The potential of antagonistic yeasts and bacteria from tomato phyllosphere and fructoplane in the control of Alternaria fruit rot of tomato

References

• FAO. 2020. FAOSTAT. Available online at: http://www.fao.org/faostat/en/#data/QC/visualize.
   Google Scholar
• FDA. 2013. CFR-Code of Federal Regulations Title 21. http://www.accessdata.fda.gov/scripts/cdrh/cfdocs/cfcfr/CFRSearch.cfm?fr=173.160.
   Google Scholar
• Al-Badri BAS, Al-Maawali SS, Al-Balushi ZM, Al-Mahmooli IH, Al-Sadi AM, Velazhahan R. 2020. Cyanide degradation and antagonistic potential of endophytic Bacillus subtilis strain BEB1 from Bougainvillea spectabilis Willd. Front Life Sci. 13:92–98.
   Google Scholar
• Al-Daghari DSS, Al-Abri SA, Al-Mahmooli IH, Al-Sadi AM, Velazhahan R. 2020. Efficacy of native antagonistic rhizobacteria in the biological control of Pythium aphanidermatum-induced damping-off of cucumber in Oman. J Plant Pathol. 102:305–310.
   Web of Science ®Google Scholar
• Al-Hussini HS, Al-Rawahi AY, Al-Marhoon AA, Al-Abri SA, Al-Mahmooli IH, Al- Sadi AM, Velazhahan R. 2019. Biological control of damping-off of tomato caused by Pythium aphanidermatum by using native antagonistic rhizobacteria isolated from Omani soil. J Plant Pathol. 101:315–322.
   Web of Science ®Google Scholar
• Al-Rawahi AY, Al-Mahmooli IH, Al-Sadi AM, Al-Sabahi JN, Velazhahan R. 2018. Toxin production by melon root rot fungus, Monosporascus cannonballus. Australas Plant Pathol. 47:543–546.
   Web of Science ®Google Scholar
• Al-Sadi AM, Al-Ghaithi AG, Al-Balushi ZM, Al-Jabri AH. 2012. Analysis of diversity in Pythium aphanidermatum populations from a single greenhouse reveals phenotypic and genotypic changes over 2006 to 2011. Plant Dis. 96:852–858.
   PubMed Web of Science ®Google Scholar
• Al-Shibli H, Dobretsov S, Al-Nabhani A, Maharachchikumbura S, Velazhahan R, Al-Sadi AM. 2019. Aspergillus terreus obtained from mangrove exhibits antagonistic activities against Pythium aphanidermatum-induced damping-off of cucumber. Peer J. 7:e7884.
   Web of Science ®Google Scholar
• Alkan N, Fortes AM. 2015. Insights into molecular and metabolic events associated with fruit response to post-harvest fungal pathogens. Front Plant Sci. 6:889.
   PubMed Web of Science ®Google Scholar
• Banani H, Spadaro D, Zhang D, Matic S, Garibaldi A, Gullino ML. 2014. Biocontrol activity of an alkaline serine protease from Aureobasidium pullulans expressed in Pichia pastoris against four postharvest pathogens on apple. Int J Food Microbiol. 182:1–8.
   Web of Science ®Google Scholar
• Banani H, Spadaro D, Zhang D, Matic S, Garibaldi A, Gullino ML. 2015. Postharvest application of a novel chitinase cloned from Metschnikowia fructicola and overexpressed in Pichia pastoris to control brown rot of peaches. Int J Food Microbiol. 199:54–61.
   PubMed Web of Science ®Google Scholar
• Barth M, Hankinson TR, Zhuang H, Breidt F. 2009. Microbiological spoilage of fruits and vegetables. In: Sperber WH, Doyle MP, editor. Compendium of the microbiological spoilage of foods and beverages. New York: Springer; p. 135–183.
   Google Scholar
• Buck JW. 2002. In vitro antagonism of Botrytis cinerea by phylloplane yeasts. Can J Bot. 80:885–891.
   Google Scholar
• Celis Zambrano C, Moreno Duran G, Sequeda-Castaneda LG, Garcia Caicedo A, Albarracín DM, Barreto Charry LC. 2014. Determining the effectiveness of Candida guilliermondii in the biological control of Rhizopus stolonifer in postharvest tomatoes. Univ Sci. 19:51–62.
   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.
   Web of Science ®Google Scholar
• Chaurasia B, Pandey A, Palni LMS, Trivedi P, Kumar B, Colvin N. 2005. Diffusible and volatile compounds produced by an antagonistic Bacillus subtilis strain cause structural deformations in pathogenic fungi in vitro. Microbiol Res. 160:75–81.
   PubMed Web of Science ®Google Scholar
• Chernin L, Brandis A, Ismailov Z, Chet I. 1996. Pyrrolnitrin production by an Enterobacter agglomerans strain with a broad spectrum of antagonistic activity towards fungal and bacterial phytopathogens. Curr Microbiol. 32:208–212.
   Web of Science ®Google Scholar
• Chernin L, Ismailov Z, Haran S, Chet I. 1995. Chitinolytic Enterobacter agglomerans antagonistic to fungal plant pathogens. Appl Environ. Microbiol. 61:1720–1726.
   PubMed Web of Science ®Google Scholar
• Contarino R, Brighina S, Fallico B, Cirvilleri G, Parafati L, Restuccia C. 2019. Volatile organic compounds (VOCs) produced by biocontrol yeasts. Food Microbiol. 82:70–74.
   PubMed Web of Science ®Google Scholar
• Cordero-Bueso G, Mangieri N, Maghradze D, Foschino R, Valdetara F, Cantoral JM, Vigentini I. 2017. Wild grape-associated yeasts as promising biocontrol agents against Vitis vinifera fungal pathogens. Front Microbiol. 8:2025.
   PubMed Web of Science ®Google Scholar
• da Cruz Cabral L, Pinto VF, Patriarca A. 2016. Control of infection of tomato fruits by Alternaria and mycotoxin production using plant extracts. Eur J Plant Pathol. 145:363–373.
   Web of Science ®Google Scholar
• De Bentzmann S, Plesiat P. 2011. The Pseudomonas aeruginosa opportunistic pathogen and human infections. Environ Microbiol. 13:1655–1665.
   PubMedGoogle Scholar
• 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.
   Web of Science ®Google Scholar
• Droby S, Chalutz E, Wilson CL, Wisniewski ME. 1989. Characterization of the biocontrol activity of Debaryomyces hansenii in the control of Penicillium digitatum on grapefruit. Can J Microbiol. 35:794–800.
   Web of Science ®Google Scholar
• El-Ghaouth A, Wilson CL, Wisniewski M. 2003. Control of postharvest decay of apple fruit with Candida saitoana and induction of defense responses. Phytopathology. 93:344–348.
   PubMed Web of Science ®Google Scholar
• El-Naggar NEA, El-Bindary AAA, Abdel-Mogib M, Nour NS. 2017. In vitro activity, extraction, separation and structure elucidation of antibiotic produced by Streptomyces anulatus NEAE-94 active against multidrug-resistant Staphylococcus aureus. Biotechnol Biotechnol Equip. 31:418–430.
   Web of Science ®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.
   Google Scholar
• Escriva L, Oueslati S, Font G, Manyes L. 2017. Alternaria mycotoxins in food and feed: an overview. J. Food Qual. 2017:1569748.
   Google Scholar
• 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.
   Web of Science ®Google Scholar
• Fitsiou L, Tzakou O, Hancianu M, Poiata A. 2007. Volatile constituents and antimicrobial activity of Tilia tomentosa Moench and Tilia cordata Miller oils. J Essent Oil Res. 19:183–185.
   Web of Science ®Google Scholar
• Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ. 2008. Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol. 74:2461–2470.
   PubMed Web of Science ®Google Scholar
• Freimoser FM, Rueda-Mejia MP, Tilocca B, Migheli Q. 2019. Biocontrol yeasts: mechanisms and applications. World J Microbiol Biotechnol. 35:154.
   PubMed Web of Science ®Google Scholar
• Garg H, Li H, Sivasithamparam K, Kuo J, Barbetti MJ. 2010. The infection processes of Sclerotinia sclerotiorum in cotyledon tissue of a resistant and a susceptible genotype of Brassica napus. Ann Bot. 106:897–908.
   Web of Science ®Google Scholar
• Geissberger P, Sequin U. 1991. Constituents of Bidens pilosa L.: do the components found so far explain the use of this plant in traditional medicine? Acta Trop. 48:251–261.
   PubMed Web of Science ®Google Scholar
• Goldstein J, Newbury DE, Joy DC, Lyman CE, Echlin P, Lifshin E, Sawyer L, Michael JR. 2003. Scanning electron microscopy and X-Ray microanalysis, 3rd ed. Berlin: Springer; p. 689.
   Google Scholar
• Hadar Y, Harman GE, Taylor AG, Norton JM. 1983. Effects of pre-germination of pea and cucumber seeds and of seed treatment with Enterobacter cloacae on rots caused by Pythium spp. Phytopathology. 73:1322–1325.
   Web of Science ®Google Scholar
• Halo BA, Al-Yahyai RA, Al-Sadi AM. 2018. Aspergillus terreus inhibits growth and induces morphological abnormalities in Pythium aphanidermatum and suppresses Pythium-induced damping-off of cucumber. Front Microbiol. 9:95.
   PubMed Web of Science ®Google Scholar
• Healy B, Cooney S, O’Brien S, Iversen C, Whyte P, Nally J, Callanan JJ, Fanning S. 2010. Cronobacter (Enterobacter sakazakii): an opportunistic foodborne pathogen. Foodborne Pathog Dis. 7:339–350.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Illakkiam D, Ponraj P, Shankar M, Muthusubramanian S, Rajendhran J, Gunasekaran P. 2013. Identification and structure elucidation of a novel antifungal compound produced by Pseudomonas aeruginosa PGPR2 against Macrophomina phaseolina. Appl Biochem. Biotechnol. 171:2176–2185.
   Web of Science ®Google Scholar
• Ippolito A, Nigro F. 2000. Impact of preharvest application of biological control agents on postharvest diseases of fresh fruits and vegetables. Crop Prot. 19:715–723.
   Web of Science ®Google Scholar
• Kagan IA, Flythe MD. 2014. Thin-layer chromatographic (TLC) separations and bioassays of plant extracts to identify antimicrobial compounds. J Vis Exp. 85:51411.
   Google Scholar
• Kalemba D, Kunicka A. 2003. Antibacterial and antifungal properties of essential oils. Curr Med Chem. 10:813–829.
   PubMed Web of Science ®Google Scholar
• Karabulut OA, Tezcan H, Daus A, Cohen L, Wiess B, Droby S. 2004. Control of preharvest and postharvest fruit rot in strawberry by Metschnikowia fructicola. Biocontrol Sci Technol. 14:513–521.
   Web of Science ®Google Scholar
• Kohl J, Kolnaar R, Ravensberg WJ. 2019. Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Front Plant Sci. 10:845.
   PubMed Web of Science ®Google Scholar
• Lahlali R, Hamadi Y, Jijakli MH. 2011. Efficacy assessment of Pichia guilliermondii strain Z1, a new biocontrol agent, against citrus blue mould in Morocco under the influence of temperature and relative humidity. Biol Control. 56:217–224.
   Web of Science ®Google Scholar
• Larena I, Torres R, De Cal A, Linan M, Melgarejo P, Domenichini P, Bellini A, Mandrin JF, Lichou J, De Eribe XO, Usall J. 2005. Biological control of postharvest brown rot (Monilinia spp.) of peaches by field applications of Epicoccum nigrum. Biol Control. 32:305–310.
   Web of Science ®Google Scholar
• Lee SB, Taylor JW. 1990. Isolation of DNA from fungal mycelia and single spores. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editor. PCR protocols: A guide to methods and applications. San Diego: Academic Press; p. 282–287.
   Google Scholar
• Lima G, Ippolito A, Nigro F, Salerno M. 1997. Effectiveness of Aureobasidium pullulans and Candida oleophila against postharvest strawberry rots. Postharvest Biol Technol. 10:169–178.
   Web of Science ®Google Scholar
• 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. Microbiol Res. 175:93–99.
   Google Scholar
• Marrufo T, Nazzaro F, Mancini E, Fratianni F, Coppola R, De Martino L, Agostinho AB, De Feo V. 2013. Chemical composition and biological activity of the essential oil from leaves of Moringa oleifera Lam. cultivated in Mozambique. Molecules. 18:10989–11000.
   PubMed Web of Science ®Google Scholar
• Meena M, Swapnil P, Upadhyay RS. 2017. Isolation, characterization and toxicological potential of Alternaria-mycotoxins (TeA, AOH and AME) in different Alternaria species from various regions of India. Sci Rep. 7:8777.
   PubMed Web of Science ®Google Scholar
• Minaxi SJ. 2010. Characterization of Pseudomonas aeruginosa RM-3 as a potential biocontrol agent. Mycopathologia. 170:181–193.
   PubMed Web of Science ®Google Scholar
• Nagarajkumar M, Bhaskaran R, Velazhahan R. 2004. Involvement of secondary metabolites and extracellular lytic enzymes produced by Pseudomonas fluorescens in inhibition of Rhizoctonia solani, the rice sheath blight pathogen. Microbiol Res. 159:73–81.
   PubMed Web of Science ®Google Scholar
• Nunes CA. 2012. Biological control of postharvest diseases of fruit. Eur J Plant Pathol. 133:181–196.
   Web of Science ®Google Scholar
• Nunes C, Usall J, Teixido N, Abadias M, Vinas I. 2002. Improved control of postharvest decay of pears by the combination of Candida sake (CPA-1) and ammonium molybdate. Phytopathology. 92:281–287.
   PubMed Web of Science ®Google Scholar
• Parafati L, Vitale A, Restuccia C, Cirvilleri G. 2017. Performance evaluation of volatile organic compounds by antagonistic yeasts immobilized on hydrogel spheres against gray, green and blue postharvest decays. Food Microbiol. 63:191–198.
   Web of Science ®Google Scholar
• Park JH, Kim HK. 1989. Biological control of Phytophtora crown and root rot of greenhouse pepper with Trichoderma harzianum and Enterobacter agglomerans by improved method of application. Korean J. Plant Pathol. 5:1–12.
   Google Scholar
• Pearson RC, Hall DH. 1975. Factors affecting the occurrence and severity of black mold of ripe tomato fruit by Alternaria alternata. Phytopathology. 65:1352–1359.
   Web of Science ®Google Scholar
• Perez MF, Contreras L, Garnica NM, Fernández-Zenoff MV, Farías ME, Sepulveda M, Ramallo J, Dib JR. 2016. Native killer yeasts as biocontrol agents of postharvest fungal diseases in lemons. PLoS one. 11:e0165590.
   PubMed Web of Science ®Google Scholar
• Prasongsuk S, Lotrakul P, Ali I, Bankeeree W, Punnapayak H. 2018. The current status of Aureobasidium pullulans in biotechnology. Folia Microbiol. 63:129–140.
   PubMed Web of Science ®Google Scholar
• 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.
   Google Scholar
• 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. 49:121–128.
   Web of Science ®Google Scholar
• Saravanakumar D, Spadaro D, Garibaldi A, Gullino ML. 2009. Detection of enzymatic activity and partial sequence of a chitinase gene in Metschnikowia pulcherrima strain MACH1 used as post-harvest biocontrol agent. Eur J Plant Pathol. 123:183–193.
   Web of Science ®Google Scholar
• Shi JF, Sun CQ. 2017. Isolation, identification, and biocontrol of antagonistic bacterium against Botrytis cinerea after tomato harvest. Braz J Microbiol. 48:706–714.
   PubMed Web of Science ®Google Scholar
• Simionato AS, Navarro MOP, de Jesus MLA, Barazetti AR, da Silva CS, Simões GC, Balbi-Peña MI, de Mello JCP, Panagio LA, de Almeida RSC, et al. 2017. The effect of phenazine-1-carboxylic acid on mycelial growth of Botrytis cinerea produced by Pseudomonas aeruginosa LV strain. Front Microbiol. 8:1102.
   Web of Science ®Google Scholar
• Singh VK, Singh AK, Kumar A. 2017. Disease management of tomato through PGPB: current trends and future perspective. 3 Biotech. 7:255.
   PubMedGoogle Scholar
• 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.
   Web of Science ®Google Scholar
• Spago FR, Mauro CSI, de Oliveira AG, Beranger JPO, Cely MVT, Stanganelli MM, Simionato AS, San Martin JAB, Andrade CGTJ, Mello JCP, Andrade G. 2014. Pseudomonas aeruginosa produces secondary metabolites that have biological activity against plant pathogenic Xanthomonas species. Crop Prot. 62:46–54.
   Web of Science ®Google Scholar
• Spalding DH. 1980. Control of Alternaria rot of tomatoes by postharvest application of imazalil. Plant Dis. 64:169–171.
   Google Scholar
• 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 Biol Technol. 26:91–98.
   Web of Science ®Google Scholar
• White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editor. PCR protocols: A guide to methods and applications. San Diego: Academic Press; p. 315–322.
   Google Scholar
• Wilson CL, Wisniewski ME. 1989. Biological control of postharvest diseases of fruits and vegetables: an emerging technology. Ann Rev Phytopathol. 27:425–441.
   Web of Science ®Google Scholar
• Wszelaki AL, Mitcham EJ. 2003. Effect of combinations of hot water dips, biological control and controlled atmospheres for control of gray mold on harvested strawberries. Postharvest Biol Technol. 27:255–264.
   Web of Science ®Google Scholar
• Zhang H, Mahunu GK, Castoria R, Yang Q, Apaliya MT. 2018. Recent developments in the enhancement of some postharvest biocontrol agents with unconventional chemicals compounds. Trends Food Sci Technol. 78:180–187.
   Web of Science ®Google Scholar
• 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. Biol Control. 57:193–201.
   Web of Science ®Google Scholar
• Zhao Y, Tu K, Shao XF, Jing W, Su ZP. 2008. Effects of the yeast Pichia guilliermondii against Rhizopus nigricans on tomato fruit. Postharvest Biol Technol. 49:113–120.
   Web of Science ®Google Scholar