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Biocontrol ability of marine yeasts against postharvest diseases in mangos caused by Colletotrichum gloeosporioides and Lasiodiplodia theobromae

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Abstract

Anthracnose and stem-end rot are among the most devastating pathogens affecting mangos, leading to significant losses due to rotting during storage. This study aimed to investigate marine strains' potential as biocontrol agents against the postharvest pathogenic fungi Colletotrichum gloeosporioides and Lasiodiplodia theobromae. A total of 415 marine yeast strains isolated from marine environments were evaluated for their antifungal activities against C. gloeosporioides and L. theobromae using a dual culture method. Out of these, 115 yeast strains were found to inhibit the growth of C. gloeosporioides, while 31 strains inhibited the growth of L. theobromae. Among these yeast strains, only eighteen proved effective against both pathogenic fungi. The strains Meyerozyma guilliermondii ARU3232-1 and Pichia kudriavzevii DMKUJC44-2 demonstrated the most significant inhibition of radial mycelial growth. The production of volatile organic compounds (VOCs) showcased an in vitro inhibitory effect on the growth of both C. gloeosporioides and L. theobromae. However, assays testing the production of cellulase, chitinase, pectinase and protease by these antagonistic yeasts yielded negative results. Additionally, there was no observed Fe3+ binding competition between the yeast and mold. M. guilliermondii ARU3232-1 showed strong biofilm formation, while P. kudriavzevii DMKUJC44-2 demonstrated moderate biofilm formation. In vivo assays indicated that M. guilliermondii ARU3232-1 reduced anthracnose disease severity by 71 ± 3%, whereas P. kudriavzevii DMKUJC44-2 decreased stem-end rot severity by 61 ± 3%. Therefore, both antagonist marine yeasts have the potential to be used as biocontrol agents against anthracnose and stem-end rot diseases of mango fruits.

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References

  • Ajitomi, A., Minoshima, A., Takushi, T., Truong, H. H., Ooshiro, A., Yamashiro, M., Arasaki, C., & Hirooka, Y. (2020). First report of mango (Mangifera indica) stem-end rot caused by two Diaporthe species and their susceptibility to procymidone. Journal of General Plant Pathology, 86, 237–244.

    Article  CAS  Google Scholar 

  • Alkan, N., & Kumar, P. (2018). Postharvest storage management of mango fruit. Achieving sustainable cultivation of mangoes. Galan Sauco, Eds, 377–402.

    Google Scholar 

  • Alvarez, A. M., & Nishijima, W. T. (1987). Post harvest diseases of papaya. Plant Disease, 71, 681–686.

    Article  Google Scholar 

  • Barkai-Golan, R. (2001). Postharvest disease of fruits and vegetables – Development and control. Elsevier Ltd.

    Google Scholar 

  • Bautista-Rosales, P. U., Calderon-Santoyo, M., Servín-Villegas, R., Ochoa-Álvarez, N. A., Vázquez-Juárez, R., & Ragazzo-Sánchez, J. A. (2014). Biocontrol action mechanisms of Cryptococcus laurentii on Colletotrichum gloeosporioides of mango. Crop Protection, 65, 194–201.

    Article  Google Scholar 

  • Cheng, L., Zhou, L., Li, D., Gao, Z., Teng, J., Nie, X., Guo, F., Wang, C., Wang, X., Li, S., & Li, X. (2023). Combining the biocontrol agent Meyerozyma guilliermondii with UV-C treatment to manage postharvest gray mold on kiwifruit. Biological Control, 180, 105198. https://doi.org/10.1016/j.biocontrol.2023.105198

    Article  CAS  Google Scholar 

  • Chi, M., Li, G., Liu, Y., Liu, G., Li, M., Zhang, X., Sun, Z., Sui, Y., & Liu, J. (2015). Increase in antioxidant enzyme activity, stress tolerance and biocontrol efficacy of Pichia kudriavzevii with the transition from a yeast-like to biofilm morphology. Biological control, 90, 113–119.

    Article  CAS  Google Scholar 

  • Chi, Z., Liu, G.-L., Lu, Y., Jiang, H., & Chi, Z.-M. (2016). Bio-products produced by marine yeasts and their potential applications. Bioresource Technology, 202, 244–252.

    Article  CAS  PubMed  Google Scholar 

  • Connell, L., Redman, R., Craig, S., Scorzetti, G., Iszard, M., & Rodriguez, R. (2008). Diversity of soil yeast isolated from South Victoria Land, Antarctica. Microbiology Ecology, 56, 448–459.

    Article  CAS  Google Scholar 

  • Delali, K.I., Chen, O., Wang, W., Yi, L., Deng, L., & 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, 111495. https://doi.org/10.1016/j.postharvbio.2021.111495

  • Galsurker, O., Diskin, S., Duanis-Assaf, D., Doron-Faigenboim, A., Maurer, D., Feygenberg, O., & Alkan, N. (2018). Harvesting mango fruit with a short stem-end altered endophytic microbiome and reduce stem-end rot. Microorganisms, 8, 558. https://doi.org/10.3390/microorganisms8040558

    Article  CAS  Google Scholar 

  • Gamagae, S. U., Sivakumar, D., & Wijesundera, R. L. C. (2004). Evaluation of post-harvest application of sodium bicarbonate-incorporated wax formulation and Candida oleophila for the control of anthracnose of papaya. Crop Protection, 23, 575–579.

    Article  CAS  Google Scholar 

  • Gardini, F., Tofalo, R., Belletti, N., Iucci, L., Suzzi, G., Torriani, S., Guerzoni, M. E., & Lanciotti, R. (2006). Characterization of yeasts involved in the ripening of Pecorino Crotonese cheese. Food Microbiology, 23, 641–648.

    Article  CAS  PubMed  Google Scholar 

  • Gava, C. A. T., De Castro, A. P. C., Pereira, C. A., & Fernandes-Júnior, P. I. (2018). Isolation of fruit colonizer yeasts and screening against mango decay caused by multiple pathogens. Biological Control, 117, 137–146.

    Article  Google Scholar 

  • Guo, J., Zhang, X., Zhang, M., Zhou, S., Luo, X., Liu, J., Liu, J., Gao, J., & Zhao, X. (2023). Multiple pathways involving in the Ca ascorbate-induced enhancement of Meyerozyma guilliermondii biocontrol efficacy. Biological Control, 186, 105319. https://doi.org/10.1016/j.biocontrol.2023.105319

    Article  CAS  Google Scholar 

  • Huang, Y., Sun, C., Guan, X., Lian, S., Li, B., & Wang, C. (2021). Biocontrol efficiency of Meyerozyma guilliermondii Y-1 against apple postharvest decay caused by Botryosphaeria dothidea and the possible mechanisms of action. International Journal of Food Microbiology, 338, 108957. https://doi.org/10.1016/j.ijfoodmicro.2020.108957

    Article  CAS  PubMed  Google Scholar 

  • Herrera-Balandrano, D. D., Wang, S.-Y., Wang, C.-X., Shi, X.-C., Liu, F.-Q., & Laborda, P. (2023). Antagonistic mechanisms of yeasts Meyerozyma guilliermondii and M. caribbica for the control of plant pathogens: A review. Biological control, 186, 105333 10.1016/j.biocontrol.2023.105333.

    Article  Google Scholar 

  • Johnson, G. I., Mead, A. J., Cooke, A. W., & Dean, J. R. (1992). Mango stem and rot pathogens fruit infection by endophytic colonization of the inflorescence and pedicel. The Annals of Applied Biology, 120, 225–234.

    Article  Google Scholar 

  • Kaewkrajay, C., Chanmethakul, T., & Limtong, S. (2020). Assessment of diversity of culturable marine yeasts associated with corals and zoanthids in the Gulf of Thailand. South China Sea. Microorganisms, 8, 474. https://doi.org/10.3390/microorganisms8040474

    Article  CAS  PubMed  Google Scholar 

  • Kaewkrajay, C., Putchakarn, S., & Limtong, S. (2021). Cultivable yeasts associated with marine sponges in the Gulf of Thailand, South China Sea. Antonie van Leeuwenhoek, 114, 253–274.

    Article  CAS  PubMed  Google Scholar 

  • Kasana, R. C., Salwan, R., Dhar, H., Dutt, S., & Gulati, A. (2008). A rapid and easy method for the detection of microbial cellulases on agar plates using Gram’s iodine. Current Microbiology, 57(503), 507. https://doi.org/10.1007/s00284-008-9276-8

    Article  CAS  Google Scholar 

  • Kurtzman, C. P., Fell, J. W., & Boekhout, T. (2011). Deffinition, Classification and Nomenclature of the yeast. In C. P. Kurtzman, J. W. Fell, & T. Boekhout (Eds.), The yeast a taxonomic study (5th ed.). Elsevier.

    Google Scholar 

  • Li, Z. (2019). Sponge and coral microbiomes. In Symbiotic Microbiomes of Coral Reefs Sponges and Corals; Li, Z., Ed.; Spinger Nature: Berlin/Heidelberg, Germany, pp. 17–28.

  • Liu, J., Sui, Y., Wisniewski, M., Droby, S., & Liu, Y. (2013). Review; Utilization of antagonistic yeasts to manage postharvest fungal diseases of fruit. International Journal of Food Microbiology, 167, 153–160.

    Article  PubMed  Google Scholar 

  • Liu, X., Gao, Y., Yang, H., Li, L., Jiang, Y., Li, Y., & Zheng, J. (2020). Pichia kudriavzevii retards fungal decay by influencing the fungal community succession during cherry tomato fruit storage. Food Microbiology, 88, 103404. https://doi.org/10.1016/j.fm.2019.103404

    Article  CAS  PubMed  Google Scholar 

  • Medina-Córdova, N., López-Aguilar, R., Ascencio, F., Castellanos, T., Campa- Córdova, A. I., & Angulo, C. (2016). Biocontrol activity of the marine yeast Debaryomyces hansenii against phytopathogenic fungi and its ability to inhibit mycotoxins production in maize grain (Zea mays L.). Biological Control, 97, 70–79.

    Article  Google Scholar 

  • Merín, M. G., Mendoza, L. M., Farias, M. E., & Morata de Ambrosini, V. I. (2011). Isolation and selection of yeasts from wine grape ecosystem secreting cold-active pectinolytic activity. International Journal of Food Microbiology, 147(144), 148. https://doi.org/10.1016/j.ijfoodmicro.2011.04.004

    Article  CAS  Google Scholar 

  • Naim, M. A., Smidt, H., & Sipkema, D. (2017). Fungi found in Mediterranean and North Sea sponges: How specific are they? PeerJ, 5, e3722. https://doi.org/10.7717/peerj.3722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson, S. C. (2008). Mango anthracnose (Collectotrichum gloeosporioides). In Cooperative Extension Service. University of Hawaii at Manoa.

    Google Scholar 

  • Nujthet, Y., Kaewkrajay, C., Kijjoa, A., & Dethoup, T. (2023). Biocontrol efficacy of antagonists Trichoderma and Bacillus against post-harvest diseases in mangos. European Journal of Plant Pathology. https://doi.org/10.1007/s10658-023-02757-1

  • Nunes, C. A. (2012). Biological control of postharvest of fruit. European Journal of Plant Pathology, 133, 181–196.

    Article  Google Scholar 

  • Parafati, L., Vitale, A., Rextuccia, C., & Cirvilleri, G. (2015). Biocontrol ability and action mechanism of food-isolated yeast strains against Botrytis cinerea causing post-harvest bunch rot of table grape. Food Microbiology, 47, 85–92.

    Article  CAS  PubMed  Google Scholar 

  • Paulino, G. V. B., Félix, C. R., Broetto, L., & Landell, M. F. (2017). Diversity of culturable yeasts associated with zoanthids from Brazilian reef and its relation with anthropogenic disturbance. Marine Pollution Bulletin, 123, 253–260.

    Article  CAS  PubMed  Google Scholar 

  • Prusky, D. (1996). Pathogen quiescence in postharvest diseases. Annual Review of Phytopathology, 34, 413–434.

    Article  CAS  PubMed  Google Scholar 

  • Prusky, D., & Plumbley, R.A. (1992). Quiescent infection of Colletotrichum in tropical and subtropical fruits. In: Baily, J.A., Jeger, M. (Eds.), Collectotrichum.

  • Robs, C. F. (1996). Enfermidades de pós-colheita do mamăo. In L. G. Mendes, J. L. L. Dantas, & C. F. G. Morales (Eds.), Mamăo No Brasil. EUFBA/ EMBRAPA-CNPMF, Cruz das Almas.

    Google Scholar 

  • Růžička, F., Hola, V., Votava, M., & Tejkalova, R. (2007). Importance of biofilm in Candida parapsilosis and evaluation of its susceptibility to antifungal agents by colorimetric method. Folia Microbiologica, 52(3), 209–214.

    Article  PubMed  Google Scholar 

  • Sarkar, A., & Rao, K. V. B. (2016). Marine yeast: A potential candidate for biotechnological applications-A review. Asian Journal of Microbiology, Biotechnology & Environmental Sciences, 18(3), 627–634.

    Google Scholar 

  • Shen, H., Wei, Y., Wang, X., Xu, C., & Shao, X. (2019). The marine yeast Sporidiobolus pararoseus ZMY-1 has antagonistic properties against Botrytis cinerea in vitro and in strawberry fruit. Postharvest Biology and Technology, 150, 1–8.

    Article  Google Scholar 

  • Sholberg, P. L., & Conway, W. S. (2001). Postharvest pathology. http://www.ba.ars.usda.gov/hb66/022pathology.pdf. Accessed 28 Jul 2023.

  • Snowdon, A. I. (2010). A colour atlas of post-harvest diseases and disorders of fruit and vegetables: General Introduction and Fruits. Manson.

    Google Scholar 

  • Souza, C. P., Burbano-Rosero, E. M., Almeida, B. C., Martins, G. G., Albertini, L. S., & Rivera, I. N. G. (2009). Culture medium for isolating chitinolytic bacteria from seawater and plankton. World Journal of Microbiology and Biotechnology, 25, 2079–2082.

    Article  Google Scholar 

  • Stepanović, S., Vuković, D., Hola, V., Bonaventura, G., Djukić, S., Ćirković, L., & Ruzicka, F. (2007). Quantification of biofilm in microtiter plates: Overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. Acta Pathologica, Microbiologica, et Immunologica Scandinavica, 115, 891–899.

    Article  PubMed  Google Scholar 

  • Suasa-ard, S., Eakjamnong, W., & Dethoup, T. (2019). A novel biological control agent against postharvest mango disease caused by Lasiodioplodia theobromae. European Journal of Plant Pathology, 155(2), 583–592.

    Article  CAS  Google Scholar 

  • Sun, C., Huang, Y., Lian, S., Saleem, M., Li, B., & Wang, C. (2021). Improving the biocontrol efficacy of Meyerozyma guilliermondii Y-1 with melatonin against postharvest gray mole in apple fruit. Postharvest Biology and Technology, 171, 111351. https://doi.org/10.1016/j.postharvbio.2020.111351

    Article  CAS  Google Scholar 

  • Vaca, I., Faúndez, C., Maza, F., Paillavil, B., Hernández, V., Acosta, F., Levicán, G., Martínez, C., & Chávez, R. (2013). Cultivable psychrotolerant yeasts associated with Antarctic marine sponges. World Journal of Microbiology and Biotechnology, 29, 183–189.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y. F., Bao, Y. H., Shen, D. H., Feng, W., Yu, T., Zhang, J., & Zheng, X. D. (2008). Biocontrol of Alternaria alternata on cherry tomato fruit by use of marine yeast Rhodosporidium paludigenum Fell & Tallman. International journal of Food Microbiology, 123, 234–239.

    Article  PubMed  Google Scholar 

  • Wang, Y., Yu, T., Xia, J., Yu, D., Wang, J., & Zheng, X. (2010). Biocontrol of postharvest gray mold of cherry tomatoes with the marine yeast Rhodosporidium paludigenum. Biological control, 53, 178–182.

    Article  Google Scholar 

  • Wang, Y., Tang, F., Xia, J., Yu, T., Wang, J., Azhati, R., & Zheng, X. D. (2011). A combination of marine yeast and food additive enhances preventive effects on postharvest decay of jujubes (Zizyphus jujube). Food Chemistry, 125, 835–840.

    Article  CAS  Google Scholar 

  • Zaky, A. S., Tucker, G. A., Daw, Z. Y., & Du, C. (2014). Marine yeast isolation and industrial application. FEMS Yeast Research, 14, 813–825.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, X., Hua, M., Song, C., & Chi, Z. (2012). Occurrence and diversity of marine yeasts in Antarctica environments. Journal of Ocean University of China, 11, 70–74.

    Article  CAS  Google Scholar 

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Acknowledgements

This work was completely supported by a grant from the National Research Council of Thailand (NRCT) and would like to thank Prof. Dr. Savitree Limtong, Department of Microbiology, Faculty of Science, Kasetsart University, for a kindly and useful suggestion.

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  1. Faculty of Science and Technology, Phranakhon Si Ayutthaya Rajabhat University, 96, Pridi Banomyong Rd., Phranakhon Si Ayutthaya, 13000, Thailand

    Chutima Kaewkrajay

  2. Faculty of Agriculture, Kasetsart University, 50 Paholyothin Rd., Bangkok, 10900, Thailand

    Tida Dethoup

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  1. Chutima Kaewkrajay
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Correspondence to Chutima Kaewkrajay.

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Kaewkrajay, C., Dethoup, T. Biocontrol ability of marine yeasts against postharvest diseases in mangos caused by Colletotrichum gloeosporioides and Lasiodiplodia theobromae. Eur J Plant Pathol 168, 709–721 (2024). https://doi.org/10.1007/s10658-023-02795-9

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