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Killer Yeasts as Biocontrol Agents of Postharvest Fungal Diseases in Lemons

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Sustainable Technologies for the Management of Agricultural Wastes

Abstract

One of the main problems affecting the citrus industry worldwide is caused by fungal diseases at postharvest stage. This leads to huge amounts of lemon fruit being unnecessarily discarded which contributed to the overall generation of agricultural wastes. Synthetic fungicides are nowadays the major agents used to control diseases of fungal origin. However, long-term and uncontrolled usage may lead to environmental problems such as growing restrictions that are mainly due to its toxicity. Among biocontrol agents, killer yeasts appear as efficient candidates especially for combating fungal postharvest decay in lemons.

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References

  • Arras G (1996) Mode of action of an isolate of Candida famata in biological control of Penicillium digitatum in orange fruits. Postharvest Biol Technol 8:191–198

    Article  Google Scholar 

  • Arras G, De Cicco V, Arru S, Lima G (1998) Biocontrol by yeasts of blue mould of citrus fruits and the mode of action of an isolate of Pichia guilliermondii. J Hortic Sci Biotechnol 73:413–418

    Article  Google Scholar 

  • Bocco A, Cuvelier MA, Richard H, Berset C (1998) Antioxidant activity and phenolic composition of citrus peel and seed extracts. J Agric Food Chem 46:2123–2129

    Article  CAS  Google Scholar 

  • Boubaker H, Saadi B, Boudyach EH, Ait Benaoumar A (2009) Sensitivity of Penicillium digitatum and Penicillium italicum to imazalil and thiabendazole in Morocco. Plant Pathol J 4:152–158

    Article  Google Scholar 

  • Carbajo MS (2011) Sistemas alternativos a los fungicidas químicos para el control de Penicillium digitatum Sacc. en limón. Trabajo de tesis para optar al grado de Magíster en Producción Vegetal, Universidad de Buenos Aires, Argentina, p 124

    Google Scholar 

  • Chanchaichaovivat A, Ruenwongsa P, Panijpan B (2007) Screening and identification of yeast strains from fruits and vegetables: potential for biological control of postharvest chilli anthracnose (Colletotrichum capsici). Biol Control 42:326–335

    Article  Google Scholar 

  • Cocco M (2005) Determinación de resistencia a fungicidas tradicionales en cepas de Penicillium digitatum y Penicillium italicum en distintas quintas y empaques de la región. Actas del II Seminario Internacional de Postcosecha de Cítricos. Ediciones INTA, pp 104–107

    Google Scholar 

  • Coelho AR, Celli MG, Ono EYS, Wosiacki G (2007) Penicillium expansum versus antagonist yeasts with perspectives of application in biocontrol and patulin degradation. Braz Arch Biol Technol 50:725–733

    Article  Google Scholar 

  • Droby S, Porat R, Cohen L, Weiss B, Shapiro B, Philosoph-Hadas S, Meir S (1999) Suppressing green mold decay in grapefruit with postharvest jasmonate application. J Am Soc Hortic Sci 124:184–188

    CAS  Google Scholar 

  • Droby S, Vinokur V, Weiss B, Cohen L, Daus A, Goldschmidt E, Porat R (2002) Induction of resistance to Penicillium digitatum in grapefruit by the yeast biocontrol agent Candida oleophila. Phytopathology 92:393–399

    Article  CAS  Google Scholar 

  • Droby S, Wisniewski M, Macarisin D, Wilson C (2009) Twenty years of postharvest biocontrol research: is it time for a new paradigm? Postharvest Biol Technol 52:137–145

    Article  Google Scholar 

  • Druvefors UÄ (2004) Yeast biocontrol of grain spoilage moulds – mode of action of Pichia anomala. Doctor’s dissertation ISSN 1401-6249, IBSN 91-576-6493-5. Retrieved January 11, 2011, from Epsilon dissertations and graduate. Theses archive web site: http://diss-epsilon.slu.se:8080/archive/00000552/01/U%C3%84Dfin0.pdf

  • Eckert JW, Ratnayake M, Gutter Y (1984) Volatiles from wounded citrus fruits stimulate germination of Penicillium digitatum conidia. Phytopathology 74:793

    Google Scholar 

  • El-Ghaouth A, Smilanick JL, Wilson CL (2000) Enhancement of the performance of Candida saitoana by the addition of glycochitosan for control of postharvest decay of apple and citrus fruit. Postharvest Biol Technol 19:249–253

    Article  Google Scholar 

  • El-Tarabily KA, Sivasithamparam K (2006) Potential of yeasts as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Mycoscience 47:25–35

    Article  Google Scholar 

  • Fan Q, Tian SP (2000) Postharvest biological control of Rhizopus rot of nectarine fruits by Pichia membranefaciens. Plant Dis 84:1212–1216

    Article  Google Scholar 

  • Ferraz LP, da Cunha T, da Silva AC, Kupper KC (2016) Biocontrol ability and putative mode of action of yeasts against Geotrichum citri-aurantii in citrus fruit. Microbiol Res 188:72–79

    Article  Google Scholar 

  • Garrán SM (1996) Enfermedades durante la postcosecha. Manual para productores de naranjas y mandarinas de la región del río Uruguay. INTA 12:173–240

    Google Scholar 

  • Giobbe S, Marceddu S, Scherm B, Zara G, Mazzarello VL, Budroni M, Migheli Q (2007) The strange case of a biofilm-forming strain of Pichia fermentans, which controls Monilinia brown rot on apple but is pathogenic on peach fruit. FEMS Yeast Res 7(8):1389–1398

    Article  CAS  Google Scholar 

  • Golubev W, Shabalin Y (1994) Mycocin production by the yeast Cryptococcus humicola. FEMS Microbiol Lett 119:105–110

    Article  CAS  Google Scholar 

  • Grevesse C, Lepoivre F, Jijakli MH (2003) Characterization of the exoglucanase-encoding gene aEXG2 and study of its role in the biocontrol activity of Pichia anomala strain K. Phytopathology 93:1145–1152

    Article  CAS  Google Scholar 

  • Harvey JM (1978) Reduction of losses in fresh market fruits and vegetables. Annu Rev Phytopathol 16:321–341

    Article  Google Scholar 

  • Hashem M, Alamri S (2009) The biocontrol of postharvest disease (Botryodiplodia theobromae) of guava (Psidium guajava L.) by the application of yeast strains. Postharvest Biol Technol 53:123–130

    Article  Google Scholar 

  • Hernández-Montiel LG, Ochoa JL, Troyo-Diéguez E, Larralde-Corona CP (2010) Biocontrol of postharvest blue mold (Penicillium italicum Wehmer) on Mexican lime by marine and citrus Debaryomyces hansenii isolates. Postharvest Biol Technol 56(2):181–187

    Article  Google Scholar 

  • Izgu DA, Kepekci RA, Izgu F (2011) Inhibition of Penicillium digitatum and Penicillium italicum in vitro and in planta with Panomycocin, a novel exo-β-1,3-glucanase isolated from Pichia anomala NCYC 434. Antonie Van Leeuwenhoek 99:85–91

    Article  CAS  Google Scholar 

  • Jamalizadeh M, Etebarian HR, Aminian H, Alizadeh A (2011) A review of mechanisms of action of biological control organisms against postharvest fruit spoilage. Bull OEPP/EPPO 41:65–71

    Article  Google Scholar 

  • Janisiewicz WJ, Korsten L (2002) Biological control of postharvest diseases of fruits. Annu Rev Phytopathol 40:411–441

    Article  CAS  Google Scholar 

  • Janisiewicz WJ, Saftner RA, Conway WS, Yoder KS (2008) Control of blue mold decay of apple during commercial controlled atmosphere storage with yeast antagonists and sodium bicarbonate. Postharvest Biol Technol 49:374–378

    Article  CAS  Google Scholar 

  • Katz H, Berkovitz A, Chalutz E, Droby S, Hofstein R, Karen-Tzoor M (1995) Compatibility of ecogens biofungicide aspire, a yeast based preparation, with other fungicides commonly used for the control of postharvest decay of citrus. Phytopathology 85:1123

    Google Scholar 

  • Kefialewa Y, Ayalewb A (2008) Postharvest biological control of anthracnose (Colletotrichum gloeosporioides) on mango (Mangifera indica). Postharvest Biol Technol 50:8–10

    Article  Google Scholar 

  • Kelman A (1989) Introduction: the importance of research on the control of postharvest diseases of perishable food crops. Phytopathology 79:1374

    Google Scholar 

  • Liu S, Tsao M (2009) Inhibition of spoilage yeasts in cheese by killer yeast Williopsis saturnus var. saturnus. Int J Food Microbiol 131:280–282

    Article  CAS  Google Scholar 

  • Liu X, Fang W, Liu L, Yu T, Lou B, Zheng X (2010) Biological control of postharvest sour rot of citrus by two antagonistic yeasts. Lett Appl Microbiol 51:30–35

    CAS  Google Scholar 

  • Long CA, Wu Z, Deng BX (2005) Biological control of Penicillium italicum of citrus and Botrytis cinerea of grape by strain 34–9 of Kloeckera apiculata. Eur Food Res Technol 221(1–2):197–201

    Article  CAS  Google Scholar 

  • Long CA, Deng BX, Deng XX (2006) Pilot testing of Kloeckera apiculata for the biological control of postharvest diseases of citrus. Ann Microbiol 56:13–17

    Article  Google Scholar 

  • López-García B, Veyrat A, Pérez-Payá E (2003) Comparison of the activity of antifungal hexapeptides and the fungicides thiabendazole and imazalil against postharvest fungal pathogens. Int J Food Microbiol 89:163–170

    Article  Google Scholar 

  • Lowes K, Shearman C, Payne J, Mackenzie D, Archer D, Merry R, Gasson M (2000) Prevention of yeast spoilage in feed and food by the yeast mycocin HMK. Appl Environ Microbiol 66:1066–1076

    Article  CAS  Google Scholar 

  • Luo Y, Zeng K, Ming J (2012) Control of blue and green mold decay of citrus fruit by Pichia membranefaciens and induction of defense responses. Sci Hortic (Amsterdam) 135:120–127

    Article  CAS  Google Scholar 

  • Magliani W, Conti S, Travassos LR, Polonelli L (2008) From yeast killer toxins to antibodies and beyond. FEMS Microbiol Lett 288:1–8

    Article  CAS  Google Scholar 

  • Makovitzki A, Viterbo A, Brotman Y, Chet I, Shai Y (2007) Inhibition of fungal and bacterial plant pathogens in vitro and in planta with ultrashort cationic lipopeptides. Appl Environ Microbiol 73(20):6629–6636

    Article  CAS  Google Scholar 

  • Makower M, Bevan EA (1963) The inheritance of the killer character in yeast (Saccharomyces cerevisiae). In: Proceedings of the 11th International Congress on Genetics, vol I. Pergamon Press, Oxford, pp 202–203

    Google Scholar 

  • Marquina D, Santos A, Peinado JM (2002) Biology of killer yeasts. Int Microbiol 5:65–71

    Article  CAS  Google Scholar 

  • McGuire RG (2000) Population dynamics of postharvest decay antagonists growing epiphytically and within wounds on grapefruit. Phytopathology 90:1217–1223

    Article  CAS  Google Scholar 

  • McGuire R, Hagenmaier R (1995) Storage waxes that support growth of Candida oleophila for biocontrol of Penicillium digitatum on citrus. Phytopathology 85:1166

    Google Scholar 

  • Meier GE (2005) Sales de sodio como alternativas a los fungicidas tradicionales para el control de moho verde y moho azul. Actas del II Seminario Internacional de Postcosecha de Cítricos. Vázquez DE, Meier GE, Cocco M. Ediciones INTA, pp 108–110

    Google Scholar 

  • Mercier I, Smilanick JL (2005) Control of green mold and sour rot of stored lemon by biofumigation with Muscodor albus. Biol Control 32:401–407

    Article  Google Scholar 

  • Muller I (2005) Investigaciones en poscosecha en INIA Salto Grande. Evaluación de nuevos fungicidas. Actas del II Seminario Internacional de Postcosecha de Cítricos. Ediciones INTA, Argentina, pp 84–88

    Google Scholar 

  • Palou L (2007) Evaluación de alternativas para el tratamiento antifúngico en poscosecha de cítricos de Producción Integrada. Rev Hortic 82:93

    Google Scholar 

  • Palou L, Smilanick JL, Droby S (2008) Alternatives to conventional fungicides for the control of citrus postharvest green and blue molds. Stewart Postharvest Rev 4:1–16

    Google Scholar 

  • Perez MF, Contreras L, Garnica NM, Fernández-Zenoff MV, Farías ME, Sepulveda M, Dib JR (2016) Native killer yeasts as biocontrol agents of postharvest fungal diseases in lemons. PLoS One 11(10):e0165590

    Article  Google Scholar 

  • Perez MF, Perez Ibarreche J, Isas AS, Sepulveda M, Ramallo J, Dib JR (2017) Antagonistic yeasts for the biological control of Penicillium digitatum on lemons stored under export conditions. Biol Control 115:135–140

    Google Scholar 

  • Platania C, Restuccia C, Muccilli S, Cirvilleri G (2012) Efficacy of killer yeasts in the biological control of Penicillium digitatum on Tarocco orange fruits (Citrus sinensis). Food Microbiol 30:219–225

    Article  Google Scholar 

  • Ragone ME (1999) Niveles de contaminación fúngica en galpones de empaque de exportación de frutas cítricas de la región de Concordia. Trabajo final de Graduación. Facultad de Ciencias Agrarias. Universidad Nacional del Nordeste. Corrientes, Argentina

    Google Scholar 

  • Ren X, Kong Q, Wang H, Yu T, Zhou W, Zheng X (2011) Biocontrol of fungal decay of citrus fruit by Pichia pastoris recombinant strains expressing cecropin A. Food Chem 131:796–801

    Article  Google Scholar 

  • Rosa MM, Tauk-Tornisielo SM, Rampazzo PE, Ceccato-Antonini SR (2010) Evaluation of the biological control by the yeast Torulaspora globosa against Colletotrichum sublineolum in sorghum. World J Microbiol Biotechnol 26:1491–1502

    Article  Google Scholar 

  • Sánchez-Torres P, Tuset JJ (2011) Molecular insights into fungicide resistance in sensitive and resistant Penicillium digitatum strains infecting citrus. Postharvest Biol Technol 59:159–165

    Article  Google Scholar 

  • Sharma R, Singh D, Singh R (2009) Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: a review. Biol Control 50:205–221

    Article  Google Scholar 

  • Smilanick JL, Mansour MF, Gabler FM, Sorenson D (2008) Control of citrus postharvest green mold and sour rot by potassium sorbate combined with heat and fungicides. Postharvest Biol Technol 47(2):226–223

    Article  CAS  Google Scholar 

  • Sulo P, Michalcakova S (1992) The K3 type killer strains of genus Saccharomyces for wine production. Folia Microbiol 37:289–294

    Article  CAS  Google Scholar 

  • Sulo P, Michalcakova S, Reiser V (1992) Construction and properties of K1 type killer wine yeasts. Biotechnol Lett 14:55–60

    Article  Google Scholar 

  • Suprapta DN, Arai K, Iwai H (1997) Effects of volatile compounds on arthrospore germination and mycelial growth of Geotrichum candidum citrus race. Mycoscience 38:31–35

    Article  CAS  Google Scholar 

  • Talibi I, Boubaker H, Boudyach EH, Ait Ben Aoumar A (2014) Alternative methods for the control of postharvest citrus diseases. J Appl Microbiol 117(1):1–17

    Article  CAS  Google Scholar 

  • Taqarort N, Echairi A, Chaussod R, Nouaim R, Boubaker H, Benaoumar AA, Boudyach E (2008) Screening and identification of epiphytic yeasts with potential for biological control of green mold of citrus fruits. World J Microbiol Biotechnol 24:3031–3038

    Article  Google Scholar 

  • Torres Leal GJ, Velázquez PD, Paz AE, Farías MF (2008) Control of Penicillium digitatum (Green mold) by sodium bicarbonate in lemon fruit in Tucuman (Argentina). In: Proceedings of the international society of citriculture, XI Congress, Wuhan, China, p 1369

    Google Scholar 

  • Tripathi P, Dubey N (2003) Exploitation of natural products as an alternative strategy to control postharvest fungal rotting of fruit and vegetables. Postharvest Biol Technol 32:235–245

    Article  Google Scholar 

  • Tuset JA (1987) Podredumbres de los frutos cítricos. Generalitat Valenciana, Valencia, p 206

    Google Scholar 

  • Utama IMS, Wills RB, Ben-yehoshua S, Kuek C (2002) In vitro efficacy of plant volatiles for inhibiting the growth of fruit and vegetable decay microorganisms. J Agric Food Chem 50(22):6371–6377

    Article  CAS  Google Scholar 

  • Vázquez DE, Ragone M, Garrán S (1995) Factores que afectan la calidad de los frutos cítricos. Informe técnico de la Estación Experimental Agropecuaria Concordia del INTA, p 14

    Google Scholar 

  • Velázquez PD, Farías MF, Carbajo MS, Torres Leal GJ (2010) Eficacia de los fungicidas azoxistrobin fluodioxinil en el control curativo de “moho verde” causado por Penicillium digitatum en frutos de limón. Libro de Resúmenes XXXIII Congreso Argentino de Horticultura, Rosario, p 142

    Google Scholar 

  • Viñas I (1990) Principios básicos de la patología de poscosecha. FRUT 5:285–292

    Google Scholar 

  • Wang YF, Bao YH, Shen DH, Feng W (2008) Biocontrol of Alternaria alternata on cherry tomato fruit by use of marine yeast Rhodosporidium paludigenum Fell & Tallman. Int J Food Microbiol 123:234–239

    Article  Google Scholar 

  • Wilson CL, Chalutz E (1989) Postharvest biological control of Penicillium rots with antagonistic yeasts and bacteria. Sci Hortic 40:105–112

    Article  Google Scholar 

  • Wisnieswski ME, Biles C, Droby S, McLaughlin R, Wilson C, Chalutz E (1991) Mode of action of the postharvest biocontrol yeast, Pichia guilliermondii. Characterization of attachment to Botrytis cinerea. Physiol Mol Plant Pathol 39:245–258

    Article  Google Scholar 

  • Wisnieswski M, Wilson C, Droby S, Chalutz E, ElGhaouth A, Stevens C (2007) Postharvest biocontrol: new concepts and applications. In: biological control: a global perspective. CAB International, Wallingford, pp 262–273

    Google Scholar 

  • Yao HJ, Tian SP (2005) Effects of a biocontrol agent and methyl jasmonate on postharvest diseases of peach fruit and the possible mechanisms involved. J Appl Microbiol 98:941–950

    Article  CAS  Google Scholar 

  • Zhang HY, Zheng XD, Xi YF (2005) Biological control of postharvest blue mold of oranges by Cryptococcus laurentii (Kufferath) Skinner. BioControl 50(2):331–342

    Article  Google Scholar 

  • Zhang D, Spadaro D, Garibaldi A, Gullino ML (2010) Selection and evaluation of new antagonists for their efficacy against postharvest brown rot of peaches. Postharvest Biol Technol 55:174–181

    Article  CAS  Google Scholar 

  • Zheng XD, Zhang HY, Sun P (2005) Biological control of postharvest green mold decay of oranges by Rhodotorula glutinis. Eur Food Res Technol 220:353–357

    Article  CAS  Google Scholar 

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Perez, M.F., Isas, A.S., Aladdin, A., El Enshasy, H.A., Dib, J.R. (2018). Killer Yeasts as Biocontrol Agents of Postharvest Fungal Diseases in Lemons. In: Zakaria, Z. (eds) Sustainable Technologies for the Management of Agricultural Wastes. Applied Environmental Science and Engineering for a Sustainable Future. Springer, Singapore. https://doi.org/10.1007/978-981-10-5062-6_7

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