Skip to main content
Log in

Bacillus species as the most promising bacterial biocontrol agents in rhizosphere and endorhiza of plants grown in rotation with each other

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

In this study, a total of 550 cultivable bacterial isolates were isolated from rhizosphere and endorhiza of rice, Berseem clover, and oilseed rape grown in rotation with each other. The potential of antifungal activity of all isolates against five rice pathogenic fungi was investigated under in vitro conditions. Of 550 isolates, 139 inhibited the mycelial growth of at least one fungal rice pathogen. The results also showed that rhizosphere and endorhiza of every third plant (three studied plants) harbored the bacteria (139 isolates) with good potential for inhibiting fungal rice pathogens in vitro. Based on biochemical tests and by comparison of 16S rDNA sequences, of the superiors six endophytic and rhizosphere isolates, which showed strong inhibitory effects against the mycelial growth of all the five fungal rice pathogens (Magnaporthe oryzae, M. salvinii, Fusarium verticillioides, F. fujikuroi, and F. proliferum), were identified. Two isolates REN4 and CEN2, isolate CEN6, isolate CEN3, and two isolates REN3 and CEN5 were closely related to Bacillus mojavensis, B. amyloliquefaciens, B. subtilis, and B. cereus respectively. Strains REN4 and REN3 were obtained from rhizosphere and endorhiza of rice, while strains CEN6 and CEN2, and strains CEN5 and CEN3 were isolated from rhizosphere and endorhiza of clover and oilseed rape respectively. Therefore, it can be concluded that plants cultivated in rotation with rice and grown on the same soil harbor protective bacteria such as genus Bacillus and that may be potential reservoirs of bio-control agents for control of the rice pathogenic fungi tested in this study.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Adhikari, T. B., Joseph, C. M., Yang, G., Phillips, D. A., & Nelson, L. M. (2001). Evaluation of bacteria isolated from rice for plant growth promotion and biological control of seedling disease of rice. Canadian Journal of Microbiology, 47, 916–924.

    Article  CAS  PubMed  Google Scholar 

  • Arguelles-Arias, A., Ongena, M., Halimi, B., Lara, Y., Brans, A., Joris, B., & Fickers, P. (2009). Bacillus amyloliquefaciens GA1 as a source of potent antibiotics and other secondary metabolites for biocontrol of plant pathogens. Microbial Cell Factories, 8, 1.

    Article  Google Scholar 

  • Azevedo, J. L., Maccheroni Jr., W., Pereira, J. O., & de Araújo, W. L. (2000). Endophytic microorganisms: a review on insect control and recent advances on tropical plants. Electronic Journal of Biotechnology, 3, 15–16.

    Article  Google Scholar 

  • Bacon, C. W., & Hinton, D. M. (2002). Endophytic and biological control potential of Bacillus Mojavensis and related species. Biological Control, 23, 274–284.

    Article  CAS  Google Scholar 

  • Badri, D. V., Chaparro, J. M., Zhang, R., Shen, Q., & Vivanco, J. M. (2013). Application of natural blends of phytochemicals derived from the root exudates of Arabidopsis to the soil reveal that phenolic-related compounds predominantly modulate the soil microbiome. Journal of Biological Chemistry, 288, 4502–4512.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bais, H. P., Walker, T. S., Schweizer, H. P., & Vivanco, J. M. (2002). Root specific elicitation and antimicrobial activity of rosmarinic acid in hairy root cultures of Ocimum basilicum. Plant Physiology and Biochemistry, 40, 983–995.

    Article  CAS  Google Scholar 

  • Card, S. D., Hume, D. E., Roodi, D., McGill, C. R., Millner, J. P., & Johnson, R. D. (2015). Beneficial endophytic microorganisms of Brassica – A review. Biological Control, 90, 102–112. doi:10.1016/j.biocontrol.2015.06.001.

    Article  Google Scholar 

  • Chaiharn, M., Chunhaleuchanon, S., & Lumyong, S. (2009). Screening siderophore producing bacteria as potential biological control agent for fungal rice pathogens in Thailand. World Journal of Microbiology and Biotechnology, 25, 1919–1928.

    Article  Google Scholar 

  • Chaparro, J. M., Badri, D. V., Bakker, M. G., Sugiyama, A., Manter, D. K., & Vivanco, J. M. (2013). Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PloS One, 8, e55731.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaparro, J. M., Badri, D. V., & Vivanco, J. M. (2014). Rhizosphere microbiome assemblage is affected by plant development. The ISME Journal, 8, 790–803.

    Article  CAS  PubMed  Google Scholar 

  • Chen, F., Wang, M., Zheng, Y., Luo, J., Yang, X., & Wang, X. (2010). Quantitative changes of plant defense enzymes and phytohormone in biocontrol of cucumber fusarium wilt by Bacillus Subtilis B579. World Journal of Microbiology and Biotechnology, 26, 675–684.

    Article  CAS  Google Scholar 

  • Chowdhury, S. P., Hartmann, A., Gao, X., & Borriss, R. (2015). Biocontrol mechanism by root-associated Bacillus amyloliquefaciens FZB42–a review. Frontiers in Microbiology, 6, 780.

    Article  PubMed  PubMed Central  Google Scholar 

  • Compant, S., Clément, C., & Sessitsch, A. (2010). Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biology and Biochemistry, 42, 669–678. doi:10.1016/j.soilbio.2009.11.024.

    Article  CAS  Google Scholar 

  • Correa, O. S., Montecchia, M. S., Berti, M. F., Ferrari, M. C. F., Pucheu, N. L., Kerber, N. L., & García, A. F. (2009). Bacillus amyloliquefaciens BNM122, a potential microbial biocontrol agent applied on soybean seeds, causes a minor impact on rhizosphere and soil microbial communities. Applied Soil Ecology, 41, 185–194.

    Article  Google Scholar 

  • Danielsson, J. (2008). Bacillus based biocontrol on Brassica. Diss (sammanfattning/summary) Uppsala: Sveriges lantbruksuniv. Acta Universitatis Agriculturae Sueciae, 2008:40, 1652-6880.

  • De Boer, W., Wagenaar, A.-M., Gunnewiek, P. J. A. K., & Van Veen, J. A. (2007). In vitro suppression of fungi caused by combinations of apparently non-antagonistic soil bacteria. FEMS Microbiology Ecology, 59, 177–185.

    Article  PubMed  Google Scholar 

  • Eljounaidi, K., Lee, S. K., & Bae, H. (2016). Bacterial endophytes as potential biocontrol agents of vascular wilt diseases – Review and future prospects. Biological Control, 103, 62–68. doi:10.1016/j.biocontrol.2016.07.013.

    Article  Google Scholar 

  • Etesami, H., Alikhani, H. A. (2016a). ​Co-inoculation with endophytic and rhizosphere bacteria allows reduced application rates of N-fertilizer for rice plant. Rhizosphere, 2, 5-12.

  • Etesami, H., & Alikhani, H. A. (2016b). Rhizosphere and endorhiza of oilseed rape (Brassica napus L.) plant harbor bacteria with multifaceted beneficial effects. Biological Control, 94, 11–24.

    Article  Google Scholar 

  • Etesami, H., Alikhani, H. A. (2017). Evaluation of Gram-positive rhizosphere and endophytic bacteria for biological control of fungal rice (Oryzia sativa L.) pathogens. European Journal of Plant Pathology, 147, 7-14.

  • Etesami, H., Mirsyedhosseini, H., Alikhani, H. A. (2013). Rapid screening of berseem clover (Trifolium alexandrinum) endophytic bacteria for rice plant seedlings growth-promoting agents. ISRN Soil Science. 2013.

  • Etesami, H., Hosseini, H. M., Alikhani, H. A., & Mohammadi, L. (2014). Bacterial biosynthesis of 1-aminocyclopropane-1-carboxylate (ACC) deaminase and indole-3-acetic acid (IAA) as endophytic preferential selection traits by rice plant seedlings. Journal of Plant Growth Regulation, 33, 654–670.

    Article  CAS  Google Scholar 

  • Garbeva, P., Van Elsas, J. D., & Van Veen, J. A. (2008). Rhizosphere microbial community and its response to plant species and soil history. Plant and Soil, 302, 19–32.

    Article  CAS  Google Scholar 

  • Garcia, T. V., Knaak, N., & Fiuza, L. M. (2015). Endophytic bacteria as biological control agents in rice fields. Arquivos do Instituto Biológico, 82, 1–9.

    Article  Google Scholar 

  • Holt, J. G., Krieg, N. R., Sneath, P. H. A., & Staley, J. T. (2010). Bergey’s manual of determinative bacteriology (ninth ed.). Baltimore: Williams and Wilkins Baltimore Md.

    Google Scholar 

  • Hossain, M. T., Chung, E. J., & Chung, Y. R. (2016). Biological control of Rice Bakanae by an endophytic Bacillus Oryzicola YC7007. The Plant Pathology Journal, 32, 228–242.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kim, W.-G., Weon, H.-Y., & Lee, S.-Y. (2008). In vitro antagonistic effects of bacilli isolates against four soilborne plant pathogenic fungi. The Plant Pathology Journal, 24, 52–57.

    Article  Google Scholar 

  • Kumar, P., Dubey, R. C., & Maheshwari, D. K. (2012). Bacillus strains isolated from rhizosphere showed plant growth promoting and antagonistic activity against phytopathogens. Microbiological Research, 167, 493–499.

    Article  CAS  PubMed  Google Scholar 

  • Li, L., Ma, J., Li, Y., Wang, Z., Gao, T., & Wang, Q. (2012). Screening and partial characterization of Bacillus with potential applications in biocontrol of cucumber fusarium wilt. Crop Protection, 35, 29–35.

    Article  CAS  Google Scholar 

  • Pérez-García, A., Romero, D., & De Vicente, A. (2011). Plant protection and growth stimulation by microorganisms: biotechnological applications of bacilli in agriculture. Current Opinion in Biotechnology, 22, 187–193.

    Article  PubMed  Google Scholar 

  • Petrini, L. E., Petrini, O., & Laflamme, G. (1989). Recovery of endophytes of Abies balsamea from needles and galls of Paradiplosis tumifex. Phytoprotection, 70, 97–103.

    Google Scholar 

  • Pieterse, C. M. J., Zamioudis, C., Berendsen, R. L., Weller, D. M., Van Wees, S. C. M., & Bakker, P. A. H. M. (2014). Induced systemic resistance by beneficial microbes. Annual Review of Phytopathology, 52, 347–375.

    Article  CAS  PubMed  Google Scholar 

  • Raaijmakers, J. M., Leeman, M., Van Oorschot, M. M. P., Van der Sluis, I., Schippers, B., & Bakker, P. (1995). Dose-response relationships in biological control of fusarium wilt of radish by pseudomonas spp. Phytopathology, 85, 1075–1080.

    Article  Google Scholar 

  • Shrestha, B. K., Karki, H. S., Groth, D. E., Jungkhun, N., & Ham, J. H. (2016). Biological control activities of rice-associated Bacillus sp. strains against sheath blight and bacterial panicle blight of rice. PloS one, 11, e0146764.

    Article  PubMed  PubMed Central  Google Scholar 

  • Song, F., & Goodman, R. M. (2001). Molecular biology of disease resistance in rice. Physiological and Molecular Plant Pathology, 59, 1–11.

    Article  CAS  Google Scholar 

  • Stang, H., Tkachuk, O. (2013). The benefits of microbial communities on the fitness of Lathyrus odoratus. Letters in General Microbiology, 2, 10-12.

  • Sturz, A. V., Christie, B. R., Matheson, B. G., & Nowak, J. (1997). Biodiversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biology and Fertility of Soils, 25, 13–19.

    Article  Google Scholar 

  • Sturz, A. V., Christie, B. R., & Nowak, J. (2000). Bacterial endophytes: potential role in developing sustainable systems of crop production. Critical Reviews in Plant Sciences, 19, 1–30.

    Article  Google Scholar 

  • Tindall, B. J., Sikorski, J., Smibert, R. A., & Krieg, N. R. (2007). Phenotypic characterization and the principles of comparative systematics. In Methods for General and Molecular Microbiology (pp. 330–393). American Society of Microbiology (3rd ed.). Washington, DC: ASM Press. doi:10.1128/9781555817497.ch15.

  • Vasudevan, P., Kavitha, S., Priyadarisini, V. B., Babujee, L., & Gnanamanickam, S. S. (2002). In Gnanamanickam (Ed.), Biological control of rice diseases Biological control of crop diseases (pp. 11–32). New York: Marcel Dekker Inc.

    Google Scholar 

  • Viebahn, M., Veenman, C., Wernars, K., van Loon, L. C., Smit, E., & Bakker, P. A. H. M. (2005). Assessment of differences in ascomycete communities in the rhizosphere of field-grown wheat and potato. FEMS Microbiology Ecology, 53, 245–253.

    Article  CAS  PubMed  Google Scholar 

  • Whipps, J. M. (1987). Effect of media on growth and interactions between a range of soil-borne glasshouse pathogens and antagonistic fungi. New Phytologist, 107, 127–142.

    Article  Google Scholar 

  • Whipps, J. M. (2001). Microbial interactions and biocontrol in the rhizosphere. Journal of Experimental Botany, 52, 487–511.

    Article  CAS  PubMed  Google Scholar 

  • Yanni, Y. G., et al. (1997). Natural endophytic association between rhizobium leguminosarum bv. Trifolii and rice roots and assessment of its potential to promote rice growth. Plant and Soil, 194, 99–114.

    Article  CAS  Google Scholar 

  • Zhang, S., Zhu, W., Wang, B., Tang, J., & Chen, X. (2011). Secondary metabolites from the invasive Solidago canadensis L. accumulation in soil and contribution to inhibition of soil pathogen Pythium ultimum. Applied Soil Ecology, 48, 280–286.

    Article  Google Scholar 

  • Zhang, Q., Zhang, J., Yang, L., Zhang, L., Jiang, D., Chen, W., & Li, G. (2014). Diversity and biocontrol potential of endophytic fungi in Brassica napus. Biological Control, 72, 98–108.

    Article  Google Scholar 

Download references

Acknowledgements

We wish to thank University of Tehran for providing the necessary facilities and funding for this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hassan Etesami.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Etesami, H., Alikhani, H.A. Bacillus species as the most promising bacterial biocontrol agents in rhizosphere and endorhiza of plants grown in rotation with each other. Eur J Plant Pathol 150, 497–506 (2018). https://doi.org/10.1007/s10658-017-1276-8

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-017-1276-8

Keywords

Navigation