Antagonistic activity of Candida utilis SCKU1 yeast against crown rot disease of ‘Hom Thong’ Banana (Musa acuminata, AAA group)
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Abstract
Candida utilis SCKU1 yeast had an antifungal activity on seven isolates of fruit postharvest pathogens ranging from 21.5–49.1% inhibition. It was the most effective antagonist against two pathogens, Colletotrichum musae BCm1 causing banana anthracnose and Lasiodiplodia pseudotheobromae DL1 causing durian fruit rot. Inhibition zone appearances on co-culture plates were observed on four pathogens including C. gloeosporioides DCg1, C. musae BCm1, L. pseudotheobromae DL1 and Phomopsis sp. isolate DP1. The largest zone of inhibition (10.15±0.75 mm wide) was noticed in L. pseudotheobromae DL1 plate. Yeast culture filtrate was able to inhibit the mycelial growth of all pathogens, but the most inhibition was found in four pathogens, C. gloeosporioides DCg1, C. gloeosporioides MCg1, C. musae BCm1 and Phomopsis sp. isolate DP1 with 80.6–84.2% inhibition. Additionally, both yeast cell suspension and its culture filtrate significantly reduced the disease severity of banana crown rot by 35.9 and 33.5%, respectively. However, the mechanism of antagonistic yeast against crow rot disease was demonstrated by producing cell wall degrading enzymes such as beta-1,3-glucanase and chitinase. Cell suspension and culture filtrate of yeast also provided the induction of disease resistance by stimulating the activity of the defense-related enzyme, phenylalanine ammonia-lyase (PAL), beta-1,3-glucanase and chitinase against the disease. PAL activity was greatly activated by both treatments at 72 h after application (haa). The activity of beta-1,3-glucanase and chitinase was also induced by both treatments starting from 48 haa, but the highest level of both enzyme activities was demonstrated at 96 haa. At 96 haa, the level of chitinase activity was extremely enhanced by culture filtrate of yeast. This preliminary study revealed that either yeast cell suspension or its culture filtrate might be alternatively used for controlling banana crow rot on banana production
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References
Ali, S., Ganai, B. A., Kamili, A. N., Bhat, A. A., Mir, Z. A., Bhat, J. A., Tyagi, A., Islam, S. T., Mushtaq, M. and Yadav, P. (2018). Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance. Microbiological Research, 212:29-37.
Alvindia, D. G. (2012). Revisiting hot water treatments in controlling crown rot of banana cv. Buñgulan. Crop Protection, 33:59-64.
Alvindia, D. G. (2013a). Enhancing the bioefficacy of Bacillus amyloliquefaciens DGA14 with inorganic salts for the control of banana crown rot. Crop Protection, 51:1-6.
Alvindia, D. G. (2013b). An integrated approach with hot water treatment and salt in the control of crown rot disease and preservation of quality in banana. International Journal of Pest Management, 59:271-278.
Alvindia, D. G. (2013c). Sodium bicarbonate enhances efficacy of Trichoderma harzianum DGA01 in controlling crown rot of banana. Journal of General Plant Pathology, 79:136-144.
Alvindia, D. G. and Natsuaki, K. (2008). Evaluation of fungal epiphytes isolated from banana fruit surfaces for biocontrol of banana crown rot disease. Crop Protection, 27:1200-1207.
Alvindia, D. G. and Natsuaki, K. T. (2009). Biocontrol activities of Bacillus amyloliquefaciens DGA14 isolated from banana fruit surface against banana crown rot-causing pathogens. Crop Protection, 28:236-242.
Assis, J. S., Maldonado, R., Muñoz, T., Maria, I. E. and Merodio, C. (2001). Effect of high carbon dioxide concentration on PAL activity and phenolic contents in ripening cherimoya fruit. Postharvest Biology and Technology, 23:33-39.
Bastiaanse, H., Bellaire, L., Lassois, L., Misson, C. and Jijakli, M. (2010). Integrated control of crown rot of banana with Candida oleophila strain O, calcium chloride and modified atmosphere packaging. Biological Control, 53:100-107.
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry, 72:248-254.
Cabral, C. D. L., Rodríguez, A., Andrade, M. J., Patriarca, A. and Delgado, J. (2021). Effect of Debaryomyces hansenii and the antifungal PgAFP protein on Alternaria spp. growth, toxin production, and RHO1 gene expression in a tomato-based medium. Food Microbiology, 97:1-8.
Capistran, L. L., Rodriguez, R. Z., Cervantes, T. C., Perez, J. J. R., Rangel, P. P. and Montiel, L. G. H. (2020). Efficiency of marine bacteria and yeasts on the biocontrol activity of Pythium ultimum in ancho-type pepper seedlings. Agronomy, 10:1-12.
Chan, Z. and Tian, S. (2005). Interaction of antagonistic yeasts against postharvest pathogens of apple fruit and possible mode of action. Postharvest Biology and Technology, 36:215-223.
Chanchaichaovivat, A., Panijpan, B. and Ruenwongsa, P. (2008). Putative modes of action of Pichia guilliermondii strain R13 in controlling chilli anthracnose after harvest. Biological Control, 47:207-215.
Chen, P. H., Chen, R. Y. and Chou, J. Y. (2018). Screening and evaluation of yeast antagonists for biological control of Botrytis cinerea on strawberry fruits. Mycobiology, 46:33-46.
Delali, K. I., Chen, O., Wang, W., Yi, L., Deng, L. and Zeng, K. (2021). Evaluation of yeast isolates from kimchi with antagonistic activity against green mold in citrus and elucidating the action mechanisms of three yeast: P. kudriavzevii, K. marxianus, and Y. lipolytica. Postharvest Biology and Technology, 176:1-11.
Deshavath, N. N., Mukherjee, G., Goud, V. V., Veeranki, V. D. and Sastri, C. V. (2020). Pitfalls in the 3, 5-dinitrosalicylic acid (DNS) assay for the reducing sugars: Interference of furfural and 5-hydroxymethylfurfural. International Journal of Biological Macromolecules, 156:180-185.
Ewané, C. A., Lassois, L., Brostaux, Y., Lepoivre, P. and De Lapeyre De Bellaire, L. (2013). The susceptibility of bananas to crown rot disease is influenced by geographical and seasonal effects. Canadian Journal of Plant Pathology, 35:27-36.
Feng, M., Lv, Y., Li, T., Li, X., Liu, J., Chen, X., Zhang, Y., Chen, X. and Wang, A. (2021). Postharvest Treatments with Three Yeast Strains and Their Combinations to Control Botrytis cinerea of Snap Beans. Foods, 10:1-26.
Francesco, D. A., Roberti, R., Martini, C., Baraldi, E. and Mari, M. (2015). Activities of Aureobasidium pullulans cell filtrates against Monilinia laxa of peaches. Microbiological Research, 181:61-67.
Freimoser, F. M., Rueda-Mejia, M. P., Tilocca, B. and Migheli, Q. (2019). Biocontrol yeasts: mechanisms and applications. World Journal of Microbiology and Biotechnology, 35:1-19.
Gao, Z., Zhang, R. and Xiong, B. (2021). Management of postharvest diseases of kiwifruit with a combination of the biocontrol yeast Candida oleophila and an oligogalacturonide. Biological Control, 156:1-6.
Han, P., Ni, L., Wei, Y., Jiang, S., Xu, F., Wang, H. and Shao, X. (2021). Optimization of the freeze-drying of marine yeast Sporidiobolus pararoseus ZMY-1 for its application in biocontrol of fungal infections. Biological Control, 161:1-8.
Hassan, H., Mohamed, M. T. M., Yusoff, S. F., Hata, E. M. and Tajidin, N. E. (2021). Selecting antagonistic yeast for postharvest biocontrol of Colletotrichum gloeosporioides in papaya fruit and possible mechanisms involved. Agronomy, 11:1-17.
Jamal, A., Farhat, H., Urooj, F., Rahman, A., Irfan, M. and Ehteshamul-Haque, S. (2021). Characterization of endophytic yeast and its suppressive effect on root rotting fungi of tomato under neem cake soil amendment. Egyptian Journal of Biological Pest Control, 31:1-12.
Johanson, A. and Blazquez, B. (1992). Fungi associated with banana crown rot on field-packed fruit from the Windward Islands and assessment of their sensitivity to the fungicides thiabendazole, prochloraz and imazalil. Crop Protection, 11:79-83.
Kamel, M. a. M., Cortesi, P. and Saracchi, M. (2016). Etiological agents of crown rot of organic bananas in Dominican Republic. Postharvest Biology and Technology, 120:112-120.
Kamsu, N. P., Tchinda, S. E., Tchameni, N. S., Jazet, D. P. M., Madjouko, M. A., Youassi Youassi, O., Sameza, M. L., Tchoumbougnang, F. and Menut, C. (2019). Antifungal activities of essential oils of cinnamon (Cinnamomum zeylanicum) and lemongrass (Cymbopogon citratus) on crown rot pathogens of banana. Indian Phytopathology, 72:131-137.
Kareem, M. M. A., Zohri, A. N. A. and Elmohsen, E. N. S. A. (2021). Novel marine yeast strains as plant growth-promoting agents improve defense in wheat (Triticum aestivum) against Fusarium oxysporum. Journal of Plant Diseases and Protection, 128:973-988.
Kulkarni, S. A., Sellamuthu, P. S., Anitha, D. P. M. and Madhavan, T. (2021). In vitro and in silico evaluation of antifungal activity of cassia (Cinnamomum cassia) and holy basil (Ocimum tenuiflorum) essential oils for the control of anthracnose and crown-rot postharvest diseases of banana fruits. Chemical Papers, 75:2043-2057.
Kulkarni, S. A., Sellamuthu, P. S., Nagarajan, S. K., Madhavan, T. and Sadiku, E. R. (2022). Antifungal activity of wild bergamot (Monarda fistulosa) essential oil against postharvest fungal pathogens of banana fruits. South African Journal of Botany, 144:166-174.
Lassois, L., Bellaire, L. and Jijakli, M. (2008). Biological control of crown rot of bananas with Pichia anomala strain K and Candida oleophila strain O. Biological Control, 45:410-418.
Lassois, L., Jijakli, M., Chillet, M. and Bellaire, L. (2010). Crown rot of bananas: preharvest factors involved in postharvest disease development and integrated control methods. Plant Disease, 94:648-658.
Maawali, S. S. A., Sadi, A. M. A., Sheriqi, S. K. A., Sabahi, J. N. A. and Velazhahan, R. (2021). The potential of antagonistic yeasts and bacteria from tomato phyllosphere and fructoplane in the control of Alternaria fruit rot of tomato. All Life, 14:34-48.
Manigo, B. (2019). Bioefficacy test of Hatake™ (Bacillus amyloliquefaciens D203 strain) for control of crown rot disease in ‘Cavendish’ bananas. Acta Horticulturae, 1:85-92.
Mehalawy, E. A. (2004). The rhizosphere yeast fungi as biocontrol agents for wilt disease of kidney bean caused by Fusarium oxysporum. International Journal of Agriculture and Biology (Pakistan), 6:310-316.
Mohamed, S. N. T., Ding, P., Kadir, J. and M Ghazali, H. (2017). Potential of UVC germicidal irradiation in suppressing crown rot disease, retaining postharvest quality and antioxidant capacity of Musa AAA "Berangan" during fruit ripening. Food Science and Nutrition, 5:967-980.
Mukherjee, A., Verma, J. P., Gaurav, A. K., Chouhan, G. K., Patel, J. S. and Hesham, A. E.-L. (2020). Yeast a potential bio-agent: future for plant growth and postharvest disease management for sustainable agriculture. Applied Microbiology and Biotechnology, 104:1497-1510.
Niroshini, G. W. K. R. and Karunaratne, A. M. (2009). Interactions of Colletotrichum musae and Lasiodiplodia theobromae and their biocontrol by Pantoea agglomerans and Flavobacterium sp. in expression of crown rot of “Embul” banana. BioControl, 54:587-596.
Oztekin, S. and Karbancioglu, G. F. (2021). Bioprospection of Metschnikowia sp. isolates as biocontrol agents against postharvest fungal decays on lemons with their potential modes of action. Postharvest Biology and Technology, 181:1-12.
Rathnayake, R., Savocchia, S., Schmidtke, L. and Steel, C. (2018). Characterisation of Aureobasidium pullulans isolates from Vitis vinifera and potential biocontrol activity for the management of bitter rot of grapes. European Journal of Plant Pathology, 151:593-611.
Restuccia, C., Lombardo, M., Scavo, A., Mauromicale, G. and Cirvilleri, G. (2020). Combined application of antagonistic Wickerhamomyces anomalus BS91 strain and Cynara cardunculus L. leaf extracts for the control of postharvest decay of citrus fruit. Food Microbiology, 92:1-6.
Sabaghian, S., Braschi, G., Vannini, L., Patrignani, F., Samsulrizal, N. H. and Lanciotti, R. (2021). Isolation and identification of wild yeast from malaysian grapevine and evaluation of their potential antimicrobial activity against grapevine fungal pathogens. Microorganisms, 9:1-16.
Santos, A., Marquina, D., Leal, J. and Peinado, J. (2000). (1→ 6)-β-D-glucan as cell wall receptor for Pichia membranifaciens killer toxin. Applied and Environmental Microbiology, 66:1809-1813.
Shao, Y. Z., Zeng, J. K., Hong, T., Yi, Z. and Wen, L. (2019). The chemical treatments combined with antagonistic yeast control anthracnose and maintain the quality of postharvest mango fruit. Journal of Integrative Agriculture, 18:1159-1169.
Souza, M. L. D., Ribeiro, L. S., Miguel, M. G. D. C. P., Batista, L. R., Schwan, R. F., Medeiros, F. H. and Silva, C. F. (2021). Yeasts prevent ochratoxin A contamination in coffee by displacing Aspergillus carbonarius. Biological Control, 155:1-11.
Thangavelu, R., Sangeetha, G. and Mustaffa, M. M. (2007). Cross-infection potential of crown rot pathogen (Lasiodiplodia theobromae) isolates and their management using potential native bioagents in banana. Australasian Plant Pathology, 36:595-605.
Tongsri, V. and Sangchote, S. (2009). Yeast metabolites inhibit banana anthracnose fungus Colletotrichum musae. Asian Journal of Food and Agro-Industry 2:807-816.
Triest, D. and Hendrickx, M. (2016). Postharvest disease of banana caused by Fusarium musae: a public health concern? PLOS Pathogens, 12:1-5.
Vargas, M., Garrido, F., Zapata, N. and Tapia, M. (2012). Isolation and selection of epiphytic yeast for biocontrol of Botrytis cinerea Pers. on table grapes. Chilean Journal of Agricultural Research, 72:332-337.
Velasquez, L. and Hammerschmidt, R. (2004). Development of a method for the detection and quantification of total chitinase activity by digital analysis. Journal of Microbiological Methods, 59:7-14.
Yadav, V., Wang, Z., Wei, C., Amo, A., Ahmed, B., Yang, X. and Zhang, X. (2020). Phenylpropanoid pathway engineering: an emerging approach towards plant defense. Pathogens, 9:1-25.
Zhang, J., Liu, J., Xie, J., Deng, L., Yao, S. and Zeng, K. (2019). Biocontrol efficacy of Pichia membranaefaciens and Kloeckera apiculata against Monilinia fructicola and their ability to induce phenylpropanoid pathway in plum fruit. Biological Control, 129:83-91.
Zhang, X., Li, B., Zhang, Z., Chen, Y. and Tian, S. (2020). Antagonistic yeasts: a promising alternative to chemical fungicides for controlling postharvest decay of fruit. Journal of Fungi, 6:1-15.
Zhao, L., Wang, Y., Dhanasekaran, S., Guo, Z., Chen, S., Zhang, X. and Zhang, H. (2021). Efficacy of Wickerhamomyces anomalus yeast in the biocontrol of blue mold decay in apples and investigation of the mechanisms involved. BioControl, 66:547-558.
Zhao, S., Guo, Y., Wang, Q., Luo, H., He, C. and An, B. (2020). Expression of flagellin at yeast surface increases biocontrol efficiency of yeast cells against postharvest disease of tomato caused by Botrytis cinerea. Postharvest Biology and Technology, 162:1-7.
Zhimo, V. Y., Dilip, D., Sten, J., Ravat, V., Bhutia, D., Panja, B. and Saha, J. (2017). Antagonistic yeasts for biocontrol of the banana postharvest anthracnose pathogen Colletotrichum musae. Journal of Phytopathology, 165:35-43.
Zong, Y., Liu, J., Li, B., Qin, G. and Tian, S. (2010). Effects of yeast antagonists in combination with hot water treatment on postharvest diseases of tomato fruit. Biological Control, 54:316-321.
