|
UPSI Digital Repository (UDRep)
|
|
| ||||||||||||||||||||||||||||
| Abstract : Universiti Pendidikan Sultan Idris |
| Colletotrichum gloeosporioides causes anthracnose disease in papaya fruit resulting in tremendous economic loss due to its latent infection. This study aimed to evaluate the biocontrol activity of antagonistic yeasts against C. gloeosporioides in papaya and determine the possible mechanism involved. One hundred and ten yeast strains were isolated from different parts of the papaya plant. Among them, only five strains, namely F001, F006, L003, FL013 and LP010, showed more than 55% radial growth inhibition of C. gloeosporioides. These five potent yeast strains were further evaluated in vitro and in vivo. The results indicated that strain F001 had the strongest biocontrol activity based on spore germination and fungal growth inhibition. In Vivo, the strain F001 caused 66.7% and 25% reductions in disease incidence and severity, respectively. Based on molecular identification, the strain F001 was confirmed as Trichosporon asahii. Despite there was no significant induction of defense enzyme activities found on the treated fruits, SEM observation showed direct attachment of T. asahii with the fungal hyphae and interfere in their establishment to the fruit surface. Based on these findings, the antagonistic yeast T. asahii strain F001 may be used as a potential natural biological control agent against anthracnose disease in papaya fruit. ? 2021 by the authors. Licensee MDPI, Basel, Switzerland. |
| References |
Rahman, M.A.; Mahmud, T.M.M.; Kadir, J.; Abdul-Rahman, R.; Begum, M.M. Major postharvest fungal diseases of papaya cv. Sekaki in Selangor, Malaysia. Pertanika J. Trop. Agric. Sci. 2008, 31, 27–34. Capdeville, G.D., Jr.; Souza, M.T.; Santos, J.R.P.; Miranda, S.d.P.; Caetano, A.R.; Torres, F.A.G. Selection and testing of epiphytic yeasts to control anthracnose in post-harvest of papaya fruit. Sci. Hortic. 2007, 111, 179–185. Paiva, E.D.; Serradilla, M.J.; Ruiz-Moyano, S.; Córdoba, M.G.; Villalobos, M.C.; Casquete, R.; Hernández, A. Combined effect of antagonistic yeast and modified atmosphere to control Penicillium expansum infection in sweet cherries cv. Ambrunés. Int. J. Food Microbiol. 2017, 241, 276–282. Hernandez-Montiel, L.G.; Gutierrez-Perez, E.D.; Murillo-Amador, B.; Vero, S.; Chiquito-Contreras, R.G.; Rincon-Enriquez, G. Mechanisms employed by Debaryomyces hansenii in biological control of anthracnose disease on papaya fruit. Postharvest Biol. Technol. 2018, 139, 31–37. Manso, T.; Nunes, C. Metschnikowia andauensis as a new biocontrol agent of fruit postharvest diseases. Postharvest Biol. Technol. 2011, 61, 64–71. Carmona-Hernandez, S.; Reyes-Pérez, J.J.; Chiquito-Contreras, R.G.; Rincon-Enriquez, G.; Cerdan-Cabrera, C.R.; HernandezMontiel, L.G. Biocontrol of Postharvest Fruit Fungal Diseases by Bacterial Antagonists: A Review. Agronomy 2019, 9, 121. Spadaro, D.; Droby, S. Development of biocontrol products for postharvest diseases of fruit: The importance of elucidating the mechanisms of action of yeast antagonists. Trends Food Sci. Technol. 2016, 47, 39–49. Liu, J.; Sui, Y.; Wisniewski, M.; Droby, S.; Liu, Y. Review: Utilization of antagonistic yeasts to manage postharvest fungal diseases of fruit. Int. J. Food Microbiol. 2013, 167, 153–160. Droby, S.; Wisniewski, M.; Macarisin, D.; Wilson, C. Twenty years of postharvest biocontrol research: Is it time for a new paradigm? Postharvest Biol. Technol. 2009, 52, 137–145. [CrossRef] 10. Wilson, C.L.; Wisniewski, M.E. Biological control of postharvest diseases of fruit and vegetables: An emerging technology. Annu. Rev. Phytopathol. 1989, 27, 425–441. Konsue, W.; Dethoup, T.; Limtong, S. Biological Control of Fruit Rot and Anthracnose of Postharvest Mango by Antagonistic Yeasts from Economic Crops Leaves. Microorganisms 2020, 8, 317. El-Tarabily, K.A.; Sivasithamparam, K. Potential of yeasts as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Mycoscience 2006, 47, 25–35. Droby, S.; Chalutz, E. Mode of action of biocontrol agents for postharvest diseases. In Biological Control of Postharvest Diseases of Fruits and Vegetables-Theory and Practice; Wilson, C.L., Wisniewski, M.E., Eds.; CRC Press: Boca Raton, FL, USA, 1994. Arras, G.; Arru, S. Mechanisms of action of some microbial antagonists against fungal pathogens. Ann. Microbiol. Enzimol. 1997, 47, 97–120. Hasan, M.F. Controlling Anthracnose and Postharvest Quality of Papaya (Carica papaya cv. Frangi) Using Bacillus subtilis Strain B34. Ph.D. Thesis, Universiti Putra Malaysia, Selangor, Malaysia, 2012. Sariah, M. Potential of Bacillus spp. as a biocontrol agent for anthracnose fruit rot of chilli. Malays. Appl. Biol. 1994, 23, 53–60. Chanchaichaovivat, A.; Ruenwongsa, P.; Panijpan, B. Screening and identification of yeast strains from fruits and vegetables: Potential for biological control of postharvest chilli anthracnose (Colletotrichum capsici). Biol. Control 2007, 42, 326–335. Zheng, M.; Shi, J.; Shi, J.; Wang, Q.; Li, Y. Antimicrobial effects of volatiles produced by two antagonistic Bacillus strains on the anthracnose pathogen in postharvest mangos. Biol. Control. 2013, 65, 200–206. Al Zaemey, A.B.; Magan, N.; Thompson, A.K. Studies on the effect of fruit-coating polymers and organic acids on growth of Colletotrichum musae in vitro and on postharvest control of anthracnose of bananas. Mycol. Res. 1993, 97, 1463–1468. Droby, S.; Wisniewski, M.E.; Cohen, L.; Weiss, B.; Touitou, D.; Eilam, Y. Influence of CaCl2 on Penicillium digitatum, grapefruit peel tissue, and biocontrol activity of Pichia guilliermondii. Phytopathology 1997, 87, 310–315. Rahman, M.A.; Kadir, J.; Mahmud, T.M.M.; Abdul-Rahman, R.; Begum, M.M. Screening of Antagonistic Bacteria for Biocontrol Activities on Colletotrichum gloeosporioides in Papaya. Asian J. Plant Sci. 2007, 6, 12–20. Edwards, K.; Johnstone, C.; Thompson, C. A simple and rapid method for the preparation of genomic plant DNA for PCR analysis. Nucleic Acids Res. 1991, 19, 1349. White, T.J.; Bruns, T.; Lee, S.; Taylor, J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In PCR Protocols: A Guide to Methods and Applications; Innis, M.A., Gelfand, D.H., Snisky, J.J., White, T.J., Eds.; Academic Press: San Diego, CA, USA, 1990. Hata, E.M.; Sijam, K.; Ahmad, Z.A.M.; Yusof, M.T.; Azman, N.A. In vitro Antimicrobial Assay of Actinomycetes in Rice against Xanthomonas oryzae pv oryzicola and as Potential Plant Growth Promoter. Braz. Arch. Biol. Technol. 2015, 58, 821–832. Nghia, N.A.; Kadir, J.; Sunderasan, E.; Abdullah, M.P.; Malik, A.; Napis, S. Morphological and Inter Simple Sequence Repeat (ISSR) Markers Analyses of Corynespora cassiicola Isolates from Rubber Plantations in Malaysia. Mycopathologia 2008, 166, 189–201. Shahnazi, S. Biological Characterization and Genetic Diversity of Fusarium spp. Associated with Yellowing Disease in Black Pepper (Piper nigrum L.) in Malaysia. Ph.D. Thesis, Universiti Putra Malaysia, Selangor, Malaysia, 2012. Tamura, K.; Stecher, G.; Peterson, D.; Filipski, A.; Kumar, S. MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Mol. Biol. Evol. 2013, 30, 2725–2729. Illeperuma, C.K.; Jayasuriya, P. Prolonged storage of ‘Karuthacolomban’ mango by modified atmosphere packaging at low temperature. J. Hortic. Sci. Biotech. 2002, 77, 153–157. Singh, V.; Deverall, B.J. Bacillus subtilis as a control agent against fungal pathogens of citrus fruit. Trans. Br. Mycol. Soc. 1984, 83, 487–490. Venkatachalam, K.; Meenune, M. Changes in physiochemical quality and browning related enzyme activity of longkong fruit during four different weeks of on-tree maturation. Food Chem. 2012, 131, 1437–1442. Tian, S.P.; Xu, Y.; Jiang, A.L.; Gong, Q.Q. Physiological and quality responses of longan fruit to high O2 or high CO2 atmospheres in storage. Postharvest Biol. Technol. 2002, 24, 335–340. Kokkinakis, D.M.; Brooks, J.L. Tomato peroxidases: Purification, characterization and catalytic properties. Plant Physiol. 1979, 63, 93–99. Jiang, Y.M.; Joyce, D.C. ABA effects on ethylene production, PAL activity, anthocyanin and phenolic contents of strawberry fruit. Plant Growth Regul. 2003, 39, 171–174. Wang, Y.S.; Tian, S.P.; Xu, Y.; Qin, G.Z.; Yao, H. Changes in the activities of pro- and anti-oxidant enzymes in peach fruit inoculated with Cryptococcus laurentii or Penicillium expansum at 0 or 20 ◦C. Postharvest Biol. Technol. 2004, 34, 21–28. Beers, J.R.F.; Sizer, I.W. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J. Biol. Chem. 1952, 95, 133–140. [CrossRef] 36. Kurabachew, H.; Wydra, K. Characterization of plant growth promoting rhizobacteria and their potential as bioprotectant against tomato bacterial wilt caused by Ralstonia solanacearum. Biol. Control 2013, 67, 75–83. Mati´ca, S.; Spadaroa, D.; Garibaldia, A.; Gullinoa, M.L. Antagonistic yeasts and thermotherapy as seed treatments to control Fusarium fujikuroi on rice. Biol. Control 2014, 73, 59–67. Kurtzman, C.P.; Fell, J.W. The Yeasts: Taxonomic Study; Elsevier Science: Amsterdam, The Netherlands, 1998. 39. Druvefors, U. Yeast Biocontrol of Grain Spoilage Mold. Ph.D. Thesis, Swedish University of Agricultural Sciences, Uppsala, Sweden, 2004. Janisiewicz, W.J.; Tworkoski, T.J.; Kurtzman, C.P. Biocontrol potential of Metchnikowia pulcherrima strains against blue mold of apple. Phytopathology 2001, 91, 1098–1108. Kurtzman, C.P.; Droby, S. Metschnikowia fructicola, a new ascosporic yeast with potential for biocontrol of postharvest fruit rots. Syst. Appl. Microbiol. 2001, 24, 395–399. [CrossRef] 42. Zheng, X.D.; Zhang, H.Y.; Sun, P. Biological control of postharvest green mold decay of oranges by Rhodotorula glutinis. Eur. Food Res. Technol. 2005, 220, 353–357. Pertot, I.; Giovannini, O.; Benanchi, M.; Caffi, T.; Rossi, V.; Mugnai, L. Combining biocontrol agents with different mechanisms of action in a strategy to control Botrytis cinerea on grapevine. Crop. Prot. 2017, 97, 85–93. Alvindia, D.G.; Natsuaki, K.T. Evaluation of fungal epiphytes isolated from banana fruit surfaces for biocontrol of banana crown rot disease. Crop. Prot. 2008, 27, 1200–1207. Li, L.; Ma, J.; Li, Y.; Wang, Z.; Gao, T.; Wang, Q. Screening and partial characterization of Bacillus with potential applications in biocontrol of cucumber Fusarium wilt. Crop. Prot. 2012, 35, 29–35. Narayanasamy, P. Biological Management of Diseases of Crops; Springer: New York, NY, USA, 2013. Zhang, D.; Spadaro, D.; Garibaldi, A.; Gullino, M.L. Selection and evaluation of new antagonists for their efficacy against postharvest brown rot of peaches. Postharvest Biol. Technol. 2010, 55, 174–181. Sharma, N. Biological Controls for Preventing Food Deterioration; Wiley Blackwell: Chichester, UK, 2014. Sharma, R.R.; Singh, D.; Singh, R. Biological control of postharvest diseases of fruits and vegetables by microbial antagonists: A review. Biol. Control 2009, 50, 205–221. Droby, S.; Chalutz, E.; Wilson, C.L. Antagonistic microorganisms as biocontrol agents of postharvest diseases of fruit and vegetables. Postharvest News Inf. 1991, 2, 169–173. Janisiewicz, W.J. Biocontrol of postharvest diseases of temperate fruits: Challenges and opportunities. In Plant-Microbe Interactions and Biological Control; Boland, J., Kuykendall, L.D., Eds.; Marcel Dekker: New York, NY, USA, 1998. El Ghaouth, A.; Wilson, C.L.; Wisniewski, M.E. Biologically-based alternatives to synthetic fungicides for the postharvest diseases of fruit and vegetables. In Diseases of Fruit and Vegetables; Naqvi, S.A.M.H., Ed.; Springer: Dordrecht, The Netherlands, 2004. Zhang, D.; Spadaro, D.; Garibaldi, A.; Gullino, M.L. Potential biocontrol activity of a strain of Pichia guilliermondii against grey mold of apples and its possible modes of action. Biol. Control 2011, 57, 193–201. Selitrennikoff, C.P. Antifungal proteins. Appl. Environ. Microbiol. 2001, 67, 2883–2894. Schmitt, M.J.; Breinig, F. Yeast viral killer toxins: Lethality and self-protection. Nat. Rev. Microbiol. 2006, 4, 212–221. Coelho, A.R.; Celli, M.G.; Ono, E.Y.S.; Wosiacki, G. Penicillium expansum versus antagonist yeasts with perspectives of application in biocontrol and patulin degradation. Braz. Arch. Biol. Technol. 2007, 50, 725–733. Hashem, M.; Alamri, S. The biocontrol of postharvest disease (Botryodiplodia theobromae) of guava (Psidium guajava L.) by the application of yeast strains. Postharvest Biol. Technol. 2009, 53, 123–130. Muccilli, S.; Wemhoff, S.; Restuccia, C.; Meinhardt, F. Exoglucanase-encoding genes from three Wickerhamomyces anomalus killer strains isolated from olive brine. Yeast 2013, 30, 33–43. Marquina, D.; Santos, A.; Peinado, J.M. Biology of killer yeasts. Int. Microbiol. 2002, 5, 65–71. Santos, A.; san Mauro, M.; Bravo, E.; Marquina, D. PMKT2, a new killer toxin from Pichia membranifaciens, and its promising biotechnological properties for control of the spoilage yeast Brettanomyces bruxellensis. Microbiology 2009, 155, 624–634. Breinig, F.; Tipper, D.J.; Schmitt, M.J. Kre1p, the plasma membrane receptor for the yeast K1 viral toxin. Cell 2002, 108, 395–405. Oregel-Zamudio, E.; Angoa-Pérez, M.V.; Oyoque-Salcedo, G.; Aguilar-González, C.N.; Mena-Violante, H.G. Effect of candelilla wax edible coatings combined with biocontrol bacteria on strawberry quality during the shelf-life. Sci. Hortic. 2017, 214, 273–279. Wisniewski, M.; Wilson, C.; Hershberger, W. Characterization of inhibition of Rhizopus stolonifer germination and growth by Enterobacter cloacae. Can. J. Bot. 1989, 67, 2317–2323. Arras, G.; de-Cicco, V.; Arru, S.; Lima, G. Biocontrol by yeasts of blue mold of citrus fruits and the mode of action of an isolate of Pichia guilliermondii. J. Hortic. Sci. 1998, 73, 413–418. Droby, S.; Chalutz, E.; Wilson, C.L.; Wisniewski, M.E. Characterization of the biocontrol activity of Debaryomyces hansenii in the control of Penicillium digitatum on grapefruit. Can. J. Microbiol. 1989, 35, 794–800. Droby, S.; Cohen, L.; Daus, A.; Weiss, B.; Horev, B.; Chalutz, E.; Katz, H.; Keren-Tzur, M.; Shachnai, A. Commercial testing of aspire: A yeast preparation for the biological control of postharvest decay of citrus. Biol. Control 1998, 12, 97–101. Wisniewski, M.; Biles, C.; Droby, S.; McLaughlin, R.; Wilson, C.; Chalutz, E. Mode of action of the postharvest biocontrol yeast, Pichia guilliermondii. I. Characterization of attachment to Botrytis cinerea. Physiol. Mol. Plant Pathol. 1991, 39, 245–258. El Ghaouth, A.; Wilson, C.; Wisniewski, M.; Droby, S.; Smilanick, J.L.; Korsten, L. Biological control of postharvest diseases of fruits and vegetables. Appl. Mycol. Biotechnol. 2002, 2, 219–238. Walsh, T.J.; Melcher, G.P.; Lee, J.W.; Pizzo, P.A. Infections due to Trichosporon species: New concepts in mycology, pathogenesis, diagnosis and treatment. Curr. Top. Med. Mycol. 1993, 5, 79–113. Arnaldo, L.C.; Padovan, A.C.B.; Chaves, G.M. Current Knowledge of Trichosporon spp. and Trichosporonosis. Clin. Microbiol. Rev. 2011, 24, 682–700. |
| This material may be protected under Copyright Act which governs the making of photocopies or reproductions of copyrighted materials. You may use the digitized material for private study, scholarship, or research. |