Skip to main content

Advertisement

Log in

Suppression of Fusarium wilt of banana by combining acid soil ameliorant with biofertilizer made from Bacillus velezensis H-6

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

Abstract

Fusarium wilt is one of the most serious banana diseases. It is caused by the soil-borne pathogen Fusarium oxysporum f. sp. cubense (Foc). The key accepted reasons for disease break-outs are the increasing number of pathogens in soil and gradual soil acidification according to published reports. Few studies have reported management methods to control these two aspects at the same time. In this study, a novel improved biological control method, combined acid soil ameliorant (ASA) with biofertilizer (BIO), was applied to manage Fusarium wilt under greenhouse conditions. A biocontrol agent, Bacillus velezensis H-6, was isolated and used for producing biofertilizer BIO6 for pot experiments. Combined ASA with BIO6 (treatments OBIO6 and ABIO6) showed greater biocontrol efficacy compared with individual treatments by 63.3% and 66.7%, respectively. They also increased rhizosphere soil pH from 4.50 to 4.89 and 5.52, respectively. Correlation analysis showed that the Foc population and Fusarium wilt disease incidence (DI) were both significantly (P < 0.05) negatively correlated with ∆pH in the rhizosphere, contents of NH4-N and organic matter (OM), and populations of bacteria and actinomycetes. Furthermore, ∆pH was significantly positively correlated with content of OM and populations of bacteria and actinomycetes, while it was negatively correlated with content of NO3-N and population of fungi. In conclusion, our novel improved biological control method revealed a greater potential to control Fusarium wilt of banana, and the effect might be a result of improving soil acid-alkali conditions to decrease the density of pathogen and manipulating the soil microbial community.

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

Similar content being viewed by others

References

  • Abriouel, H., Franz, C. M. A. P., Omar, N. B., & Gálvez, A. (2011). Diversity and applications of Bacillus bacteriocins. FEMS Microbiology Reviews, 35, 201–232.

    Article  CAS  PubMed  Google Scholar 

  • Alabouvette, C. (1999). Fusarium wilt suppressive soils: An example of disease-suppressive soils. Australasian Plant Pathology, 28, 57–64.

    Article  Google Scholar 

  • Badri, D. V., & Vivanco, J. M. (2009). Regulation and function of root exudates. Plant, Cell & Environment, 32, 666–681.

    Article  CAS  Google Scholar 

  • Bever, J. D., Platt, T. G., & Morton, E. R. (2012). Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annual Review of Microbiology, 66, 265–283.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blaya, J., Lloret, E., Ros, M., & Pascual, J. A. (2015). Identification of predictor parameters to determine agro-industrial compost suppressiveness against Fusarium oxysporum and Phytophthora capsici diseases in muskmelon and pepper seedlings. Journal of the Science of Food and Agriculture, 95, 1482–1490.

    Article  CAS  PubMed  Google Scholar 

  • Butler, D. (2013). Fungus threatens top banana. Nature, 504, 195–196.

    Article  CAS  PubMed  Google Scholar 

  • Cao, Y., Wang, J. D., Wu, H. S., Yan, S. H., Guo, D. J., Wang, G. F., & Ma, Y. (2016). Soil chemical and microbial responses to biogas slurry amendment and its effect on Fusarium wilt suppression. Applied Soil Ecology, 107, 116–123.

    Article  Google Scholar 

  • Caracuel, Z., Roncero, M. I. G., Espeso, E. A., González-Verdejo, C. I., García-Maceira, F. I., & Pietro, A. D. (2003). The pH signalling transcription factor PacC controls virulence in the plant pathogen Fusarium oxysporum. Molecular Microbiology, 48, 765–779.

    Article  CAS  PubMed  Google Scholar 

  • Cavaglieri, L., Orlando, J., Rodriguez, M. I., Chulze, S., & Etcheverry, M. (2005). Biocontrol of Bacillus subtilis against Fusarium verticillioides in vitro and at the maize root level. Research in Microbiology, 156, 748–754.

    Article  CAS  PubMed  Google Scholar 

  • Chen, Y. F., Chen, W., Huang, X., Hu, X., Zhao, J. T., Gong, Q., Li, X. J., & Huang, X. L. (2013). Fusarium wilt-resistant lines of Brazil banana (Musa spp., AAA) obtained by EMS-induced mutation in a micro-cross-section cultural system. Plant Pathology, 62, 112–119.

    Article  CAS  Google Scholar 

  • Deltour, P., França, S. C., Pereira, O. L., Cardoso, I., Neve, S. D., Debode, J., & Höfte, M. (2017). Disease suppressiveness to Fusarium wilt of banana in an agroforestry system: Influence of soil characteristics and plant community. Agriculture, Ecosystems & Environment, 239, 173–181.

    Article  Google Scholar 

  • Domínguez, J., Negrín, M. A., & Rodríguez, C. M. (1996). Soil chemical characteristics in relation to Fusarium wilts in banana crops of Gran Canaria Island (Spain). Communications in Soil Science and Plant Analysis, 27, 2649–2662.

    Article  Google Scholar 

  • El-Hassan, S. A., & Gowen, S. R. (2006). Formulation and delivery of the bacterial antagonist Bacillus subtilis for management of lentil vascular wilt caused by Fusarium oxysporum f. Sp. lentis. Journal of Phytopathology, 154, 148–155.

    Article  Google Scholar 

  • Fan, X. L., & Li, J. (2014). Effectiveness of alkaline fertilizer on the control of banana Fusarium wilt and regulation of soil acidity in banana orchard. Journal of Plant Nutrition and Fertilization, 20, 938–946.

    Google Scholar 

  • Fang, X. L., You, M. P., & Barbetti, M. J. (2012). Reduced severity and impact of Fusarium wilt on strawberry by manipulation of soil pH, soil organic amendments and crop rotation. European Journal of Plant Pathology, 134, 619–629.

    Article  Google Scholar 

  • Fu, L., Penton, C. R., Ruan, Y. Z., Shen, Z. Z., Xue, C., Li, R., & Shen, Q. R. (2017). Inducing the rhizosphere microbiome by biofertilizer application to suppress banana Fusarium wilt disease. Soil Biology and Biochemistry, 104, 39–48.

    Article  CAS  Google Scholar 

  • Gao, Z. F., Zhang, B. J., Liu, H. P., Han, J. C., & Zhang, Y. J. (2017). Identification of endophytic Bacillus velezensis ZSY-1 strain and antifungal activity of its volatile compounds against Alternaria solani and Botrytis cinerea. Biological Control, 105, 27–39.

    Article  Google Scholar 

  • Garbeva, P., Postma, J., van Veen, J. A., & van Elsas, J. D. (2006). Effect of above-ground plant species on soil microbial community structure and its impact on suppression of Rhizoctonia solani AG3. Environmental Microbiology, 8, 233–246.

    Article  CAS  PubMed  Google Scholar 

  • Ghorbani, R., Wilcockson, S., Koocheki, A., & Leifert, C. (2008). Soil management for sustainable crop disease control: A review. Environmental Chemistry Letters, 6, 149–162.

    Article  CAS  Google Scholar 

  • Huang, J. L., Li, H. L., & Yuan, H. X. (2006). Effect of organic amendments on Verticillium wilt of cotton. Crop Protection, 25, 1167–1173.

    Article  Google Scholar 

  • Huang, J. F., Wei, Z., Hu, J., Yang, C. L., Gu, Y., Mei, X. L., Shen, Q. R., Xu, Y. C., & Riaz, K. (2017a). Chryseobacterium nankingense sp. nov. WR21 effectively suppresses Ralstonia solanacearum growth via intensive root exudates competition. BioControl, 62, 567–577.

    Article  Google Scholar 

  • Huang, Q. Y., Tang, S. H., Huang, X., Zhang, F. B., Yi, Q., Li, P., & Fu, H. T. (2017b). Influence of rice cultivation on the abundance and fractionation of Fe, Mn, Zn, Cu, and Al in acid sulfate paddy soils in the Pearl River Delta. Chemical Geology, 448, 93–99.

    Article  CAS  Google Scholar 

  • Jetiyanon, K., & Kloepper, J. W. (2002). Mixtures of plant growth-promoting rhizobacteria for induction of systemic resistance against multiple plant diseases. Biological Control, 24, 285–291.

    Article  Google Scholar 

  • Komada, H. (1975). Development of a selective medium for quantitative isolation of Fusarium oxysporum from natural soil. Review of Plant Protection Research, 8, 114–125.

    Google Scholar 

  • Lang, J. J., Hu, J., Ran, W., Xu, Y. C., & Shen, Q. R. (2011). Control of cotton Verticillium wilt and fungal diversity of rhizosphere soils by bio-organic fertilizer. Biology and Fertility of Soils, 48, 191–203.

    Article  Google Scholar 

  • Lee, H.-H., Park, J., Lim, J. Y., Kim, H., Choi, G. J., Kim, J. C., & Seo, Y. S. (2015). Complete genome sequence of Bacillus velezensis G341, a strain with a broad inhibitory spectrum against plant pathogens. Journal of Biotechnology, 211, 97–98.

    Article  CAS  PubMed  Google Scholar 

  • Lievens, B., Brouwer, M., Vanachter, A. C. R. C., Lévesque, C. A., Cammue, B., & Thomma, B. (2005). Quantitative assessment of phytopathogenic fungi in various substrates using a DNA macroarray. Environmental Microbiology, 7, 1698–1710.

    Article  CAS  PubMed  Google Scholar 

  • Ling, N., Xue, C., Huang, Q. W., Yang, X. M., Xu, Y. C., & Shen, Q. R. (2010). Development of a mode of application of bioorganic fertilizer for improving the biocontrol efficacy to Fusarium wilt. BioControl, 55, 673–683.

    Article  Google Scholar 

  • Liu, Y. X., Shi, J. X., Feng, Y. G., Yang, X. M., Li, X., & Shen, Q. R. (2013). Tobacco bacterial wilt can be biologically controlled by the application of antagonistic strains in combination with organic fertilizer. Biology and Fertility of Soils, 49, 447–464.

    Article  Google Scholar 

  • Mak, C., Mohamed, A. A., Liew, K. W., & Ho, Y. W. (2004). Early screening technique for fusarium wilt resistance in banana micropropagated plants. Banana Improvement, 18, 219–227.

    Google Scholar 

  • Manikandan, R., Karthikeyan, G., & Raguchander, T. (2017). Soil proteomics for exploitation of microbial diversity in Fusarium wilt infected and healthy rhizosphere soils of tomato. Physiological and Molecular Plant Pathology, 100, 185–193.

    Article  CAS  Google Scholar 

  • Meng, Q. X., & Hao, J. J. J. (2017). Optimizing the application of Bacillus velezensis BAC03 in controlling the disease caused by Streptomyces scabies. BioControl, 62, 535–544.

    Article  CAS  Google Scholar 

  • Muyzer, G., Waal, E. C. D., & Uitierlinden, A. G. (1993). Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology, 59, 695–700.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nel, B., Steinberg, C., Labuschagne, N., & Viljoen, A. (2007). Evaluation of fungicides and sterilants for potential application in the management of Fusarium wilt of banana. Crop Protection, 26, 697–705.

    Article  CAS  Google Scholar 

  • Ploetz, R. C. (2006). Fusarium-induced diseases of tropical, perennial crops. Phytopathology, 96, 648–652.

    Article  Google Scholar 

  • Qiu, M. H., Zhang, R. F., Xue, C., Zhang, S. S., Li, S. Q., Zhang, N., & Shen, Q. R. (2012). Application of bio-organic fertilizer can control Fusarium wilt of cucumber plants by regulating microbial community of rhizosphere soil. Biology and Fertility of Soils, 48, 807–816.

    Article  CAS  Google Scholar 

  • Roh, J. Y., Liu, Q., Choi, J. Y., Wang, Y., Shim, H. J., Xu, H. G., Choi, G. J., Kim, J.-C., & Je, Y. H. (2009). Construction of a recombinant Bacillus velezensis strain as an integrated control agent against plant diseases and insect pests. Journal of Microbiology and Biotechnology, 19, 1223–1229.

    Article  CAS  PubMed  Google Scholar 

  • Rotenberg, D., Wells, A. J., Chapman, E. J., Whitfield, A. E., Goodman, R. M., & Cooperband, L. R. (2007). Soil properties associated with organic matter-mediated suppression of bean root rot in field soil amended with fresh and composted paper mill residuals. Soil Biology and Biochemistry, 39, 2936–2948.

    Article  CAS  Google Scholar 

  • Saravanan, T., Muthusamy, M., & Marimuthu, T. (2003). Development of integrated approach to manage the fusarial wilt of banana. Crop Protection, 22, 1117–1123.

    Article  Google Scholar 

  • Shen, Z. Z., Wang, D. S., Ruan, Y. Z., Xue, C., Zhang, J., Li, R., & Shen, Q. R. (2014). Deep 16S rRNA pyrosequencing reveals a bacterial community associated with Banana Fusarium Wilt disease suppression induced by bio-organic fertilizer application. PLoS One, 9, e98420.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen, Z. Z., Ruan, Y. Z., Wang, B. B., Zhong, S. T., Su, L. X., Li, R., & Shen, Q. R. (2015). Effect of biofertilizer for suppressing Fusarium wilt disease of banana as well as enhancing microbial and chemical properties of soil under greenhouse trial. Applied Soil Ecology, 93, 111–119.

    Article  Google Scholar 

  • Song, S., Chen, X., Huang, D. M., Xu, Y., Zeng, H. C., Hu, X. W., Xu, B. Y., Jin, Z. Q., & Wang, W. Q. (2016). Identification of miRNAs differentially expressed in Fusarium wilt-resistant and susceptible banana varieties. South African Journal of Botany, 106, 244–249.

    Article  CAS  Google Scholar 

  • Sun, J. B., Zou, L. P., Li, W. B., Yang, J. H., Wang, Y. G., Xia, Q. Y., & Peng, M. (2018). Rhizosphere soil properties and banana Fusarium wilt suppression influenced by combined chemical and organic fertilizations. Agriculture, Ecosystems & Environment, 254, 60–68.

    Article  CAS  Google Scholar 

  • Taubenhaus, J. J., Ezekiel, W. N., & Killough, D. T. (1928). Relation of cotton root rot and fusarium wilt to the acidity and alkalinity of the soil. Bulletin, 389, 1–19.

    Google Scholar 

  • Wang, B. B., Li, R., Ruan, Y. Z., Ou, Y. N., Zhao, Y., & Shen, Q. R. (2015). Pineapple-banana rotation reduced the amount of Fusarium oxysporum more than maize-banana rotation mainly through modulating fungal communities. Soil Biology and Biochemistry, 86, 77–86.

    Article  CAS  Google Scholar 

  • Xiong, W., Li, R., Ren, Y., Liu, C., Zhao, Q. Y., Wu, H. S., Jousset, A., & Shen, Q. R. (2017). Distinct roles for soil fungal and bacterial communities associated with the suppression of vanilla Fusarium wilt disease. Soil Biology and Biochemistry, 107, 198–207.

    Article  CAS  Google Scholar 

  • Xu, L. B., Huang, B. Z., Wu, Y. L., Huang, Y. H., & Dong, T. (2011). The cost-benefit analysis for bananas diversity production in China Foc. Zones. American Journal of Plant Science, 2, 561–568.

    Article  Google Scholar 

  • Zelenev, V. V., van Bruggen, A. H., & Semenov, A. M. (2005). Short-term wavelike dynamics of bacterial populations in response to nutrient input from fresh plant residues. Microbial Ecology, 49, 83–93.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, N., He, X., Zhang, J., Raza, W., Yang, X. M., Ruan, Y. Z., Shen, Q. R., & Huang, Q. W. (2014). Suppression of Fusarium wilt of banana with application of bio-organic fertilizers. Pedosphere, 24, 613–624.

    Article  CAS  Google Scholar 

  • Zhao, J., Dong, Y., Xie, X. B., Li, X., Zhang, X. X., & Shen, X. (2011). Effect of annual variation in soil pH on available soil nutrients in pear orchards. Acta Ecologica Sinica, 31, 212–216.

    Article  Google Scholar 

  • Zhu, Q. C., de Vries, W., Liu, X. J., Hao, T. X., Zeng, M. F., Shen, J. B., & Zhang, F. S. (2018). Enhanced acidification in Chinese croplands as derived from element budgets in the period 1980-2010. Science of the Total Environment, 618, 1497–1505.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The study was financially supported by Science and Technology Planning Project of Guangdong Province (2015A020209053 and 2015B020237007), National Key Research and Development Plan (2016YFD0800600), and Special Fund for Agro-scientific Research in the Public Interest of China (201003016).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yuwan Pang.

Ethics declarations

The authors declare that the research complies with ethical standards.

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

ESM 1

(DOC 12 kb)

Figure S1

(DOC 876 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, J., Pang, Y., Zhang, F. et al. Suppression of Fusarium wilt of banana by combining acid soil ameliorant with biofertilizer made from Bacillus velezensis H-6. Eur J Plant Pathol 154, 585–596 (2019). https://doi.org/10.1007/s10658-019-01683-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-019-01683-5

Keywords

Navigation