Biocontrol of Grey Mold on Strawberry Fruit by Bacillus spp. and Study of the Mechanisms Involved

Ilham Barakat, Noureddine Chtaina, Kaoutar Caidi, Fatiha Bentata

Abstract

Grey mold, caused by the fungus Botrytis cinerea, is one of the most prevalent diseases affecting strawberry plants (Fragaria ananassa). The objective of this study was to assess the antagonistic effect of 5 bacterial strains belonging to the genus Bacillus spp. (BA1, BF2, BB3, BI3, and BO4) against B. cinerea, tested both in vitro and in vivo on strawberry fruits. The strains exhibited antifungal activity against B. cinerea under in vitro conditions, both through direct confrontations and antibiosis tests, as well as through the effect of organic compounds. Strain BO4 could inhibit mycelial growth by 62.92% through direct confrontation and 64.58% through the secretion of volatile organic compounds. Additionally, the strain BF2 demonstrated a high antibiosis effect (74.64%) compared to the control at a concentration of 25%. Treating fruits with the bacterial suspension and culture filtrate of the 5 studied strains controlled grey mold growth in vivo, as indicated by low severity indices in strawberries treated with strains BI3, BF2, and BA1, marked by percentages of 24.44%, 24.44%, and 37.78%, respectively, for preventive treatment. The difference in the effectiveness of various strains depended on the treatment mode; preventive treatment proved to be more effective compared to curative treatment.

Keywords

antagonism; Bacillus spp.; biological control; Botrytis cinerea; postharvest diseases

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References

Abbey, J. A., Percival, D., Abbey, L., Asiedu, S. K., Prithiviraj, B., & Schilder, A. (2019). Biofungicides as alternative to synthetic fungicide control of grey mould (Botrytis cinerea)–prospects and challenges. Biocontrol Science and Technology, 29(3), 207–228. https://doi.org/10.1080/09583157.2018.1548574

Arrebola, E., Sivakumar, D., Bacigalupo, R., & Korsten, L. (2010). Combined application of antagonist Bacillus amyloliquefaciens and essential oils for the control of peach postharvest diseases. Crop Protection, 29(4), 369–377. https://doi.org/10.1016/j.cropro.2009.08.001

Calvo, H., Marco, P., Blanco, D., Oria, R., & Venturini, M. E. (2017). Potential of a new strain of Bacillus amyloliquefaciens BUZ-14 as a biocontrol agent of postharvest fruit diseases. Food Microbiology, 63, 101–110. https://doi.org/10.1016/j.fm.2016.11.004

Chiang, K. S., Liu, H. I., & Bock, C. (2017). A discussion on disease severity index values. Part I: Warning on inherent errors and suggestions to maximise accuracy. Annals of Applied Biology, 171(2), 139–154. https://doi.org/10.1111/aab.12362

De Moura, G. G. D., de Barros, A. V., Machado, F., Martins, A. D., da Silva, C. M., Durango, L. G. C., ... & Doria, J. (2021). Endophytic bacteria from strawberry plants control gray mold in fruits via production of antifungal compounds against Botrytis cinerea L. Microbiological Research, 251, 126793. https://doi.org/10.1016/j.micres.2021.126793

Dennis, C., & J. Webster. (1971). Antagonistic properties of species-groups of Trichoderma: II. Production of volatile antibiotics. Transactions of the British Mycological Society, 57(1), 41–48. https://doi.org/10.1016/S0007-1536(71)80078-5

Fira, D., Dimkić, I., Berić, T., Lozo, J., & Stanković, S. (2018). Biological control of plant pathogens by Bacillus species. Journal of Biotechnology, 285, 44–55. https://doi.org/10.1016/j.jbiotec.2018.07.044

Gao, H., Li, P., Xu, X., Zeng, Q., & Guan, W. (2018). Research on volatile organic compounds from Bacillus subtilis CF-3: Biocontrol effects on fruit fungal pathogens and dynamic changes during fermentation. Frontiers in Microbiology, 9, 456. https://doi.org/10.3389/fmicb.2018.00456

Gao, P., Qin, J., Li, D., & Zhou, S. (2018). Inhibitory effect and possible mechanism of a Pseudomonas strain QBA5 against gray mold on tomato leaves and fruits caused by Botrytis cinerea. PLoS ONE, 13(1), e0190932. https://doi.org/10.1371/journal.pone.0190932

Gao, Z., Zhang, B., Liu, H., Han, J., & Zhang, Y. (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. https://doi.org/10.1016/j.biocontrol.2016.11.007

Hang, N. T. T., Oh, S. O., Kim, G. H., Hur, J. S., & Koh, Y. J. (2005). Bacillus subtilis S1-0210 as a biocontrol agent against Botrytis cinerea in strawberries. The Plant Pathology Journal, 21(1), 59–63. https://doi.org/10.5423/PPJ.2005.21.1.059

Ilham, B., Chtaina, N., Grappin, P., Abdenbi, E., & Brahim, E. (2020). Efficacy of secondary metabolites produced by Bacillus amyloliquefaciens on the inhibition of Zymoseptoria tritici. Global Journal of Science Frontier Research, 20(D1), 9–16. Retrieved from https://journalofscience.org/index.php/GJSFR/article/view/2580

Ji, S. H., Paul, N. C., Deng, J. X., Kim, Y. S., Yun, B. S., & Yu, S. H. (2013). Biocontrol activity of Bacillus amyloliquefaciens CNU114001 against fungal plant diseases. Mycobiology, 41(4), 234–42. https://doi.org/10.5941/myco.2013.41.4.234

Jiang, C. H., Liao, M. J., Wang, H. K., Zheng, M. Z., Xu, J. J., & Guo, J. H. (2018). Bacillus velezensis, a potential and efficient biocontrol agent in control of pepper gray mold caused by Botrytis cinerea. Biological Control, 126, 147–57. https://doi.org/10.1016/j.biocontrol.2018.07.017

Kahramanoğlu, İ., Panfilova, O., Kesimci, T. G., Bozhüyük, A. U., Gürbüz, R., & Alptekin, H. (2022). Control of postharvest gray mold at strawberry fruits caused by Botrytis cinerea and improving fruit storability through Origanum onites L. and Ziziphora clinopodioides L. volatile essential oils. Agronomy, 12(2), 389. https://doi.org/10.3390/agronomy12020389

Kefi, A., Slimene, I. B., Karkouch, I., Rihouey, C., Azaeiz, S., Bejaoui, M., ... & Limam, F. (2015). Characterization of endophytic Bacillus strains from tomato plants (Lycopersicon esculentum) displaying antifungal activity against Botrytis cinerea Pers. World Journal of Microbiology and Biotechnology, 31, 1967–1976. https://doi.org/10.1007/s11274-015-1943-x

Kilani-Feki, O., Khedher, S. B., Dammak, M., Kamoun, A., Jabnoun-Khiareddine, H., Daami-Remadi, M., & Tounsi, S. (2016). Improvement of antifungal metabolites production by Bacillus subtilis V26 for biocontrol of tomato postharvest disease. Biological Control, 95, 73–82. https://doi.org/10.1016/j.biocontrol.2016.01.005

Luo, L., Zhao, C., Wang, E., Raza, A., & Yin, C. (2022). Bacillus amyloliquefaciens as an excellent agent for biofertilizer and biocontrol in agriculture: An overview for its mechanisms. Microbiological Research, 259, 127016. https://doi.org/10.1016/j.micres.2022.127016

Maung, C. E. H., Baek, W. S., Choi, T. G., & Kim, K. Y. (2021). Control of grey mould disease on strawberry using the effective agent, Bacillus amyloliquefaciens Y1. Biocontrol Science and Technology, 31(5), 468–82. https://doi.org/10.1080/09583157.2020.1867707

Nicot, P. C., Bardin, M., Alabouvette, C., & Köhl, J. (2011). Potential of biological control based on published research. 1. Protection against plant pathogens of selected crops. Classical and augmentative biological control against diseases and pests: Critical status analysis and review of factors influencing their success, pp. 1–11. Retrieved from https://www.researchgate.net/publication/254838853_Chapter_1_Potential_of_biological_control

Nifakos, K., Tsalgatidou, P. C., Thomloudi, E. E., Skagia, A., Kotopoulis, D., Baira, E., ... & Katinakis, P. (2021). Genomic analysis and secondary metabolites production of the endophytic Bacillus velezensis Bvel1: A biocontrol agent against Botrytis cinerea causing bunch rot in post-harvest table grapes. Plants, 10(8), 1716. https://doi.org/10.3390/plants10081716

Patel, J. J., & Brown, M. E. (1969). Interactions of Azotobacter with rhizosphere and root-surface microflora. Plant and Soil, 31, 273–281. https://doi.org/10.1007/BF01373570

Romanazzi, G., Smilanick, J. L., Feliziani, E., & Droby, S. (2016). Integrated management of postharvest gray mold on fruit crops. Postharvest Biology and Technology, 113, 69–76. https://doi.org/10.1016/j.postharvbio.2015.11.003

Sedra, M. H., & Maslouhy, M. A. (1995). La fusariose vasculaire du palmier dattier (Bayoud). II. Action inhibitrice des filtrats de culture de six microorganismes antagonistes isolés des sols de la palmeraie de Marrakech sur le développement in vitro de Fusarium oxysporum f. sp. albedinis. Al Awamia, 90, 1–8. Retrieved from https://scholar.google.co.id/scholar?cites=5870104220054670988&as_sdt=2005&sciodt=0,5&hl=id

Toral, L., Rodríguez, M., Béjar, V., & Sampedro, I. (2018). Antifungal activity of lipopeptides from Bacillus XT1 CECT 8661 against Botrytis cinerea. Frontiers in Microbiology, 9, 377923. https://doi.org/10.3389/fmicb.2018.01315

Zhang, X., Zhou, Y., Li, Y., Fu, X., & Wang, Q. (2017). Screening and characterization of endophytic Bacillus for biocontrol of grapevine downy mildew. Crop Protection, 96, 173–79. https://doi.org/10.1016/j.cropro.2017.02.018

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