Search for Author, Title, Keyword
ORIGINAL ARTICLE
Control of Mould Spoilage on Apples Using Yeasts as Biological Control Agents
 
More details
Hide details
1
Post-Harvest and Agro-Processing Technologies Division, ARC Infruitec-Nietvoorbij, South Africa
 
2
Department of Agriculture, Cape Peninsula University of Technology, Wellington, South Africa
 
3
Bioresource Engineering Research Group (BioERG), Department of Biotechnology, Cape Peninsula University of Technology, Cape Town, South Africa
 
4
Biometry, ARC Infruitec-Nietvoorbij, South Africa
 
5
Crop Development Division, ARC Infruitec-Nietvoorbij, South Africa
 
 
Submission date: 2021-12-15
 
 
Final revision date: 2022-03-31
 
 
Acceptance date: 2022-04-01
 
 
Online publication date: 2022-05-31
 
 
Publication date: 2022-05-31
 
 
Corresponding author
Heinrich W. du Plessis   

Post-Harvest and Agro-Processing Technologies, ARC Infruitec-Nietvoorbij, Stellenbosch, South Africa
 
 
Pol. J. Food Nutr. Sci. 2022;72(2):119-128
 
KEYWORDS
TOPICS
ABSTRACT
Considerable quantities of fruit are lost during pre- and post-harvest stages due to mould spoilage. The aim of this study was to evaluate the antagonistic effect of selected yeasts against spoilage mould Botrytis cinerea, Penicillium expansum and Alternaria alstroemeriae. One hundred and four yeast isolates were screened for antagonistic activity against B. cinerea, P. expansum and A. alstroemeriae using radial inhibition, dual and mouth-to-mouth plate assays. Sixty-seven out of 104 yeasts showed growth inhibition activity against P. expansum, while 36 yeasts inhibited B. cinerea, 47 yeasts inhibited A. alstroemeriae, but only 22 yeasts showed inhibition activity against all three moulds. Candida pyralidae Y63, Meyerozyma guilliermondii Y88 and Zygoascus hellenicus Y89 showed highest inhibition activity against all three moulds, when mode of inhibition was due to direct contact. Volatile organic compounds produced by Pichia kluyveri Y64, C. pyralidae Y63 and M. guilliermondii Y88 showed the highest growth inhibition against all three moulds. These yeasts were also evaluated against all three moulds on apples. P. kluyveri Y64 showed 100%, 57% and 26% growth inhibition against A. alstroemeriae, B. cinerea and P. expansum, respectively, on apples and performed slightly better than a commercial fungicide against B. cinerea and P. expansum. While M. guillermondii Y88 showed 100%, 60% and 18% inhibition on apples against A. alstroemeriae, B. cinerea and P. expansum, respectively. P. kluyveri Y64 and M. guilliermondii Y88 showed potential as biofungicides and warrant further investigation.
ACKNOWLEDGEMENTS
The authors would like to thank Agricultural Research Council (ARC) and National Research Foundation (NRF) of South Africa for funding and infrastructure. The opinions, findings and conclusions or recommendations expressed in this publication is that of the authors alone, and the NRF accepts no liability whatsoever in this regard. Thank you to Ms Louise Smit for culturing and supplying Botrytis cinerea. The authors extend their gratitude to all students, interns, technicians and research assistants for their individual contributions.
FUNDING
This work was supported by the Agricultural Research Council (ARC) and National Research Foundation (NRF) of South Africa (Grant Numbers: 117833 and 122220).
REFERENCES (39)
1.
Al-Hindi, R.R., Al-Najada, A.R., Mohamed, S.A. (2011). Isolation and identification of some fruit spoilage fungi: Screening of plant cell wall degrading enzymes. African Journal of Microbiology Research, 5(4), 443-448.
 
2.
Al-Maawali, S.S., Al-Sadi, A.M., Ali Khalifa Alsheriqi, S., Nasser Al-Sabahi, J., 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(1), 34-48. https://doi.org/10.1080/268952....
 
3.
Al-Rahbi, B.A.A., Al-Sadi, A.M., Al-Mahmooli, I.H., Al-Maawali, S.S., Al-Mahruqi, N.M.T., Velazhahan, R. (2021). Meyerozyma guilliermondii SQUCC-33Y suppresses postharvest fruit rot of strawberry caused by Alternaria alternata. Australasian Plant Pathology, 50(3), 349-352. https://doi.org/10.1007/s13313....
 
4.
Banjara, N., Nickerson, K.W., Suhr, M.J., Hallen-Adams, H.E. (2016). Killer toxin from several food-derived Debaryomyces hansenii strains effective against pathogenic Candida yeasts. International Journal of Food Microbiology, 222, 23-29. https://doi.org/10.1016/j.ijfo....
 
5.
Benito, S., Palomero, F., Morata, A., Uthurry, C., Suárez-Lepe, J.A. (2009). Minimization of ethylphenol precursors in red wines via the formation of pyranoanthocyanins by selected yeasts. International Journal of Food Microbiology, 132(2-3), 145-152. https://doi.org/10.1016/j.ijfo....
 
6.
Bonaterra, A., Badosa, E., Cabrefiga, J., Francés, J., Montesinos, E. (2012). Prospects and limitations of microbial pesticides for control of bacterial and fungal pomefruit tree diseases. Trees, 26, 215–226. https://doi.org/10.1007/s00468....
 
7.
Chen, P.H., Chen, R.Y., Chou, J.Y. (2018). Screening and evaluation of yeast antagonists for biological control of Botrytis cinerea on strawberry fruits. Mycobiology, 46(1), 33-46. https://doi.org/10.1080/122980....
 
8.
Choińska, R., Piasecka-Jóźwiak, K., Chabłowska, B., Dumka, J., Łukaszewicz, A. (2020). Biocontrol ability and volatile organic compounds production as a putative mode of action of yeast strains isolated from organic grapes and rye grains. Antonie van Leeuwenhoek, 113(8), 1135-1146. https://doi.org/10.1007/s10482....
 
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. https://doi.org/10.1016/j.fm.2....
 
10.
Cordero-Bueso, G., Mangieri, N., Maghradze, D., Foschino, R., Valdetara, F., Cantoral, J.M., Vigentini, I. (2017). Wild grape-associated yeasts as promising biocontrol agents against Vitis vinifera fungal pathogens. Frontiers in Microbiology, 8, art. no. 2025. https://doi.org/10.3389/fmicb.....
 
11.
De Simone, N., Capozzi, V., Amodio, M.L., Colelli, G., Spano, G., Russo, P. (2021). Microbial-based biocontrol solutions for fruits and vegetables: recent insight, patents, and innovative trends. Recent Patents on Food, Nutrition & Agriculture, 12(1), 3-18. https://doi.org/10.2174/221279....
 
12.
Du Plessis, K. (2017). Post-harvest Innovation Programme Innovate flipbook, pp. 82-83 [https://www.postharvestinnovat...] (Accessed: 01 March 2021).
 
13.
Droby, S. (2005). Improving quality and safety of fresh fruits and vegetables after harvest by the use of biocontrol agents and natural materials. I International Symposium on Natural Preservatives in Food Systems, ISHS Acta Horticulturae, 709, 45-52. https://doi.org/10.17660/ActaH....
 
14.
FAOstat. (2020). Food and Agricultural Organisation of the United Nations – Statistical Division. Production – Crops and livestock products [www.faostat.org] (Accessed: 25 March 2022).
 
15.
Fernández-Ortuño, D., Torés, J.A., De Vicente, A., Pérez-García, A. (2008). Mechanisms of resistance to QoI fungicides in phytopathogenic fungi. International Microbiology, 11(1), 1-9.
 
16.
Grevesse, C., Lepoivre, P., Jijakli, M.H. (2003). Characterization of the exoglucanase-encoding gene PaEXG2 and study of its role in the biocontrol activity of Pichia anomala strain K. Phytopathology, 93(9), 1145-1152. https://doi.org/10.1094/PHYTO.....
 
17.
Han, J., Zhao, L., Zhu, H., Dhanasekaran, S., Zhang, X., Zhang, H. (2021). Study on the effect of alginate oligosaccharide combined with Meyerozyma guilliermondii against Penicillium expansum in pears and the possible mechanisms involved. Physiological and Molecular Plant Pathology, 115, art. no. 101654. https://doi.org/10.1016/j.pmpp....
 
18.
Hua, S.S.T., Beck, J.J., Sarreal, S.B.L., Gee, W. (2014). The major volatile compound 2-phenylethanol from the biocontrol yeast, Pichia anomala, inhibits growth and expression of aflatoxin biosynthetic genes of Aspergillus flavus. Mycotoxin Research, 30(2), 71-78. https://doi.org/10.1007/s12550....
 
19.
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(2), 153–160. https://doi.org/10.1016/j.ijfo....
 
20.
Lõoke, M., Kristjuhan, K., Kristjuhan, A. (2011). Extraction of genomic DNA from yeasts for PCR-based applications. BioTechniques, 50(5), 325-328. https://doi.org/10.2144/000113....
 
21.
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. https://doi.org/10.1016/j.bioc....
 
22.
Mercier, J., Lindow, S.E. (2001). Field performance of antagonistic bacteria identified in a novel laboratory assay for biological control of fire blight of pear. Biological Control, 22(1), 66–71. https://doi.org/10.1006/bcon.2....
 
23.
Mewa-Ngongang, M., Du Plessis, H.W., Chidi, B.S., Hutchinson, U.F., Ntwampe, K.S.O., Okudoh, V.I., Jolly, N.P. (2021). Physiological and antagonistic properties of Pichia kluyveri for curative and preventive treatments against post-harvest fruit fungi. Polish Journal of Food and Nutrition Sciences, 71(3), 245-253. https://doi.org/10.31883/pjfns....
 
24.
Mewa-Ngongang, M., du Plessis, H.W., Hlangwani, E., Ntwampe, S.K.O., Chidi, B.S., Hutchinson, U.F., Jolly, N.P. (2019a). Activity interactions of crude biopreservatives against spoilage yeast consortia. Fermentation, 5(3), art. no. 53. https://doi.org/10.3390/fermen....
 
25.
Mewa-Ngongang, M., du Plessis, H.W., Ntwampe, S.K.O., Chidi, B.S., Hutchinson, U.F., Mekuto, L., Jolly, N.P. (2019b). The use of Candida pyralidae and Pichia kluyveri to control spoilage microorganisms of raw fruits used for beverage production. Foods, 8(10), art. no. 454. https://doi.org/10.3390/foods8....
 
26.
Mitchell, T.G., Freedman, E.Z., White, T.J., Taylor, J.W. (1994). Unique oligonucleotide primers in PCR for identification of Cryptococcus neoformans. Journal of Clinical Microbiology, 32(1), 253-255. https://doi.org/10.1128/jcm.32....
 
27.
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(1), 40-48. https://doi.org/10.1016/j.post....
 
28.
Nunes, C.A. (2012). Biological control of postharvest diseases of fruit. European Journal of Plant Pathology, 133(1), 181-196. https://doi.org/10.1007/s10658....
 
29.
Núñez, F., Lara, M.S., Peromingo, B., Delgado, J., Sánchez-Montero, L., Andrade, M.J. (2015). Selection and evaluation of Debaryomyces hansenii isolates as potential bioprotective agents against toxigenic penicillia in dry-fermented sausages. Food Microbiology, 46, 114-120. https://doi.org/10.1016/j.fm.2....
 
30.
Oliveira, C.M., Auad, A.M., Mendes, S.M., Frizzas, M.R. (2014). Crop losses and the economic impact of insect pests on Brazilian agriculture. Crop Protection, 56, 50-54. https://doi.org/10.1016/j.crop....
 
31.
Parveen, S., Wani, A.H., Bhat, M.Y., Koka, J.A., Wani, F.A. (2016). Management of postharvest fungal rot of peach (Prunus persica) caused by Rhizopus stolonifer in Kashmir Valley, India. Plant Pathology and Quarantine, 6(1), 19-29. https://doi.org/10.5943/ppq/6/....
 
32.
Quaglia, M., Ederli, L., Pasqualini, S., Zazzerini, A. (2011). Biological control agents and chemical inducers of resistance for postharvest control of Penicillium expansum Link. on apple fruit. Postharvest Biology and Technology, 59(3), 307-315. https://doi.org/10.1016/j.post....
 
33.
Robiglio, A., Sosa, M.C., Lutz, M.C., Lopes, C.A., Sangorrín, M.P. (2011). Yeast biocontrol of fungal spoilage of pears stored at low temperature. International Journal of Food Microbiology, 147(3), 211-216. https://doi.org/10.1016/j.ijfo....
 
34.
Romanazzi, G., Feliziani, E., Baños, S.B., Sivakumar, D. (2017). Shelf life extension of fresh fruit and vegetables by chitosan treatment. Critical Reviews in Food Science and Nutrition, 57(3), 579-601. https://doi.org/10.1080/104083....
 
35.
Romanazzi, G., Smilanick, J.L., Feliziani, E., Droby, S. (2016). Integrated management of postharvest grey mould on fruit crops. Postharvest Biology and Technology, 113, 69-76. https://doi.org/10.1016/j.post....
 
36.
Ruiz-Moyano, S., Hernández, A., Galvan, A.I., Córdoba, M.G., Casquete, R., Serradilla, M.J., Martín, A. (2020). Selection and application of antifungal VOCs-producing yeasts as biocontrol agents of grey mould in fruits. Food Microbiology, 92, art. no. 103556. https://doi.org/10.1016/j.fm.2....
 
37.
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.bioc....
 
38.
Wang, X., Glawe, D.A., Kramer, E., Weller, D., Okubara, P.A. (2018) Biological control of Botrytis cinerea: interactions with native vineyard yeasts from Washington State. Phytopathology, 108(6), 691-701. https://doi.org/10.1094/PHYTO-....
 
39.
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. https://doi.org/10.1016/j.bioc....
 
 
CITATIONS (7):
1.
Perfume Guns: Potential of Yeast Volatile Organic Compounds in the Biological Control of Mycotoxin-Producing Fungi
Safa Oufensou, Hassan Ul, Virgilio Balmas, Samir Jaoua, Quirico Migheli
Toxins
 
2.
Screening of antagonistic yeast strains for postharvest control of Penicillium expansum causing blue mold decay in table grape
Nayyereh Alimadadi, Zahra pourvali, Shaghayegh Nasr, Seyed Fazeli
Fungal Biology
 
3.
Microbial volatilome in food safety. Current status and perspectives in the biocontrol of mycotoxigenic fungi and their metabolites
Hassan Ul, Safa Oufensou, Randa Zeidan, Quirico Migheli, Samir Jaoua
Biocontrol Science and Technology
 
4.
Characterization of Antioxidant and Antimicrobial Activity and Phenolic Compound Profile of Extracts from Seeds of Different Vitis Species
Luisa Pozzo, Teresa Grande, Andrea Raffaelli, Vincenzo Longo, Stanisław Weidner, Ryszard Amarowicz, Magdalena Karamać
Molecules
 
5.
Antagonistic mechanisms of yeasts Meyerozyma guilliermondii and M. caribbica for the control of plant pathogens: A review
Daniela Herrera-Balandrano, Su-Yan Wang, Cai-Xia Wang, Xin-Chi Shi, Feng-Quan Liu, Pedro Laborda
Biological Control
 
6.
Challenges in apple preservation: Fungicide resistance and emerging biocontrols
Mohammed Khadiri, Hassan Boubaker, Haitam Lahmamsi, Mohammed Taoussi, Rachid Ezzouggari, Latifa Askarne, Abdelaaziz Farhaoui, Essaid Barka, Rachid Lahlali
Physiological and Molecular Plant Pathology
 
7.
Bioprotective yeasts: Potential to limit postharvest spoilage and to extend shelf life or improve microbial safety of processed foods
Yan He, Pascal Degraeve, Nadia Oulahal
Heliyon
 
eISSN:2083-6007
ISSN:1230-0322
Journals System - logo
Scroll to top