, M., De Cicco, V., & Salerno, M. (1985). La Difesa delle Piante, 2, 179–180.

    Google Scholar 

  12. Rosciglione, B., Burgio, A., Bottalico, A., & Laviola, C. (1991). Journal of Phytopathology, 133, 23–28.

    Article  Google Scholar 

  13. Haggag, W. M. (2010). Life Sciences, 7, 57–62.

    Google Scholar 

  14. Alstroëm, S. (2001). Journal of Phytopathology, 149, 57–64.

    Article  Google Scholar 

  15. Stoltzfus, J. R., So, R., Malarvithi, P. P., Ladha, J. K., & de Bruijn, F. J. (1998). Plant and Soil, 194, 25–36.

    Article  Google Scholar 

  16. Berg, G., Krechel, A., Ditz, M., Sikora, R. A., Ulrich, A., & Hallmann, J. (2005). FEMS Microbiology Ecology, 51, 215–229.

    Article  CAS  Google Scholar 

  17. Cho, S. J., Park, S. R., Kim, M. K., Lim, W. J., Ryu, S. K., An, C. L., Hong, S. Y., Lee, Y. H., Jeong, S. G., Cho, Y. U., & Yun, H. D. (2002). Bioscience, Biotechnology, and Biochemistry, 66, 1270–1275.

    Article  CAS  Google Scholar 

  18. Dujiff, B. J., Gianinazzi-Pearson, V., & Lemanceau, P. (1997). New Phytologist 135, 325-334 17.

  19. Safiyazov, J. S., Mannanov, R. N., & Sattarova, R. K. (1995). Field Crops Research, 43, 51–54.

    Article  Google Scholar 

  20. Coco, V., Grimaldi, V., Grasso, S., Catara, A. (2003). Atti del Convegno Mi.P.A.F. “Ricerche e Sperimentazioninel Settore dell’Agrumicoltura Italiana”, Acireale, Italy.

  21. Kalai-Grami, L., Ben Slimane, I., Mnari-Hattab, M., Rezgui, S., Aouani, M. A., Hajlaoui, M. R., Limam, F. (2014). World Journal of Microbiology and Biotechnology, 30, 529–538.

  22. Sturz, A. V., Christie, B. R., Matheson, B. G., Arsenault, W. J., & Buchanan, N. A. (1999). Plant Pathology, 48, 360–369.

    Article  Google Scholar 

  23. Puentea, M., Ching, Y., Li, B., & Yoav Bashana, C. (2009). Environmental and Experimental Botany, 66, 402–408.

    Article  Google Scholar 

  24. Mpiga, P., Bélanger, R. R., Paulitz, T. C., & Benhamou, N. (1997). Physiological and Molecular Plant Pathology, 50, 301–320.

    Article  Google Scholar 

  25. Doty, S. L. (2008). New Phytologist, 179, 318–333.

    Article  CAS  Google Scholar 

  26. Strobel, G., Daisy, B., Castillo, U., & Harper, J. (2004). Journal of Natural Products, 67, 257–268.

    Article  CAS  Google Scholar 

  27. Strobel, G., & Daisy, B. (2003). Microbiology and Molecular Biology, 67, 491–502.

    Article  CAS  Google Scholar 

  28. Lakhoua, H. (1997). Revue INAT, 1, 181–182.

  29. Gachet, J. P., & Elmir, A. (1972). Annales INRAT, 45, 3–45.

  30. El Baltagy, A., Nishioka, K., Suzuki, H., Sato, T., Sato, Y. I., Morisaki, H., Mitsui, H., & Minamisawa, K. (2000). Soil Science & Plant Nutrition, 46, 617–629.

    Article  Google Scholar 

  31. Sadfi, N., Cherif, M., Fliss, I., Boudabbous, A., & Antoun, H. (2001). Journal of Plant Pathology, 83, 101–118.

    CAS  Google Scholar 

  32. Whipps, J. M. (1987). New Phytologist, 107, 127–142.

    Article  Google Scholar 

  33. Korsten, L., De Jager, E. S., De Villurs, E. E., Lourens, A., & Wehner, F. C. (1995). Plant Disease, 79, 1149–1156.

    Article  Google Scholar 

  34. Kasana, R. C., Salwan, R., Dhar, H., Dutt, S., & Gulati, A. (2008). Current Microbiology, 57, 503–507.

    Article  CAS  Google Scholar 

  35. Laurent, P., Bouchon, L., Guespin-Michel, J. F., & Orange, N. (2000). Applied and Environmental Microbiology, 66, 1538–1543.

    Article  CAS  Google Scholar 

  36. Fransen, N. G., O’Connell, M. B., & Arendt, E. K. (1997). International Journal of Food Microbiology, 36, 235–239.

    Article  CAS  Google Scholar 

  37. Kamil, Z., Rizk, M., Saleh, M., & Moustafa, S. (2007). Global Journal Molecular Science, 2, 57–66.

    Google Scholar 

  38. Hsu, S. C., Hsu, J. L. S. C., & Lockwood, J. L. (1975). Applied Microbiology, 29, 422–426.

    CAS  Google Scholar 

  39. Liba, C. M., Ferrara, F. I. S., Manfio, G. P., Fantinatti-Garboggini, F., Albuquerque, R. C., Pavan, C., Ramos, P. L., Moreira-Filho, C. A., & Barbosa, H. R. (2006). Journal of Applied Microbiology, 101, 1076–1086.

    Article  CAS  Google Scholar 

  40. Schwyn, B., & Neilands, J. B. (1987). Analytical Biochemistry, 160, 47–56.

    Article  CAS  Google Scholar 

  41. Bric, J. M., Bostock, R. M., & Silverstone, S. E. (1991). Applied and Environmental Microbiology, 57, 535–538.

    CAS  Google Scholar 

  42. Versalovic, J., Koeuth, T., & Lupski, J. R. (1991). Nucleic Acids Research, 19, 6823–6831.

    Article  CAS  Google Scholar 

  43. Laguerre, G., Van Berkum, P., Amarger, N., & Prevost, D. (1997). Applied and Environmental Microbiology, 63, 4748–4758.

    CAS  Google Scholar 

  44. Weisburg, W. G., Barns, S. M., Pelletier, D. A., & Lane, D. J. (1991). Journal of Bacteriology, 173, 697–703.

    CAS  Google Scholar 

  45. Wagenaar, M. M., & Clardy, J. (2001). Journal of Natural Products, 64, 1006–1009.

    Article  CAS  Google Scholar 

  46. Wang, L. T., Lee, F. L., Tai, C. J., & Kuo, H. P. (2008). International Journal of Systematic and Evolutionary Microbiology, 58, 671–675.

    Article  CAS  Google Scholar 

  47. Manzano, M., Giusto, C., Iacumin, L., Cantoni, C., & Comi, G. (2009). Food Microbiology, 26, 259–264.

    Article  CAS  Google Scholar 

  48. Ronimus, R. S., Parker, L. E., Turner, N., Poudel, S., Rückert, A., & Morgan Hugh, W. (2003). International Journal of Food Microbiology, 85, 45–61.

    Article  CAS  Google Scholar 

  49. Gurtler, V., & Mayall, B. C. (2001). International Journal of Systematic and Evolutionary Microbiology, 51, 3–16.

    Article  CAS  Google Scholar 

  50. Ronimus, R. S., Parker, L. E., & Morgan, H. W. (1997). FEMS Microbiology Letters, 147, 75–79.

    Article  CAS  Google Scholar 

  51. Sorokulova, I. B., Reva, O. N., Smirnov, V. V., Pinchuk, I. V., Lapa, S. V., & Urdaci, M. C. (2003). Letters in Applied Microbiology, 37, 169–173.

    Article  CAS  Google Scholar 

  52. Katara, J., Deshmukh, R., Nagendra, K., Kaur, S., & Kaur, S. (2013). Journal of Biological Sciences, 13, 514–520.

    Article  CAS  Google Scholar 

  53. Mahaffee, W. F., & Kloepper, J. W. (1997). Microbial Ecology, 34, 210–223.

    Article  Google Scholar 

  54. Trivedi, P., Spann, T., & Wang, N. (2011). Microbiology Ecology, 62, 324–336.

    Article  CAS  Google Scholar 

  55. Dudeja, S. S., Giri, R., Ranjana, S., Pooja, S. M., & Kothe, E. (2012). Journal of Basic Microbiology, 52, 248–260.

    Article  CAS  Google Scholar 

  56. Haefele, D. M., & Lindow, S. E. (1987). Applied and Environmental Microbiology, 53, 2528–2533.

    CAS  Google Scholar 

  57. Mocali, S., Bertelli, E., Di, C. F., & Mengoni, A. (2003). Research in Microbiology, 154, 105–114.

    Article  Google Scholar 

  58. Verma, S. C., Ladha, I. K., & Tripathi, A. K. (2001). Journal of Biotechnology, 81, 127–141.

    Article  Google Scholar 

  59. van Loon, L. C. (2000). In R. S. S. Fraser, L. C. Van Loon, & A. J. Slusarenko (Eds.), Mechanisms of resistance to plant diseases: systemic acquired resistance (pp. 521–574). Dordrencht: Kluwer.

    Chapter  Google Scholar 

  60. Compant, S., Clement, C., & Sessitsch, A. (2010). Soil Biology & Biochemistry, 42, 669–678.

    Article  CAS  Google Scholar 

  61. Athukorala, S. N. P., Fernando, W. G. D., & Rashid, K. Y. (2009). Canadian Journal of Microbiology, 55, 1021–1032.

    Article  CAS  Google Scholar 

  62. Mora, I., Cabrefiga, J., & Montesinos, E. (2011). International Microbiology, 14, 213–223.

    CAS  Google Scholar 

  63. Tapi, A., Chollet-Imbert, M., Schorens, B., & Jacques, P. (2010). Applied Microbiology and Biotechnology, 85, 1521–1531.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Prof. Ezzedine Aouani for valuable discussion and critical reading of the manuscript. The Tunisian Ministry of Higher Education, Scientific Research is gratefully acknowledged for funding.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ferid Limam.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 85 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kalai-Grami, L., Saidi, S., Bachkouel, S. et al. Isolation and Characterization of Putative Endophytic Bacteria Antagonistic to Phoma tracheiphila and Verticillium albo-atrum . Appl Biochem Biotechnol 174, 365–375 (2014). https://doi.org/10.1007/s12010-014-1062-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-014-1062-4

Keywords

Navigation