Biodiversity and biocontrol activity of grape epiphyte yeasts in control of gray mold disease

Document Type : Research Paper

Authors

1 1. Assistant Professor, Plant Protection Research Department, West Azarbaijan Agricultural and Natural Resources Research Center, AREEO, Urmia, Iran.

2 Associate Professor, Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran.

3 Associate professor, Department of Agriculture, Medicinal Plants and Drugs Research Institute, Shahid Beheshti University, Evin, Tehran, Iran.

10.22092/bcpp.2024.365188.362

Abstract

Grape gray decay disease caused by Botrytis cinerea is one of the important factors causing rotting and reducing the quantity and quality of the grapes during the stages before and after harvesting, which makes the use of chemical fungicides inevitable. Considering the environmental issues with the excessive use of chemical fungicides for humans and the environment, the use of products based on biological agents has received special attention. Among biological agents, some yeasts have been shown to possess antagonistic activity against fungi and are considered as safe and sound alternatives for chemical pesticides. The present study aimed to identify grape epiphytic yeasts and investigate their ability against the pathogenic fungus B. cinerea in the post–harvest stage. A total of 67 yeast isolates were isolated from the surface of grape fruits in the vineyards of West Azarbaijan province. Based on morphological studies and nucleotide sequence analysis of the D1/D2 domain of the large subunit 26S rDNA gene, the isolates belong to 21 species and 11 genera. Aureobasidium pullulans was recognized as the dominant species of grape flora. The ability of 67 yeast isolates to control B. cinerea growth by the dual–culture method showed that 16 isolates belonging to 7 genera succeeded in inhibiting the growth of the gray mold, which isolates Rhodotorula glutinis G54 and Metschnikowia pulcherrima G9 showed the greatest of capability against B. cinerea. A significant difference (P≤0.01) was observed between the 16 selected isolates in terms of inhibition of gray rot on grape berries, as a completely randomized design with four replications. The isolates Meyerozyma guilliermondii G30, Rh. glutinis G54 and M. pulcherrima G9 were the most effective isolates in reducing the disease on grape berries with 92.59, 91.37 and 90.15 percent rot inhibition, respectively. Studies of mechanisms involved in biological control showed that 12 isolates were able to produce protease, 6 isolates were able to produce pectinase and 12 isolates produced amylase. Also, it was found that 9 isolates can form biofilm and 8 isolates produced a siderophore. Finally, it was found that the grape flora has a high diversity of yeasts and the superior yeast isolates including G30, G54 and G9, with various biocontrol mechanisms (such as antibiosis, protease and amylase activities as well as siderophore production), have a high potential to inhibit the gray rot of grape. However, it is necessary to conduct more studies on selected isolates to creat practical formulations for biological control or integrated management of fungal diseases of fruits and vegetables.
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Keywords

Main Subjects

References

Banani, H., Spadaro, D., Zhang, D., Matic, S., Garibaldi, A. & Gullino, M.L. 2014. Biocontrol activity of an alkaline serine protease from Aureobasidium pullulans expressed in Pichia pastoris against four postharvest pathogens on apple. International Journal of Food Microbiology, 182– 183:1–8.
Baakza, A., Vala, A.K., Dave, B.P. & Dube, H.C. 2004. A comparative study of siderophore production by fungi from marine and terrestrial habitats. Journal of Experimental Marine Biology and Ecology, 311: 1–9.
Contarino, R., Brighina, S., Fallico, B., Cirvilleri, G., Parafati, L. & Restuccia, C. 2019. Volatile organic compounds (VOCs) produced by biocontrol yeasts. Food Microbiology, 82: 70–74
Di Canito, A., Mateo–vargas, M.A., Mazzieri, M., Cantoral, J., Foschino, R. & Cordero–Bueso, G. 2021. The role of yeasts as biocontrol agents for pathogenic fungi on postharvest grapes: a review. Foods, 10: 1–15.
Di Francesco, A., Di Foggia, M., Corbetta, M., Baldo, D., Ratti, C. & Baraldi, E. 2021. Biocontrol activity and plant growth promotion exerted by Aureobasidium pullulans strains. Journal of Plant Growth Regulation, 40, 1233–1244.
Di Francesco, A., Martini, C., Mari, M. 2016. Biological control of postharvest diseases by microbial antagonists: How many mechanisms of action? European Journal of Plant Pathology, 145: 711–717.
Droby, S., Lschinski, S., Cohen, L., Daus, A., Chand–Goyal, T., Eckert, J.W. & Manulis, S. 1999. Characterization of an epiphytic yeast population of grapefruit capable of suppression of green mold decay caused by Penicillium digitatum. Biological Control, 16: 27–34.
Nadia, G., Sherien, M.M., Atalla, El–mougy, N.S. & Abdel–Kader, M.M. 2018. Production of pectinase by Saccharomyces cerevisiae and its application as biocontrol agent against navel orange and apple fruits decay. Bioscience Research, 2218–3973.
Etebarian, H.R., Sholberg, P.L., Eastwell, K.C. & Sayler, R.J. 2005.Biological control of apple blue mold with Pseudomonas fluorescens. Microbiology, 51: 591–598.
Elshafie, H.S., Caputo, L., De Martino, L., Grul’ová, D., Zheljazkov, V.Z., De Feo, V. & Camele, I. 2020. Biological investigations of essential oils extracted from three Juniperus species and evaluation of their antimicrobial, antioxidant and cytotoxic activities. Journal of Appl.ied Microbiology, 129: 1261–1271.
Esteves, M., Lage P., Sousa, J., Centeno, F., Teixeira, M.F., Tenreiro, R. & Mendes–Ferreira, A. .2023 Biocontrol of wine yeasts against four grape phytopathogenic fungi disclosed by time–course monitoring of inhibitory activates. Frontiers in Microbiology, 14: 1146065.
Fialho, M.B., Toffano, L., Pedroso, M.P., Augusto, F. & Pascholati S.F. 2010. Volatile organic compounds produced by Saccharomyces cerevisiae inhibit the in vitro development of Guignardia citricarpa, the causal agent of citrus black spot. World Journal of Microbiology and Biotechnoogy, 26: 925–932.
Gattlen, J., Zinn, M., Guimond, S., Körner, E., Amberg, C. & Mauclaire, L. 2011. Bioflm formation by the yeast Rhodotorula mucilaginosa: process, repeatability and cell attachment in a continuous bioflm reactor. Biofouling, 27: 979–991.
Giobbe, S., Marceddu, S., Scherm, B., Zara, G., Mazzarello, V.L, Budroni, M. & Migheli, Q. 2007. The strange case of a bioflm–forming strain of Pichia fermentans, which controls Monilinia brown rot on apple but is pathogenic on peach fruit. FEMS Yeast Reserch, 7: 1389–1398.
Grzegorczyk, M., Szalewicz, A., Żarowska, B., Połomska, X., Wątorek, W., Wojtatowicz, M. & Drobnoustroje, w. 2015. biologicznej ochronie roślin przed chorobami grzybowymi. Acta Scientific Biotechnology, 14: 19–42.
Huang, R., Li, G.Q., Zhang, J., Yang, L., Che, H.J., Jiang, D.H. & Huang, H.C. 2011. Control of postharvest Botrytis fruit rot of strawberry by volatile organic compounds of Candida intermedia. Phytopathology, 101: 859–869.
Horváth, E., Dályai, L., Szabó, E., Barna, T., Kalmár, L., Posta, J., Sipiczki, M., Csoma, H. & Ida Miklós1. 2021. The antagonistic Metschnikowia andauensis produces extracellular enzymes and pulcherrimin, whose production can be promoted by the culture factors. Natire Profilo, 11: 10593.
Kowalska, J., Krzymińska, J. & Tyburski, J. 2022. Yeasts as a potential biological agent in plant disease protection and yield improvement – A short review. Agriculture, 12(9): 1404.
Kwasiborski, A., Bajji, M., Renaut, J., Delaplace, P. & Jijakli, M.H.  2014. Dentification of metabolic pathways expressed by Pichia anomala Kh6 in the presence of the pathogen Botrytis cinerea on apple: new possible targets for biocontrol improvement, PLoS ONE 9(3): e91434.
La Spada, F., Aloi, F., Coniglione, M., Pane, A. & Cacciola, S.O. 2021. Natural biostimulants elicit plant immune system in an integrated management strategy of the postharvest green mold of orange fruits incited by Penicillium digitatum. Front Plant Science, 12: 1149.
Libkind, D., Brizzio, S., Ruffini, A., Gadanho, M., van Broock, M. & Sampaio, P. 2003. Molecular characterization of carotenogenic yeasts from aquatic environments in Patagonia, Argentina. Antonie van Leeuwenhoek, 84: 313–322.
Liu, J., Sui, Y., Wisniewski, M., Droby, S., Liu, Y. 2013. A review, Utilization of antagonistic yeasts to manage postharvest fungal disease control. International Journal of Food Microbiology, 167: 153–160.
Mokhtarnejad, l. 2015. Investigating of biodiversity and phylogeny of yeasts in the soils of Lake Urmia and the biological control of grape cluster diseases using species of the genus Pichia. pp. 187
Moraes Bazioli, J.M., Belinato, J.R., Costa, J.H., Akiyama, D.Y., de Pontes, J.G.M., Kupper, K.C., Augusto, F., de Carvalho, J.E. & Fill, T.P. 2019. Biological control of citrus postharvest phytopathogens. Toxins, 11: 460.
Nally, M.C. Pesce, V.M. Maturano, Y.P. Muñoz, C.J. Combina, M. Toro, M.E. de Figueroa, L.C. & Vazquez, F. 2012. Biocontrol of Botrytis cinerea in table grapes by non–pathogenic indigenous Saccharomyces cerevisiae yeasts isolated from viticultural environments in Argentina. Postharvest Biology and Technology, 64: 40–48.
Nally, M., Pesce, V., Maturano, Y., Assaf, L.R., Toro, M., de Figueroa, L.C. & Vazquez, F. 2015. Antifungal modes of action of Saccharomyces and other biocontrol yeasts against fungi isolated from sour and grey rots. International Journal of Food Microbiology, 204: 91–100.
Palmieri, D., Ianiri, G., Del Grosso, C., Barone, G., De Curtis, F. & Castoria, R. 2022 Advances and perspectives in the use of biocontrol agents against fungal plant diseases. Horticulturae, 8: 577.
Parafati, L., Vitale, A., Restuccia, 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.
Parafati, L., Vitale, A., Restuccia, 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.
Pereyra, M.M., Díaz, M.A., Soliz–Santander, F.F., Poehlein, A., Meinhardt, F. & Daniel, R. 2021. Screening methods for isolation of biocontrol Epiphytic yeasts against Penicillium digitatum in lemons. Journal of Fungi, 7: 166.
Pertot, I., Giovannini, O., Benanchi, M., Caffi, T., Rossi, V. & Mugnai, L. 2017. Combining biocontrol agents with different mechanisms of action in a strategy to control Botrytis cinerea on grapevine. Crop Protection, 97: 85–93.
Pretscher, J., Fischkal, T., Branscheidt, S., Jäger, L., Kahl, S. & Schlander, M. 2018. Yeasts from different habitats and their potential as biocontrol agents. Fermentation, 4–31.
Pretorius, I.S., Van Der Westhuizen, T.J. & Augustyn, O.P.H. 1999. Yeast biodiversity in vineyards and wineries and it’s importance to the South–African wine industry. A review. South African Journal of Enology and Viticulture, 20: 61–69.
Punja, Z.K. & Utkhede, R.S. 2003. Using fungi and yeasts to manage vegetable crop diseases. Trends Biotechnology, 21: 400–407.
Pusey, P.L., Stockwell, V.O. & Mazzola, M. 2009. Epiphytic bacteria and yeasts on apple blossoms and their potential as antagonists of Erwinia amylovora. Phytopathology, 99: 571–581.
Podgórska–Kryszczuk, I., Solarska E. & Kordowska–Wiater, M. 2022. Biological Control of Fusarium culmorum, Fusarium graminearum and Fusarium poae by Antagonistic Yeasts. Pathogens, 11: 86: 1–16.
Rabosto, X., Carrau, M., Paz, A., Boido, E., Dellacassa, E. & Carrau, F.M. 2006. Grapes and Vineyard Soils as Sources of Microorganisms for Biological Control of Botrytis cinerea. American Journal of Enology and Viticulture, 57: 332–338.
Reyes–bravo, P., Acuña–fontecilla, A., Rosales, I.M.I. M. & Godoy, L. 2019. Evaluation of native wine yeast as biocontrol agents against fungal pathogens related to postharvest diseases. Journal of Agronomy & Agricultural Science.
Ruzicka, F., Hola, V., Votava, M. & Tekkalov_a, R. 2007. Importance of biofilm in Candida parapsilosis and evaluation of its susceptibility to antifungal agents by colorimetric method. Folia Microbiol, 52: 209–214.
Schwyn, B. & Neilands, J.B. 1987. Universal chemical assay for the detection and determination of siderophores. Annual Biochemistry, 60: 47–56.
Sànchez–Torres, P. & Tuset, J.J. 2011. Molecular insights into fungicide resistance in sensitive and resistant Penicillium digitatum strains infecting citrus. Postharvest Biology and Technology, 59: 159–165.
Sansone, G., Rezza, I., Calvente, V., Benuzzi, D. & de Tosetti, M.I.S. 2005. Control of Botrytis cinerea strains resistant to iprodione in apple with rhodotorulic acid and yeasts. Postharvest Biology and Technology, 35: 245–251.
Saravanakumar, D., Ciavorella, A., Spadaro, D., Garibaldi, A. & Gullino, M.L. 2008. Metschnikowia pulcherrima strain MACH1 outcompetes Botrytis cinerea, Alternaria alternata and Penicillium expansum in apples through iron depletion. Postharvest Biology and Technology, 49: 121–128.
Savary, S., Ficke, A., Aubertot, J.N. & Hollier, C. 2012. Crop losses due to diseases and their implications for global food production losses and food security. Food Security, 4(4): 519–537.
Sanzani, S.M., De Girolamo, A., Schena, L., Solfrizzo, M., Ippolito, A. & Visconti, A. 2009. Control of Penicillium expansum and patulin accumulation on apples by quercetin and umbelliferone. European Food Research Technology, 228: 381–389.
Sharma, R.R. Singh, D. & Singh, R. 2009. Biological control of postharvest diseases of fruits and vegetables by microbial antagonists. Biological Control, 50: 205–221.
Sipiczki, M. 2006. Metschnikowia strains isolated from botrytized grapes antagonize fungal and bacterial growth by iron depletion. Applied and Environmental Microbiology, 72: 6716–6724.
Spadaro, D. & Droby, S. 2016. Development of biocontrol products for postharvest diseases of fruit: the importance of elucidating the mechanisms of action of yeast antagonists. Trends Food Science and Technology, 47: 39–49.
Strauss, M.L.A., Jolly, N.P., Lambrechts, M.G. & Van Rensburg, P. 2001. Screening for the production of extracellular hydrolytic enzymes by non–saccharomyces wine yeasts. Journal of Applied Microbiology, 91: 182–190.
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S. & MEG, A. 2011.  Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molcular Biology and Evolution, 28: 2731–2739.
Tian, Y.Q., Li, W., Jiang, Z.T., Jing, M.M. & Shao, Y.Z. 2018. The preservation effect of Metschnikowia pulcherrima yeast on anthracnose of postharvest mango fruits and the possible mechanism. Food Science and Biotechnology, 27: 95–105.
Usall, J., Ippolito, A., Sisquella, M. & Neri, F. 2016. Physical treatments to control postharvest diseases of fresh fruits and vegetables. Postharvest Biology and Technology, 122: 30–40.
Vargas, M., Garrido, F., Zapata, N. & Tapia, M. 2012. Isolation and Selection of Epiphytic Yeat for Biocontrol of Botrytis cinerea Pers. on Table Grapes. Chil. Journal of Agriculture Research, 72: 332–337.
Vero, S., Mondino, P., Burgueño, J., Soubes, M. & Wisniewski, M. 2002. Characterization of biocontrol activity of two yeast strains from Uruguay against blue mold of apple. Postharvest Biology and Technology, 26: 91–98.
Wallace, R.L., Hirkala, D.L. & Nelson, L.M. 2018. Mechanisms of action of three isolates of Pseudomonas fluorescens active against postharvest grey mold decay of apple during commercial storage. Biological Control, 117: 13–20.
Wang, W., Chi, Z., Li, J. & Wang, X. 2009. Siderophore production by the marine–derived Aureobasidium pullulans and its antimicrobial activity. Bioresource Technology, 100: 2639–2641.
Wilson, C.L. & Wisniewski, M. 1989. Biological control of post harvest diseases offruit and vegetables: an emerging technology. Annual Review of Phytopathology, 27: 425–441.
Yang, H., Wang, L., Li, S., Gao, X., Wu, N., Zhao, Y. & Sun, W. 2021. Control of postharvest grey spot rot of loquat fruit with Metschnikowia pulcherrima E1 and potential mechanisms of action. Biological Control, 152: 104406
Zajc, J., Černoša, A., Di Francesco, A., Castoria, R., De Curtis, F., Lima, G., Badri, H., Jijakli, H., Ippolito, A., Čar, C.G., Zalar, P., Cimerman N.G. & Janisiewicz W.J. 2020. Characterization of Aureobasidium pul[1]lulans isolates selected as biocontrol agents against fruit decay pathogens. Fungal Genetics and Biology, 10:1–13.
Zhang, H., Godana, E. A., Sui, Y., Yang, Q., Zhang, X. & Zhao, L. 2020. Biological control as an alternative to synthetic fungicides for the management of grey and blue mould diseases of table grapes: a review. Critical Review in Microbiology, 46: 450–462.
Zhang, D., Spadaro, D., Valente, S., Garibaldi, A. & Gullino, M.L. 2012. Cloning, characterization, expression and antifungal activity of an alkaline serine protease of Aureobasidium pullulans PL5 involved in the biological control of postharvest pathogens. International Journal of Food Microbiology, 153: 453–464.
Zhou, Y., Li, W., Zeng, J. & Shao, Y. 2018. Mechanisms of action of the yeast Debaryomyces nepalensis for control of the pathogen Colletotrichum gloeosporioides in mango fruit. Biological Control, 123: 111–119.
 
 
BioControl in Plant Protection
Volume 11, Issue 1
August 2023
Pages 63-81

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