Biocontrol ability and volatile organic compounds production as a putative mode of action of yeast strains isolated from organic grapes and rye grains
Tóm tắt
The inhibiting activity of three yeast strains belonging to Pichia kudriavzevii, Pichia occidentalis, and Meyerozyma quilliermondii/Meyerozyma caribbica genera against common plant pathogens representing Mucor spp., Penicillium chrysogenum, Penicillium expansum, Aspergillus flavus, Fusarium cereals, Fusarium poae, as well as Botrytis cinerea genera was investigated. The yeast strains tested had a positive impact on growth inhibition of all target plant pathogens. The degree of inhibition was more than 50% and varied depending on both the yeast antagonist and the mold. Ethyl esters of medium-chain fatty acids, phenylethyl alcohol, and its acetate ester prevailed among the analyzed volatile organic compounds (VOCs) emitted by yeasts in the presence of the target plant pathogens. Due to the method used, assuming no contact between the antagonist and the pathogen, the antagonistic activity of the yeast strains studied resulted mainly from the production of biologically active VOCs. Moreover, the antagonistic activity was not only restricted to a single plant pathogen but effective towards molds of different genera, making the yeast strains studied very useful for potential application in biological control.
Tài liệu tham khảo
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 postharvest pathogens of apples. Biol Control 109:14–20
Cao J, Zhang H, Yang Q, Ren R (2013) Efficacy of Pichia caribbica in controlling blue mold rot and patulin degradation in apples. Int J Food Microbiol 162(2):167–173
Castoria R, Morena V, Caputo L, Panfili G, De Curtis F, De Cicco V (2005) Effect of the biocontrol yeast Rhodotorula glutinis strain LS11 on patulin accumulation in stored apples. Phtyopathology 95:1271–1278
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
Coehlo AR, Celli MG, Ono EYS, Wosiacki G, Hoffman FL, Pagnocca FC, Hirooka EY (2007) Penicillium expansum versus antagonist yeasts and patulin degradation in vitro. Braz Arch Biol Technol 50:725–733
Cortes-Barco A, Goodwin P, Hsiang T (2010) Comparison of induced resistance activated by benzothiadiazole, (2R,3R)-butanediol and an isoparafin mixture against anthracnose of Nicotiana benthamiana. Plant Pathol 59:643–653
Di Francesco A, Ugolini L, Lazzeri L, Mari M (2015) Production of volatile organic compounds by Aureobasidium pullulans as a potential mechanism of action against postharvest fruit pathogens. Biol Control 81:8–14
Druvefors AU, Passoth V, Schnürer J (2005) Nutrients effects on biocontrol of Penicillium roqueforti by Pichia anomala J121 during airtight storage of wheat. Appl Environ Microbiol 71:1865–1869
Farkas Z, Márki-Zay J, Kucsera J, Vágvölgyi C, Golubev W, Pfeiffer I (2012) Characterization of two different toxins of Wickerhamomyces anomalus (Pichia anomala) VKM Y-159. Acta Biol Hung 63(2):277–287
Fialho MB, Toffano 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 J Microbiol Biotechnol 26:925–932
Fiahlo MB, Moraes MHD, Tremocoldi AR, Pascholati SF (2011) Potential of antimicrobial volatile organic compounds to control Sclerotinia sclerotiorum in bean seeds. Pesqui Agropecu Bras Bras 46(2):137–142
Fincheira P, Quiroz A (2018) Microbial volatiles as plant growth inducers. Microbiol Res 208:63–75
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. Int J Food Microbiol 189:45–50
Freimoser FM, Rueda-Mejia MP, Tilocca B, Migheli Q (2019) Biocontrol yeasts: mechanisms and applications. World J Microbiol Biotechnol 35:154
Guyard C, Séguy N, Cailliez JC, Drobecq H, Polonelli L, Dei-Cas E, Menozzi FD (2002) Characterization of a Williopsis saturnus var. mrakii high molecular weight secreted killer toxin with broad-spectrum antimicrobial activity. J Antimicrob Chemother 49(6):961–971
Huang R, Li GQ, Zhang J, Yang L, Che HJ, Jiang DH, Huang HC (2011) Control of postharvest Botrytis fruit rot of strawberry by volatile organic compounds of Candida intermedia. Phytopathology 101:859–869
Irtwange SV (2006) Application of biological control agents in pre- and postharvest operations. Agricultural Engineering International: the CIGR Ejournal. Invited overview No. 3, vol VIII
Jeleń HH (2003) Use of solid phase microextratction (SPME) for profiling fungal volatile metabolites. Lett Appl Microbiol 36:263–267
Kanchiswamy CN, Malnoy M, Maffei ME (2015) Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front Plant Sci 6(151):1–23
Koumba Kone M, Tagro Guehi S, Durand N, Ban-Koffi L, Berthiot L, Fontana Tachon A, Brou K, Boulanger R, Monte TD (2016) Contribution of predominant yeasts to the occurrence of aroma compounds during cocoa bean fermentation. Food Res Int 89:910–917
Kurtzman CP, Robnett CJ, Basehoar-Powers E (2008) Phylogenetic relationships among species of Pichia, Issatchenkia and Williopsis determined from multigene sequence analysis, and the proposal of Barnettozyma gen. nov., Lindnera gen. nov. and Wickerhamomyces gen. nov. FEMS Yeast Res 8(6):939–954
Lahlali R, Hamadi Y, El Guilli M, Jijakli MH (2011) Efficacy assessment of Pichia guilliermondi strain Z1, a new biocontrol agent, against citrus blue mould in Morocco under the influence of temperature and relative humidity. Biol Control 56(3):217–224
Li R, Zhang H, Liu W, Zheng X (2011) Biocontrol of postharvest gray and blue mold decay of apples with Rhodotorula mucilaginosa and possible mechanisms of action. Int J Food Microbiol 146(2):151–156
Li N, Alfiky A, Wang W, Islam M, Nourollahi K, Liu X, Kang S (2018) Volatile compound-mediated recognition and inhibition between Trichoderma biocontrol agents and Fusarium oxysporum. Front Microbiol 9:2614
Lima JR, Gondim DMF, Oliveira JTA, Oliveira FSA, Goncalves LRB, Viana FMP (2013) Use of killer yeast in the management of postharvest papaya anthracnose. Postharvest Biol Technol 83:58–64
Liu HM, Guo JH, Cheng YJ, Liu P, Long CA, Deng BX (2010) Inhibitory activity of tea polyphenol and Hanseniaspora uvarum against Botrytis cinerea infections. Lett Appl Microbiol 51(3):258–263
Liu P, Cheng Y, Yang M, Liu Y, Chen K, Long C, Deng X (2014) Mechanism of action for 2-phenylethanol isolated from Kloeckera apiculata in control of Penicillium molds of citrus fruits. BMC Microbiol 14:242
Masoud W, Kaltoft CH (2006) The effects of yeasts involved in the fermentation of Coffea arabica in East Africa on growth and ochratoxin A (OTA) production by Aspergillus ochraceus. Int J Food Microbiol 106:229–234
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(14):1133–1142
Meshram V, Kapoor N, Chopra G, Saxena S (2017) Muscodor camphora, a new record from Cinnamomum camphora. Mycosphere 8(4):568–582
Morath SU, Hung R, Bennett JW (2012) Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev 26:73–83
Moya P, Girotti JR, Toledo AV, Sisterna MN (2018) Antifungal activity of Trichoderma VOCs against Pyrenophora teres, the causal agent of barley net blotch. J Plant Prot Res 58(1):45–53
Nally MC, Pesce VM, Maturano YP, Assaf LR, Toro ME, de Figueroa LC, Vazquez F (2015) Antifungal modes of action of Saccharomyces and other biocontrol yeasts against fungi isolated from sour and grey rots. Int J Food Microbiol 204:91–100
O’Donnell K (1993) Fusarium and its near relatives. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, pp 225–233
Olstorpe M, Passoth V (2011) Pichia anomala in grain biopreservation. Antonie van Leeuwenhoek J Microbiol 99(1):57–62
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 Microbiol 47:85–92
Piasecka-Jóźwiak K, Chabłowska B (2017) Anti-mold properties of yeast strains as a biological agent for protection of grain during storage. J Res Appl Agric Eng 62(4):84–89
Pretscher J, Fischkal T, Branscheidt S, Jager L, Kahl S, Schlander M, Thines E, Claus H (2018) Yeasts from different habitats and their potential as biocontrol agents. Fermentation 4(31):3–17
Robiglio A, Sosa MC, Lutz MC, Lopes CA, Sangorrín MP (2011) Yeast biocontrol of fungal spoilage of pears stored at low temperature. Int J Food Microbiol 147(3):211–216
Ruiz-Moyano S, Martín A, Villalobos MC, Calle A, Serradilla MJ, Córdoba MG, Hernández A (2016) Yeasts isolated from figs (Ficus carica L.) as biocontrol agents of postharvest fruit diseases. Food Microbiol 57:45–53
Saravanakumar D, Ciavorella A, Spadaro D, Garibaldi A, Gullino ML (2008) Metschnikowia pulcherrima strain MACH1 outcompetes Botrytis cinerea, Alternaria alternata and Penicillium expansum in apples through iron depletion. Postharvest Biol Technol 49(1):121–128
Siddiquee S, Cheong BE, Taslima K, Kausar H, Hasan MM (2012) Separation and identification of volatile compounds from liquid cultures of Trichoderma harzianum by GC-MS using three different capillary columns. J Chromatogr Sci 50:358–367
Song GC, Ryu CM (2013) Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. Int J Mol Sci 14:9803–9819
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 Sci Technol 47:39–49
Stoppacher N, Kluger B, Zeilinger S, Krska R, Schuhmacher R (2010) Identification and profiling of volatile metabolites of the biocontrol fungus Trichoderma atroviride by HS-SPME-GC-MS. J Microbiol Methods 81:187–193
Strobel G, Dirkse E, Sears J, Markworth C (2001) Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiology 147:2943–2950
Ting ASY, Mah SW, Tee CS (2010) Identification of volatile metabolites from fungal endophytes with biocontrol potential towards Fusarium oxysporum F. sp. cubense Race 4. Am J Agric Biol Sci 5(2):177–182
Wan M, Li G, Zhang J, Jiang D, Huang HC (2008) Effect of volatile substances of Streptomyces platensis F-1 on control of plant fungal diseases. Biol Control 46:552–559
Wang C, Wang Z, Qiao X, Li Z, Li F, Chen M, Wang Y, Huang Y, Cui H (2013) Antifungal activity of volatile organic compounds from Streptomyces alboflavus TD-1. FEMS Microbiol Lett 341:45–51
White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA et al (eds) PCR protocols: a guide to methods and applications. Academic Press, Inc., New York, pp 315–322
Zhang Z, Pawliszyn J (1993) Headspace solid phase microextraction. Anal Chem 65:1843–1852