In vitro Evaluation of Burkholderia ambifaria for the Biological Control of Major Postharvest Fungal Pathogens in Citrus Fruits

Authors

DOI:

https://doi.org/10.24925/turjaf.v13is1.2352-2357.7827

Keywords:

Citrus, Biological control, Burkholderia ambifaria, MALDI TOF MS

Abstract

Postharvest fungal diseases in mandarin fruits cause significant economic and nutritional losses during transport and storage. The control of postharvest diseases in citrus fruit involves frequent and large amounts of chemical fungicides. Increasing concerns about health hazards and environmental pollution caused by the use of chemicals have necessitated the development and use of environmentally friendly control strategies as an alternative to chemicals for the control of post-harvest diseases in citrus fruits. The bacterial isolates as biological control agents (BCAs) are one of the most suitable alternatives to synthetic fungicides, which are banned or restricted for use in post-harvest disease management. Fungal diseases such as black mould (Aspergillus niger), blue mould (Penicillium italicum), green mould (Penicillium digitatum), sour rot (Geotrichum citri-aurantii), and anthracnose (Colletotrichum gloeosporioides) cause the most significant postharvest losses in citrus fruit. The BCA bacterial isolate used in this study was isolated from healthy mandarins and identified as Burkholderia ambifaria by Matrix Assisted Laser Desorption Ionisation Time of Flight-Mass Spectrometry (MALDI TOF MS; MicroFlex LT, Bruker Daltonics, Bremen, Germany) analysis. In this study, the antagonistic activity of B. ambifaria on the inhibition of mycelial growth of A niger, P. italicum, P. digitatum, G. citri-aurantii and C. gloeosporioides isolated from mandarin fruits was determined under in vitro conditions. In dual culture tests, the BCA B. ambifaria isolate inhibited the mycelial growth of C. gloeosporioides by 66.67%, A. niger by 69.40%, G. citri-aurantii by 73.33%, P. italicum and P. digitatum by 77.78%. The high level of antagonistic activity of the bacterial isolate in inhibiting the mycelial growth of fungal pathogens showed that B. ambifaria has the potential to be used as a BCA against diseases occurring during post-harvest storage.

Author Biographies

Yusuf Gümüş, Hatay Mustafa Kemal University, Faculty of Agriculture, Department of Plant Protection, 31034, Hatay, Türkiye

Hatay Mustafa Kemal University, Faculty of Agriculture, Department of Plant Protection, 31034, Hatay, Türkiye

Aysun Uysal, Hatay Mustafa Kemal University, Centre for Implementation and Research of Plant Health Clinic, 31034, Hatay, Türkiye

Hatay Mustafa Kemal University, Centre for Implementation and Research of Plant Health Clinic, 31034, Hatay, Türkiye

Soner Soylu, Hatay Mustafa Kemal University, Faculty of Agriculture, Department of Plant Protection, 31034, Hatay, Türkiye

Hatay Mustafa Kemal University, Faculty of Agriculture, Department of Plant Protection, 31034, Hatay, Türkiye

Emine Mine Soylu, Hatay Mustafa Kemal University, Faculty of Agriculture, Department of Plant Protection, 31034, Hatay, Türkiye

Hatay Mustafa Kemal University, Faculty of Agriculture, Department of Plant Protection, 31034, Hatay, Türkiye

Şener Kurt, Hatay Mustafa Kemal University, Faculty of Agriculture, Department of Plant Protection, 31034, Hatay, Türkiye

Hatay Mustafa Kemal University, Faculty of Agriculture, Department of Plant Protection, 31034, Hatay, Türkiye

References

An, C., Ma, S., Liu, C., Ding, H., & Xue, W. (2022). Burkholderia ambifaria XN08: A plant growth-promoting endophytic bacterium with biocontrol potential against sharp eyespot in wheat. Frontiers in Microbiology, 13, 906724. https://doi.org/10.3389/fmicb.2022.906724

Anonymous (2020a). Yaş meyve sebze sektörü Türkiye geneli değerlendirme raporu. https://www.akib.org.tr/files/documents/2020/Rapor/Ekim%202020%20YMS%20%C4%B0hracat%20De%C4%9Ferlendirme%20Raporu.pdf

Bhatta, U. K. (2022). Alternative management approaches of citrus diseases caused by Penicillium digitatum (green mold) and Penicillium italicum (blue mold). Frontiers in Plant Science, 12, 833328. https://doi.org/10.3389/fpls.2022.833328

Brown, G. E. (2003). Sour rot: Causal organism and disease cycle. University of Florida, Institute of Food and Agricultural Science Extension Service Fact Sheet, Gainesville, 137.

Butler, E. E., Fogle, D., & Miranda, M. (1988). Galactomyces citri-aurantii, a newly found teleomorph of Geotrichum citri-aurantii, the cause of sour rot of citrus fruit. Mycotaxon, 33, 197-212.

Carolis, E. D., Posteraro, B., Lass-Flo, C., Vella, A., Florio, A. R., Torelli, R., Girmenia, C., Colozza, C., Tortorano, A. M., Sanguinetti M., & Fadda, G. (2012). Species identification of Aspergillus, Fusarium and Mucorales with direct surface analysis by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clinical Microbiology and Infection, 18, 475-484. https://doi.org/10.1111/j.1469-0691.2011.03599.x

Chalupová, J., Raus, M., Sedlarova, M., & Sebela, M. (2014). Identification of fungal microorganisms by MALDI-TOF mass spectrometry. Biotechnology Advances, 32(1), 230-41. https://doi.org/10.1016/j.biotechadv.2013.11.002

Chen, X., Liu, J., Chen, A. J., Wang, L., Jiang, X., Gong, A., Liu, W., & Wu, H. (2024). Burkholderia ambifaria H8 as an effective biocontrol strain against maize stalk rot via producing volatile dimethyl disulfide. Pest Management Science, 80, 4125-4136. https://doi.org/10.1002/ps.7924

Desouki, A., Ahmed Reda, L., Rashed, M., & Shehata, S. (2023). Morphological and molecular identification of Penicillium digitatum causing green mould of citrus fruits in Egypt. Arab Universities Journal of Agricultural Sciences, 31(2), 281-293. https://doi.org/10.21608/AUJAS.2023.125489

Duman, K., & Soylu, S. (2019). Characterization of plant growth-promoting traits and antagonistic potentials of endophytic bacteria from bean plants against Pseudomonas syringae pv. phaseolicola. Bitki Koruma Bülteni, 59, 59-69. https://doi.org/10.16955/bitkorb.597214

Eckert, J. W., & Eaks, I. L. (1989). Postharvest disorders and diseases of citrus fruits. In W. Reuter, E. C. Calavan, & G. E. Carman (Eds.), The citrus industry (Vol. 5, pp. 179-260). University of California Press.

Food and Agriculture Organization [FAO] (2023). FAOSTAT, World production data. http://www.fao.org/faostat/en/#data/QC/visualize

Gomes, A. A. M., Queiroz, M. V., & Pereira, O. L. (2015). Mycofumigation for the biological control of post-harvest diseases in fruits and vegetables: A review. Austin Journal of Biotechnology & Bioengineering, 2, 1051.

Gümüş, Y., & Soylu, E. M. (2024). Endofit ve epifit bakteri izolatlarının bazı turunçgil fungal hastalık etmenlerine karşı in vitro biyokontrol etkinlik ve etki mekanizmalarının belirlenmesi. KSÜ Tarım ve Doğa Dergisi, 27(6), 1376-1391. https://doi.org/10.18016/ksutarimdoga.vi.1459337

Hoog, G. D., Guarro, J., Gene, J. F. M. J., & Figueras, M. J. (2000). Atlas of clinical fungi (No. Ed. 2, pp. viii+-1126).

Huang, F., Chen, G. Q., Hou, X., Fu, Y. S., Cai, L., Hyde, K. D., & Li, H. Y. (2013). Colletotrichum species associated with cultivated citrus in China. Fungal Diversity, 61(1), 61-74. https://doi.org/10.1007/s13225-013-0256-4

Kara, M., & Soylu, E. M. (2020). Assessment of glucosinolate-derived isothiocyanates as potential natural antifungal compounds against citrus sour rot disease agent Geotrichum citri-aurantii. Journal of Phytopathology, 168, 2792-89. https://doi.org/10.1111/jph.12889

Kara, M., Uysal, A., Soylu, S., Kurt, Ş., & Soylu, E. M. (2017). Identification of plant-associated microorganisms employing MALDI-TOF mass spectrometry as a rapid detection technique. International Conference on Agriculture, Forest, Food Sciences and Technologies, 15-17 May 2017, s.1111, Cappadocia/Turkey.

Lane, D. J. (1991). 16S/23S rRNA Sequencing. In: Stackebrandt, E. and Goodfellow, M., Eds., Nucleic Acid Techniques in Bacterial Systematic, John Wiley and Sons, New York, 115-175.

Lelliot, R. A., & Stead, D. E. (1987). Methods for the diagnosis of bacterial diseases of plants. (T.F. Preece, Editor). In: Methods in plant pathology. Vol 2, Blackwell Scientific Publications. pp. 176-177, Oxford.

Li, W., Roberts, D. P., Dery, P. D., Meyer, S. L. F., Lohrke, S., Lumsden, R. D., & Hebbar, K. P. (2002). Broad-spectrum antibiotic activity and disease suppression by the potential biocontrol agent Burkholderia ambifaria BC-F. Crop Protection, 21(2), 129-135. https://doi.org/10.1016/S0261-2194(01)00072-1

Lima, W. G., Spósito, M. B., Amorim, L., Gonçalves, F. P., & Melo de Filho, P. A. (2011). Colletotrichum gloeosporioides, a new causal agent of citrus post-bloom fruit drop. European Journal of Plant Pathology, 131(1), 157-165. https://doi.org/10.1007/s10658-011-9795-1

Liu, Y., Yao, S., Deng, L., Ming, J., & Zeng, K. (2019). Different mechanisms of action of isolated epiphytic yeasts against Penicillium digitatum and Penicillium italicum on citrus fruit. Postharvest Biology and Technology, 152, 100-110. https://doi.org/10.1016/j.postharvbio.2019.03.002

Lv, X., Zhao, S., Ning, Z., Zeng, H., Shu, Y., Tao, O., Xiao, C., Lu, C., & Liu, Y. (2015). Citrus fruits as a treasure trove of active natural metabolites that potentially provide benefits for human health. Chemistry Central Journal, 9, 68. https://doi.org/10.1186/s13065-015-0145-9

Perrone, G., Susca, A., Cozzi, G., Ehrlich, K., Varga, J., Frisvad, J. C., Meijer, M., Noonim, P., Mahakarnchanakul, W., & Samson, R. A. (2007). Biodiversity of Aspergillus species in some important agricultural products. Studies in Mycology, 59, 53-66. https://doi.org/10.3114/sim.2007.59.07

Prusky, D. (2011). Reduction of the incidence of postharvest quality losses, and future prospects. Food Security, 3, 463-474. https://doi.org/10.1007/s12571-011-0146-0

Rahman, M. A., Mahmud, T. M. M., Kadir, J., Abdul Rahman, R., & Begum, M. M. (2009). Enhancing the efficacy of Burkholderia cepacia B23 with calcium chloride and chitosan to control anthracnose of papaya during storage. The Plant Pathology Journal, 25(4), 361-368.

Schaad, N., Jones, J., & Chun, W. (2001). Laboratory Guide for Identification of Plant Pathogenic Bacteria. 3rd Edition, APS, St. Paul, Minnesota.

Scuderi, G., Bonaccorsi, A., Panebianco, S., Vitale, A., Polizzi, G., & Cirvilleri, G. (2009). Some strains of Burkholderia gladioli are potential candidates for postharvest biocontrol of fungal rots in citrus and apple fruits. Journal of Plant Pathology, 91(1), 207-213. https://www.jstor.org/stable/41998595

Sharma, R. R., Singh, D., & Singh, R. (2009). Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: A review. Biological Control, 50(3), 205-221. https://doi.org/10.1016/j.biocontrol.2009.05.001

Shi, J., & Du, J. (2023). Identification of postharvest fruit biocontrol strain Burkholderia contaminans against fungal decay. European Journal of Horticultural Science, 88(1), 1-12.

Soylu, E. M., Soylu, S., Kara, M., & Kurt, Ş. (2020). Sebzelerde sorun olan önemli bitki fungal hastalık etmenlerine karşı vermikomposttan izole edilen mikrobiyomların in vitro antagonistik etkilerinin belirlenmesi. KSÜ Tarım ve Doğa Dergisi, 23(1), 7-18. https://doi.org/10.18016/ksutarimdoga.vi.601936

Soylu, S., Kara, M., Soylu, E. M., Uysal, A., & Kurt, Ş. (2022). Determination of biocontrol potentials of endophytic bacteria in biological control of citrus sour rot disease caused by Geotrichum citri-aurantii. Tekirdağ Ziraat Fakültesi Dergisi, 19(1), 177-191. https://doi.org/10.33462/jotaf.944704

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), 1-30. https://doi.org/10.1080/07352680091139169

Sutton, B. C. (1980). The Coelomycetes: Fungi Imperfecti with Pycnidia, Aservuli and Stromata. Kew, UK: Commonwealth Mycological Institute.

Tekiner, N., Tozlu, E., & Kotan, R. (2019). Domateste Alternaria alternata (Fr.) Keissl’nın bazı bakteriler ile biyolojik mücadelesi. Plant Protection Bulletin, 59(4), 57-68. https://doi.org/10.16955/bitkorb.550112

Türkiye İstatistik Kurumu [TUIK] (2023). Tarım verileri. https://data.tuik.gov.tr/Kategori/GetKategori?p=tarim-111&dil=1

Visagie, C. M., Houbraken, J., Frisvad, J. C., Hong, S. B., Klaassen, C. H. W., Perrone, G., Seifert, K. A., Varga, J., Yaguchi, T., & Samson, R. A. (2014). Identification and nomenclature of the genus Penicillium. Studies in Mycology, 78, 343-371. https://doi.org/10.1016/j.simyco.2014.09.001

Zhang, Z., Zhu, Z., Ma, Z., & Li, H. (2009). A molecular mechanism of azoxystrobin resistance in Penicillium digitatum UV mutants and a PCR-based assay for detection of azoxystrobin-resistant strains in packing- or store-house isolates. International Journal of Food Microbiology, 131(2-3), 157-161. https://doi.org/10.1016/j.ijfoodmicro.2009.02.015

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Published

25.09.2025