Efficacy of some Yeast Strains for Preventing Infection of Pistachio with Aspergillus flavus and Aflatoxin

Subject Areas : Plant Pathology

Hadi Golzari ¹ , Mahdi Pirnia ² , Mohammad Moradi ³ , Roohollah Saberi-Rise ⁴ , Seyed Kazem Sabbagh ⁵ , Mojtaba Keykhasaber ⁶

1 - Department of Plant Protection, Faculty of Agriculture, University of Zabol, Zabol, Iran
2 - Department of Plant Protection, Faculty of Agriculture, University of Zabol, Zabol, Iran
3 - Pistachio Research Center, Horticultural Science Research Institute, Agricultural Research, Education and Extension Organization (AREEO), Rafsanjan, Iran
4 - Department of Plant Protection, Faculty of Agriculture, Vali-e-Asr University of Rafsanjan, Rafsanjan, Iran
5 - Department of Biology, Faculty of Science, Yazd University, Yazd, Iran
6 - Department of Plant Protection, Faculty of Agriculture, University of Zabol, Zabol, Iran

Received: 2023-07-29 Accepted : 2023-10-02 Published : 2023-11-04

Keywords: biocontrol, Volatile organic compounds, Nuts, toxin,

Abstract :

Aspergillus flavus and aflatoxin on pistachio are the most important hazards to human health, which start in the orchard and will continue to the storage. This research selected 16 most effective yeast strains through dual culture (DC) assay according to the interaction between 376 yeast strains and A. flavus isolate P1684 in an initial screening. The antifungal ability of the strains was determined to be 94.5%, 72.08 %, and 91.31% in DC, volatile organic compounds (VOCs), and extracellular secretions (ESs) assays, respectively. In DC and VOCs assays, the YE 43-6 yeast strain showed maximum inhibition of growth, whereas powder and liquid formulation of the YE 43-10 yeast strain showed better performance. Ammonia vapor assay revealed that yeast strains significantly reduced aflatoxin production in A. flavus. Under in-situ conditions, trees were sprayed with cell/spore populations of both effective yeasts and A. flavus to determine the ability of yeast strains to compete with the pathogen. After 45 days, the fruits were harvested, and the average number of colonies per pistachio fruit unit (CFU/Nut) was determined. The highest and lowest reduction of populations were observed in YE 43-10 (85.71%) and YE 36-9 (35.18%), respectively. In both YE 43-6 and YE 43-10 strains, powder formulation was slightly more effective than liquid, and VOCs effectively prevented pistachio contamination with A. flavus and aflatoxin.

References:

Abadias M, Usall J, Teixidó N, Viñas I (2003) Liquid formulation of the post-harvest biocontrol agent Candida sake CPA-1 in isotonic solutions. Phytopathology. 93, 436–442.
Abdel-Kareem MM, Rasmey AM, Zohri AA (2019) The action mechanism and biocontrol potentiality of novel isolates of Saccharomyces cerevisiae against the aflatoxigenic Aspergillus flavus. Letters of Applied Microbiology 68, 104–111.
Ando H, Hatanaka K, Ohata I, Yamashita-Kitaguchi Y, Kurata A, Kishimoto N (2012) Antifungal activities of volatile substances generated by yeast isolated from Iranian commercial cheese. Food Control. 26, 472–478.
Armando MR, Dogi CA, Rosa CA, Dalcero AM, Cavaglieri LR (2012) Saccharomyces cerevisiae strains and the reduction of Aspergillus parasiticus growth and aflatoxin B1 production at different interacting environmental conditions, in vitro. Food Additives and Contaminants. Part A 29, 1443–1449. https://doi.org/10.1080/19440 049.2012.69865 5.
Arrarte E, Garmendia G, Rossini C, Wisniewski M Vero S (2017) Volatile organic compounds produced by Antarctic strains of Candida sake play a role in the control of post-harvest pathogens of apples. Biological Control. 109, 14–20. https://doi.org/10.1016/j.biocontrol.2017.03.002.
Bar-Shimon M, Yehuda H, Cohen L, Weiss B, Kobeshnikov A, Daus A, Goldway M, Wisniewski M, Droby S (2004) Characterization of extracellular lytic enzymes produced by the yeast biocontrol agent Candida oleophila. Current Genetics. 45, 140–148. https ://doi. org/10.1007/s00294-003-0471-7.
Buxdorf K, Rahat I, Gafni A, Levy M (2013) The epiphytic fungus Pseudozyma aphidis induces jasmonic acid- and salicylic acid/nonexpressor of PR1-independent local and systemic resistance. Plant Physiology. 161, 2014–2022. https://doi.org/10.1104/pp.112. 212969.
European Food Safety Authority (EFSA) (2005) Opinion of the Scientific Committee on a request from EFSA related to a generic approach to the safety assessment by EFSA of microorganisms used in food/ feed and the production of food/feed additives. European Food Safety Authority. 3, 226. https://doi.org/10.2903/j.efsa.2005.226.
European Food Safety Authority (EFSA) (2015) Peer review of the pesticide risk assessment of the active substance Saccharomyces cerevisiae strain LAS02. European Food Safety Authority. 13, 4322. https://doi.org/10.2903/j.efsa.2015.4322.
Fani SR, Moradi M, Probst C, Zamanizadeh HR, Mirabolfathy M, Haidukowski M, Logrieco AF (2014) A critical evaluation of cultural methods for the identification of atoxigenic Aspergillus flavus isolates for aflatoxin mitigation in pistachio orchards of Iran. European Journal of Plant Pathology.140(4), 631-642.
Farbo MG, Urgeghe P, Fiori S, Marcello A, Oggiano S, Balmas V, Hassan Z, Jaoua S, Migheli Q (2018) Effect of yeast volatile organic compounds on ochratoxin A-producing Aspergillus carbonarius and A. ochraceus. International Journal of Food Microbiology. 284, 1–10. https://doi.org/10.1016/j.ijfoo dmicr o.2018.06.023.
Fialho MB, Tofano L, Pedroso MP, Augusto F, Pascholati SF (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 Biotechnology. 26, 925–932. https://doi.org/10.1007/s1127 4-009-0255-4.
Fiori S, Fadda A, Giobbe S, Berardi E, Migheli Q (2008) Pichia angustais an effective biocontrol yeast against post-harvest decay of apple fruit caused by Botrytis cinerea and Monilia fructicola. Federation of European Microbiological Societies Yeast Research. 8, 961–963. https://doi.org/10.1111/j.1567-1364.2008.00424.x
Fiori S, Urgeghe PP, Hammami W, Razzu S, Jaoua S, Migheli Q (2014) Biocontrol activity of four non-and low-fermenting yeast strains against Aspergillus carbonarius and their ability to remove ochratoxin A from grape juice. International Journal of Food Microbiology. 189, 45–50. https://doi.org/10.1016/j.ijfoo dmicr o.2014.07.020.
Freimoser FM, Rueda-Mejia MP, Tilocca B, Migheli Q (2019) Biocontrol yeasts: mechanisms and applications. World Journal of Microbiology and Biotechnology. 35, 154 https:// doi.org/10.1007/s11274-019-2728-4.
Hadwiger LA, McDonel H, Glawe D (2015) Wild yeast strains as prospective candidates to induce resistance against potato late blight (Phytophthora infestans). American Journal of Potato Research. 92, 379–386. https://doi.org/10.1007/s1223 0-015-9443-y.
Hosseini N, Rezanejad F, ZamaniBahramabadi E (2022) Effects of soil texture, irrigation intervals, and cultivar on some nut qualities and different types of fruit blankness in pistachio (Pistacia vera L.). International Journal of Horticultural Science and Technology. 9, 41-53.
Hua SST (2008) Progress in prevention of aflatoxin contamination in food by preharvest application of a yeast strain, Pichia anomala WRL6. Mod. Multidiscip. Applied Microbiology. 322–326.
Hua SST, Beck JJ, Sarreal SB, 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 favus. Mycotoxin Research. 30, 71–78. https://doi.org/10.1007/s1255 0-014-0189-z.
Huang R, Li GQ, Zhang J, Yang L, Che HJ, Jiang DH, Huang HC (2011) Control of post-harvest Botrytis fruit rot of strawberry by volatile organic compounds of Candida intermedia. Phytopathology. 101, 859–869. https://doi.org/10.1094/PHYTO -09-10-0255.
Jiang F, Zheng X, Chen J (2009) Microarray analysis of gene expression profile induced by the biocontrol yeast Cryptococcus laurentii in cherry tomato fruit. Gene. 430, 12–16.
Junker K, Chailyan A, Hesselbart A, Forster J, Wendland J (2019) Multi-omics characterization of the necrotrophic mycoparasite Saccharomycopsis schoenii. PLoS Pathogens. 15, e1007692. https://doi.org/10.1371/journ al.ppat.10076 92.
Kurtzman CP, Boekhout T, Robert V, Fell JW, Deak T (2003) Methods to identify yeasts. In: Yeasts in Food (Boekhout T, Robert V, ed). Behr’s Verlag. Hamburg. 69–121.
Kurtzman CP, Robnett CJ (1998) Identification and phylogeny of ascomycetous yeasts from analysis of nuclear large subunit (26S) ribosomal DNA partial sequences. Antonie van Leeuwenhoek International Journal of General and Molecular Microbiology. 73, 331–371.
La Penna M, Nesci A, Etcheverry M (2004) In vitro studies on the potential for biological control on Aspergillus section Flavi by Kluyveromyces spp. Letters of Applied Microbiology. 38, 257–264.
Li BQ, Zhou ZW, Tian SP (2008) Combined effects of endo- and exogenous trehalose on stress tolerance and biocontrol efficacy of two antagonistic yeasts. Biological Control. 46, 187–193.
Liu J, Tian SP, Li BQ, Qin GZ (2009) Enhancing viability of two biocontrol yeasts in liquid formulation by applying sugar protectant combined with antioxidant. Biological Control. 54, 817–824.
Lopes MR, Klein MN, Ferraz LP, da Silva AC, Kupper KC (2015) Saccharomyces cerevisiae: a novel and efficient biological control agent for Colletotrichum acutatum during pre-harvest. Microbiology Research. 175, 93–99.
Luksa J, Podoliankaite M, Vepstaite I, Strazdaite-Zieliene Z, Urbona-vicius J, Serviene E (2015) Yeast beta-1,6-glucan is a primary target for the Saccharomyces cerevisiae K2 toxin. Eukaryot Cell. 14, 406–414. https://doi.org/10.1128/EC.00287-14.
Mahbobinejhad Z, Aminian H, Ebrahimi L, Vahdati K. (2019) Reduction of aflatoxin production by exposing Aspergillus flavus to CO2. Journal of Crop Protection 8(4), 441-448.
Masoud W, Poll L, Jakobsen M (2005) Influence of volatile compounds produced by yeasts predominant during processing of Coffea arabica in East Africa on growth and ochratoxin A (OTA) production by Aspergillus ochraceus. Yeast. 22, 1133–1142. https://doi.org/10.1002/yea.1304.
Melin P, Håkansson S, Schnürer J (2007) Optimisation and comparison of liquid and dry formulations of the biocontrol yeast Pichia anomala J121. Applied Microbiology and Biotechnology. 73, 1008–1016.
Nazoori F, ZamaniBahramabadi E, Mirdehghan H (2022) Effect of sulfur pesticide on the quality of fresh pistachios in cold storage. International Journal of Horticultural Science and Technology. 9, 453-462.
Nazoori F, ZamaniBahramabadi E, Mirdehghan H, Yousefi M (2022) Preharvest application of sulfur as pesticide on fresh hull and kernel of pistachio (Pistacia vera L.). International Journal of Horticultural Science and Technology. 9, 117-129.
Pei-Hua C, Rou-Yun C, Chou JY (2018) Screening and evaluation of yeast antagonists for biological control of Botrytis cinerea on strawberry fruits. Mycobiology. 46(1), 33-46, DOI: 10.1080/12298093.2018.1454013.
Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA (2014) Induced systemic resistance by benefi-cial microbes. Annual Review of Phytopathology. 52, 347–375. https://doi. org/10.1146/annurev-phyto-082712-102340.
Pitt JI, Hocking AD, Glenn DR (1983) An improved medium for detection of Aspergillus flavus and A. parasiticus. Journal of Applied Bacteriology. 54, 109–114.
Pretscher J, Fischkal T, Branscheidt S, Jäger L, Kahl S, Schlander M, Thines E, Claus H (2018) Yeasts from different habitats and their potential as biocontrol agents. Fermentation. 4, 31.
Ren X, Zhang Q, Zhang W, Mao, J, Peiwu L (2020) Control of aflatoxigenic molds by antagonistic microorganisms: inhibitory behaviors, bioactive compounds, related mechanisms and influencing factors. Toxins. 12-24.
Revillion JP, Brandelli A, Ayub MAZ (2003) Production of yeast extract from whey using Kluyveromyces marxianus. Brazilian Archives of Biology and Technology. 46, 121–8.
Sommer B, Overy DP, Haltli B, Kerr RG (2016) Secreted lipases from Malassezia globosa: recombinant expression and determination of their substrate specificities. Microbiology. 162, 1069–1079.
Tayel AA, El-Tras WF, Moussa SH, El-Agamy MA (2013) Antifungal action of Pichia anomala against aflatoxigenic Aspergillus flavus and its application as a feed supplement. Journal of the Science of Food and Agriculture. 93, 3259–3263.
Yu T, Zheng XD (2006) Salicylic acid enhances biocontrol efficacy of the antagonist Cryptococcus laurentii in apple fruit. Journal of Plant Growth Regulation. 25, 166–174. https://doi.org/10.1007/s00344-005-0077-z.
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. Post-harvest Biology and Technology. 26, 91–98.
Whipps JM (1997) Developments in the biological control of soil-borne plant pathogens. Advances in Botanical Research. Academic Press, UK. pp. 1-134.
Zajc J, Gostincar C, Cernosa A, Gunde-Cimerman N (2019) Stress-tolerant yeasts: opportunistic pathogenicity versus biocontrol potential. Genes (Basel). 10, 42.
Zhang D, Spadaro D, Garibaldi A, Gullino ML (2011) Potential biocontrol activity of a strain of Pichia guilliermondii against grey mold of apples and its possible modes of action. Biological Control. 57, 193–201.