Biological control of chickpea Fusarium wilt and root rot caused by Fusarium oxysporum and Fusarium solani with plant probiotic bacteria

پژوهش‌های حبوبات ایران

Article 9, Volume 11, Issue 1 - Serial Number 21, June 2020, Pages 112-123   

Document Type: Original Articles

DOI: 10.22067/ijpr.v11i1.70081

Authors

Masoud Sohrbi¹; Khosro Chehri¹; Rouhallah Sharifi^{* 2}

¹Department of Biology, Razi University, Kermanshah, Iran

²Department of Plant Protection, Razi University, Kermanshah, Iran

Abstract

Introduction
Wilt and root rot diseases caused by Fusarium oxysporum and Fusarium solani are among the most important diseases of chickpea throughout the world and Iran. However, there is not effective chemical fungicide against these soil-borne pathogenic fungi. In recent years, rhizospheric bacteria and fungi developed as promising biofungicides against soil-borne plant pathogens. These microbes exploit several mechanisms such as antibiotics, volatile organic compounds, sidereophore and induced systemic resistance to suppress pathogenic fungi. Recently, the cost of agrochemical innovation and the period of time for their registration have increased rapidly due to stringent legislation, both of these reasons favor investment in the manufacture of biopesticides. The annual progress rate of the biopesticide bazaar is more than 16%, but that of synthetic pesticides has been decreasing by 1.5% annually. Biopesticide companies such as Agroquest, Gustafson, Marrone Bio Innovation, Certis, BioWorks, Becker Underwood, ABiTEP GmbH, and Prophyta have released effective biopesticides to the market. Agrochemical great-companies such as Bayer CropScience have also been engrossed in the bio-pesticide market. Bayer CropScience bought Agroquest in 2012 at a price of 425 million US dollars. Overall, biological control of plant pathogens is promising technology in management of plant disease in sustainable agriculture.
 
Materials & Methods
 In this study, potential of plant growth promoting rhizobacteria (PGPRs) were investigated on biological control of this diseases in laboratory and greenhouse condition. Soil samples were collected from chickpea fields in Kermanshah and Kurdestan provinces. The effect of isolated bacteria were assessed on mycelial growth of F. oxysporum and F. solani in dual culture test. The chickpea seeds were inoculated by 109 CFU/ml of each bacterial isolates and sown in pots. The effect of bacterial isolates have been investigated on plant growth factors in greenhouse situation. The same experiment was conducted to assess the biocontrol ability of selected isolates against Fusarium wilt and root rot disease of chickpea. The greenhouse experiments were conducted based on completely randomized design with four replicates. Data were subjected to analysis of variance procedure in SAS ver. 9.1 software and means compression analysis was done by Fisher protected LSD. Finally, the 16S rDNA of the four selected isolates, B2, B3, B6 and B13 were sequenced and identified based on Genebank data.
 
Results & Discussion
Sixteen out of 100 isolated inhibited the growth of both fungi in vitro. Isolates B13 with 11 mm inhibition zone had the highest growth inhibition activity against F. oxysporum. In absence of pathogens, B2 increased aerial part dry weight from 1.08 to 3.69 g in greenhouse condition. B3 and B4 were the best isolates in improving root growth. They increase root dry weight to 1.42 and 1.36 g, respectively. B2 and B13 isolates had the greatest effect on plant health and reduced disease severity up to 90% in F. oxysporum inoculated plants. The lowest biocontrol activity against F. oxysporum was recorded for isolate B6. B2 increased aerial part fresh weight from 0.56 to 2.49 g, root fresh weight from 0.24 to 1.31 g. B6 was the best isolate for suppression of F. solani and reduced the disease index by 73%. This isolate increased aerial organs fresh weight as up to 3.2 folds and root fresh weight up to 2.9 folds. However, all of bacteria isolates were able to reduce Fusarium root rot disease, significantly. Isolates B2, B3, B6 and B13 were characterized as Bacillus sp., Achromobacter sp., Bacillus pumilus and Burkholderia sp. based on 16S rDNA sequencing, respectively. Bacillus spp. strains exploit several mechanisms such as antibiosis, volatile organic compound production and induced systemic resistance against plant pathogens. These bacteria are good candidate to be formulated in spore suspension form. Here, Achromobacter introduced as good candidate for biological control of Fusarium diseases of chickpea for first time. Overall, plant probiotic bacteria could be consider as promising approach in management of chickpea Fusarium diseases.
 
Conclusion
Bacterial isolates have different ability in plant growth improvement and suppression of plant pathogens. Bacillus sp. was the best isolate for enhancing the shoot dry weight while Achromobacter sp. was the best to improving root dry weight. Indeed, bacteria have several mechanisms for promoting plant growth. Auxin induction by volatiles of Bacillus spp. increase root while decreasing the shoot accumulation of auxin. Overall, consortia of bacteria strains seems to be promising approach to suppression of both diseases in chickpea.

Keywords

Biological Control; Fusarium oxysporum; Fusarium solani; PGPR; Sustainable Agriculture

References

Ahmadzadeh, M., Sharifi Tehrani, A., and Nabizadeh, M. 2009. Biological control of Rhizoctonia Solani Kuhn casual agent of common bean damping-off through Burkholderia cpacia (ex. Burk) Yabucchi. Iranian Journla of Plant Protection Science 39: 81-90.

2. Baby, V., Rajakumar, S., and Ayyasamy, P. 2013. Reduction of ferric iron in synthetic medium amended with acetate as a sole carbon source. International Journl of Current Microbiology 2: 501-513.

3. Bertrand, H., Plassard, C., Pinochet, X., Touraine, B., Normand, P., and Cleyet-Marel, J. 2000. Stimulation of the ionic transport system in Brassica napus by a plant growth-promoting rhizobacterium (Achromobacter sp.). Canadian Journal of Microbology 46: 229-236.

4. Cachinero, J., Hervas, A., Jimenez-Diaz, R., and Tena, M. 2002. Plant defence reactions against fusarium wilt in chickpea induced by incompatible race 0 of Fusarium oxysporum f. sp. ciceris and nonhost isolates of F. oxysporum. Plant Pathology 51: 765-776.

5. Ebrahimi Kazemabad, Z., Rohani, H., Jamali, F., and Mahdikhani Moghadam, E. 2013. Antagonistic effect of Pseudomonas fluorescens isolates against Fusarium oxysporum f. sp. ciceris. Iranian Journal of Pulses Research 3: 1-10.

6. Gerlach, W., and Nirenberg, H. 1982. The Genus Fusarium-A Pictorial Atlas Berlin-Dahlem.

7. Glazebrook, J. 2005. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Reveiw of Phytopathology. 43: 205-227.

8. Golpayegani, S., Zafari, D., and Khodakaramian, G. 2011. The Biological control of important faba bean root rot agents caused by rhizospheric antagonist bacteria. Iranian Journal of Plant Protection Science 41: 283-292.

9. Hagedorn, C., Gould, W., and Bardinelli, T. 1989. Rhizobacteria of cotton and their repression of seedling disease pathogens. Applied and Environmental Microbology 55: 2793-2797.

10. Hartman, G., Huang, Y., Nelson, R., and Noel, G. 1997. Germplasm evaluation of Glycine max for resistance to Fusarium solani, the causal organism of sudden death syndrome. Plant Disease 81: 515-518.

11. Hayat, R., Ali, S., Amara, U., Khalid, R., and Ahmed, I. 2010. Soil beneficial bacteria and their role in plant growth promotion: a review. Annals of Microbiology 60: 579-598.

12. Henis, Y., and Inbar, M. 1968. Effect of Bacillus subtilis on growth and sclerotium formation by Rhizoctonia solani. Phytopathology 58: 933-938.

13. Jamali, F., Sharifi Tehrani, A., Okhovat, M., and Zakeri, Z. 2005. Effect of antagonistic bacteria on the control of Fusarium wilt of chickpea caused by Fusarium oxysporum under greenhouse conditions Iran Journal of Agricultural Sciences 36: 711-717.

14. Jiang, H., Dong, H., Zhang, G., Yu, B., Chapman, L.R., and Fields, M.W. 2006. Microbial diversity in water and sediment of Lake Chaka, an athalassohaline lake in northwestern China. Applied and Environmental Microbiology 72: 3832-3845.

15. Kang, S.M., Khan, A.L., Hamayun, M., Shinwari, Z.K., Kim, Y.H., Joo, G.J., and Lee, I.J. 2012. Acinetobacter calcoaceticus ameliorated plant growth and influenced gibberellins and functional biochemicals. Pakistan Journal of Botany 44: 365-372.

16. Kumar, A., Prakash, A., and Johri, B. 2011. Bacillus as PGPR in crop ecosystem. In: Bacteria in Agrobiology: Crop Ecosystems. Springer. p. 37-59.

17. Leclère, V., Bechet, M., Adam, A., Guez, J.S., Wathelet, B., Ongena, M., Thonart, P., Gancel, F., Chollet-Imbert, M., and Jacques, P. 2005. Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism's antagonistic and biocontrol activities. Applied and Environmental Microbiology 71: 4577-4584.

18. Manafi Dizaji, R., Babay Ahari, A., Arzanlou, M., and Valizadeh, M. 2012. Assessment of resistance in tomato varieties under greenhouse conditions against Fusarium wilt, and biological control of the disease. Journal of Agricultural Science And Sustainable Production 22: 145-158.

19. Mayak, S., Tirosh, T., and Glick, B.R. 2004. Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiology and Biochemistry 42: 565-572.

20. Moretti, M., Gilardi, G., Gullino, M., and Garibaldi, A. 2008. Biological control potential of Achromobacter xylosoxydans for suppressing Fusarium wilt of tomato. International Journal of Botany 4: 369-375.

21. Nakkeeran, S., Kavitha, K., Chandrasekar, G., Renukadevi, P., and Fernando, W. 2006. Induction of plant defence compounds by Pseudomonas chlororaphis PA23 and Bacillus subtilis BSCBE4 in controlling damping-off of hot pepper caused by Pythium aphanidermatum. Biocontrol Science and Technology16: 403-416.

22. Naseby, D., Pascual, J., and Lynch, J. 2000. Effect of biocontrol strains of Trichoderma on plant growth, Pythium ultimum populations, soil microbial communities and soil enzyme activities. Journal of Applied Microbiology 88: 161-169.

23. Pieterse, C.M., Leon-Reyes, A., Van der Ent, S., and Van Wees, S.C. 2009. Networking by small-molecule hormones in plant immunity. Nature Chemical Biology 5: 308-316.

24. Rademaker, J.L., and de Bruijn, F.J. 1997. Characterization and classification of microbes by rep-PCR genomic fingerprinting and computer assisted pattern analysis. DNA Markers: Protocols, Applications and Overviews 1: 151-171.

25. Serajzadeh, N., Khodakaramian, G., and Soleymani Pari, M.J. 2013. Interaction between root nodulating bacteria and Fusarium solani the causal agent of faba-bean root rot. Scientific Journal Management System 2: 1-8.

26. Shanthi, A.T., and Vittal, R.R. 2013. Biocontrol potentials of plant growth promoting rhizobacteria against Fusarium wilt disease of cucurbit. International Journal of Phytopathology 2: 155-161.

27. Sharifi, R., and Ryu, C.M. 2016a. Are bacterial volatile compounds poisonous odors to a fungal pathogen Botrytis cinerea, alarm signals to Arabidopsis seedlings for eliciting induced resistance, or both? Frontiers in Microbiology 7: DOI: 10.3389/fmicb.2016.00196.

28. Sharifi, R., and Ryu, C.M. 2016b. Making healthier or killing enemies? Bacterial volatile-elicited plant immunity plays major role upon protection of Arabidopsis than the direct pathogen inhibition. Communicative & Integrative Biology. DOI: 10.1080/19420889.2016.1197445.

29. Sharifi, R., DOI Ryu, C.M. 2017. Chatting with a tiny belowground member of the holobiome: communication between plants and growth-promoting Rhizobacteria. Advances in Botanical Research 82: 135-160.

30. Singh, P.K., Singh, M., Agnihotri, V., and Vyas, D. 2013. Arbuscular mycorrhizal fungi: biocontrol against Fusarium wilt of chickpea. International Journal of Scientific Research Publication 3: 1-5.

31. Srinivasan, K., Gilardi, G., Garibaldi, A., and Gullino, M. 2009. Bacterial antagonists from used rockwool soilless substrates suppress Fusarium wilt of tomato. Journal of Plant Pathology 147-154.

32. Szczech, M., and Shoda, M. 2006. The Effect of mode of application of Bacillus subtilis RB14‐C on its efficacy as a biocontrol agent against Rhizoctonia solani. Journal of Phytopathology 154: 370-377.

33. Tangerina, M.M., Correa, H., Haltli, B., Vilegas, W., and Kerr, R.G. 2017. Bioprospecting from cultivable bacterial communities of marine sediment and invertebrates from the underexplored Ubatuba region of Brazil. Archive of Microbiology 199: 155-169.

34. Weller, D., and Cook, R. 1983. Suppression of take-all of wheat by seed treatments with fluorescent pseudomonads. Phytopathology 73: 463-469.

35. You, Y.H., Park, J.M., Yi, P.H., Back, C.G., Park, M.J., Han, K.S., Yoon, J.B., Kim, H.H., and Park, J.H. 2017. Microflora of phytopathogen-transferring Bradysia agrestis: a step toward finding ideal candidates for paratransgenesis. Symbiosis 71: 35-46.