DOI QR코드

DOI QR Code

Broad-Spectrum Activity of Volatile Organic Compounds from Three Yeast-like Fungi of the Galactomyces Genus Against Diverse Plant Pathogens

  • Cai, Shu-Ting (Department of Biology, National Changhua University of Education) ;
  • Chiu, Ming-Chung (Department of Biology, National Changhua University of Education) ;
  • Chou, Jui-Yu (Department of Biology, National Changhua University of Education)
  • 투고 : 2020.08.23
  • 심사 : 2020.11.23
  • 발행 : 2021.02.28

초록

The application of antagonistic fungi for plant protection has attracted considerable interest because they may potentially replace the use of chemical pesticides. Antipathogenic activities confirmed in volatile organic compounds (VOCs) from microorganisms have potential to serve as biocontrol agents against pre- and post-harvest diseases. In the present study, we investigated Galactomyces fungi isolated from rotten leaves and the rhizosphere of cherry tomato (Lycopersicon esculentum var. cerasiforme). VOCs produced by Galactomyces fungi negatively affected the growth of phytopathogenic fungi and the survival of nematodes. Mycelial growths of all nine examined phytopathogenic fungi were inhibited on agar plate, although the inhibition was more intense in Athelia rolfsii JYC2163 and Cladosporium cladosporioides JYC2144 and relatively moderate in Fusarium sp. JYC2145. VOCs also efficiently suppressed the spore germination and mycelial growth of A. rolfsii JYC2163 on tomatoes. The soil nematode Caenorhabditis elegans exhibited higher mortality in 24 h in the presence of VOCs. These results suggest the broad-spectrum activity of Galactomyces fungi against various plant pathogens and the potential to use VOCs from Galactomyces as biocontrol agents.

키워드

참고문헌

  1. 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. https://doi.org/10.1016/j.tifs.2015.11.003
  2. Carmona-Hernandez S, Reyes-Perez JJ, Chiquito-Contreras RG, et al. Biocontrol of postharvest fruit fungal diseases by bacterial antagonists: a review. Agronomy. 2019;9:121. https://doi.org/10.3390/agronomy9030121
  3. Freimoser FM, Rueda-Mejia MP, Tilocca B, et al. Biocontrol yeasts: mechanisms and applications. World J Microbiol Biotechnol. 2019;35:154. https://doi.org/10.1007/s11274-019-2728-4
  4. Morath SU, Hung R, Bennett JW. Fungal volatile organic compounds: a review with emphasis on their biotechnological potential. Fungal Biol Rev. 2012;26:73-83. https://doi.org/10.1016/j.fbr.2012.07.001
  5. Minerdi D, Bossi S, Gullino ML, et al. Volatile organic compounds: a potential direct long-distance mechanism for antagonistic action of Fusarium oxysporum strain MSA 35. Environ Microbiol. 2009;11:844-854. https://doi.org/10.1111/j.1462-2920.2008.01805.x
  6. Cernava T, Aschenbrenner IA, Grube M, et al. A novel assay for the detection of bioactive volatiles evaluated by screening of lichen-associated bacteria. Front Microbiol. 2015;6:398. https://doi.org/10.3389/fmicb.2015.00398
  7. Irtwange SV. Application of biological control agents in pre- and postharvest operations. Int J Agric Eng. 2006;8:1-12.
  8. Eayre CG, Skaria M, Bull CT, et al. An avirulent Galactomyces species that controls green mold of citrus caused by Penicillium digitatum. Subtrop Plant Sci. 2003;55:46-50.
  9. McKay AH, Forster H, Adaskaveg JE. Toxicity and € resistance potential of selected fungicides to Galactomyces and Penicillium spp. causing postharvest fruit decays of citrus and other crops. Plant Dis. 2012;96:87-96. https://doi.org/10.1094/PDIS-06-11-0466
  10. Schisler DA, Janisiewicz WJ, Boekhout T, et al. Agriculturally important yeasts: biological control of field and postharvest diseases using yeast antagonists, and yeasts as pathogens of plants. In: Kurtzman CP, Fell JW, Boekhout T, editors. The yeasts. 4th ed. Amsterdam (The Netherlands): Elsevier; 2011. p. 45-52.
  11. Chen PH, Chen RY, Chou JY. Screening and evaluation of yeast antagonists for biological control of Botrytis cinerea on strawberry fruits. Mycobiology. 2018;46:33-46. https://doi.org/10.1080/12298093.2018.1454013
  12. Zhang L, Khabbaz SE, Wang A, et al. Detection and characterization of broad-spectrum antipathogen activity of novel rhizobacterial isolates and suppression of Fusarium crown and root rot disease of tomato. J Appl Microbiol. 2015;118: 685-703. https://doi.org/10.1111/jam.12728
  13. Silva JCP, Campos VP, Barros AF, et al. Plant volatiles reduce the viability of the root-knot nematode Meloidogyne incognita either directly or when retained in water. Plant Dis. 2018;102:2170-2179. https://doi.org/10.1094/PDIS-01-18-0143-RE
  14. Freire ES, Campos VP, Pinho RSC, et al. Volatile substances produced by Fusarium oxysporum from coffee rhizosphere and other microbes affect Meloidogyne incognita and Arthrobotrys conoides. J Nematol. 2012;44:321-328.
  15. Riedel RM. Interactions of plant-parasitic nematodes with soil-borne plant pathogens. Agric Ecosyst Environ. 1988;24:281-292. https://doi.org/10.1016/0167-8809(88)90072-2
  16. Akhtar M, Malik A. Roles of organic soil amendments and soil organisms in the biological control of plant-parasitic nematodes: a review. Bioresour Technol. 2000;74:35-47. https://doi.org/10.1016/S0960-8524(99)00154-6
  17. Oka Y, Koltai H, Bar-Eyal M, et al. New strategies for the control of plant-parasitic nematodes. Pest Manag Sci. 2000;56:983-988. https://doi.org/10.1002/1526-4998(200011)56:11<983::AID-PS233>3.0.CO;2-X
  18. McSorley R. Overview of organic amendments for management of plant-parasitic nematodes, with case studies from Florida. J Nematol. 2011;43: 69-81.
  19. Fuhrich DG, Lessey BA, Savaris RF. Comparison of HSCORE assessment of endometrial beta3 integrin subunit expression with digital HSCORE using computerized image analysis *(ImageJ). Anal Quant Cytopathol Histpathol. 2013;35:210-216.
  20. Michereff SJ, Silveira NSS, Reis A, et al. Epiphytic bacteria antagonistic to Curvularia leaf spot of yam. Microb Ecol. 1994;28:101-110. https://doi.org/10.1007/BF00170250
  21. Huang R, Li GQ, Zhang J, et al. Control of postharvest Botrytis fruit rot of strawberry by volatile organic compounds of Candida intermedia. Phytopathology. 2011;101:859-869. https://doi.org/10.1094/PHYTO-09-10-0255
  22. R Core Team. R: a language and environment for statistical computing. Vienna (Austria): R Foundation for Statistical Computing; 2019. Available from: https://www.r-project.org/
  23. Knudsen GR, Dandurand LMC. Ecological complexity and the success of fungal biological control agents. Adv Agric. 2014;2014:1-11.
  24. Sacristan N, Gonzalez L, Castro JM, et al. Technological characterization of Geotrichum candidum strains isolated from a traditional Spanish goats' milk cheese. Food Microbiol. 2012;30:260-266. https://doi.org/10.1016/j.fm.2011.10.003
  25. Grondin E, Sing ASC, James S, et al. Flavour production by Saprochaete and Geotrichum yeasts and their close relatives. Food Chem. 2017;237:677-684. https://doi.org/10.1016/j.foodchem.2017.06.009
  26. Pretscher J, Fischkal T, Branscheidt S, et al. Yeasts from different habitats and their potential as biocontrol agents. Fermentation. 2018;4:31. https://doi.org/10.3390/fermentation4020031
  27. Frezal L, Jacqua G, Neema C. Adaptation of a fungal pathogen to host quantitative resistance. Front Plant Sci. 2018;9:1554. https://doi.org/10.3389/fpls.2018.01554
  28. Le May C, Montarry J, Morris CE, et al. Editorial: plant pathogen life-history traits and adaptation to environmental constraints. Front Plant Sci. 2020;10:1730. https://doi.org/10.3389/fpls.2019.01730
  29. Gubler WD, Feliciano CJ, Bordas AC, et al. X. fragariae and C. cladosporioides cause strawberry blossom blight. Calif Agr. 1999;53:26-28.
  30. Nam MH, Park MS, Kim HS, et al. Cladosporium cladosporioides and C. tenuissimum cause blossom blight in strawberry in Korea. Mycobiology. 2015;43:354-359. https://doi.org/10.5941/MYCO.2015.43.3.354
  31. Robles-Yerena L, Ayala-Escobar V, Leyva-Mir SG, et al. First report of Cladosporium cladosporioides causing leaf spot on tomato in Mexico. J Plant Pathol. 2019;101:759-759. https://doi.org/10.1007/s42161-018-00218-x
  32. Wang X, Radwan MM, Tarawneh AH, et al. Antifungal activity against plant pathogens of metabolites from the endophytic fungus Cladosporium cladosporioides. J Agric Food Chem. 2013;61:4551-4555. https://doi.org/10.1021/jf400212y
  33. Paynter Q, Hennecke B. Competition between two biological control agents, Neurostrota gunniella and Phloeospora mimosae-pigrae, and their impact on the invasive tropical shrub Mimosa pigra. Biocontrol Sci Technol. 2001;11:575-582. https://doi.org/10.1080/09583150120076139
  34. Osemwegie OO, Oghenekaro AO, Owolo LO. Effects of pulverized Ganoderma spp., on Sclerotium rolfsii Sacc and post-harvest tomato (Lycopersicon esculentum Mill.) fruits preservation. J Appl Sci Res. 2010;6:1794-1800.
  35. Jia XH, Fu JF, Wang WH, et al. First report of Athelia bombacina causing postharvest fruit rot on pear. J Integr Agric. 2018;17:2596-2599. https://doi.org/10.1016/S2095-3119(18)62091-X
  36. Dodd SL, Hill RA, Stewart A. Control of Athelia rolfsii disease on lentil seedlings using 6-pentyla-pyrone. Soil Biol Biochem. 2000;32:1033-1034. https://doi.org/10.1016/S0038-0717(00)00003-1
  37. El-Hasan A, Walker F, Sch€one J, et al. Antagonistic effect of 6-pentyl-alpha-pyrone produced by Trichoderma harzianum toward Fusarium moniliforme. J Plant Dis Prot. 2007;114:62-68. https://doi.org/10.1007/BF03356205
  38. Riga E. The effects of Brassica green manures on plant parasitic and free living nematodes used in combination with reduced rates of synthetic nematicides. J Nematol. 2011;43:119-121.
  39. Casas-Flores S, Herrera-Estrella A. Antagonism of plant parasitic nematodes by fungi. In: Kubicek CP, Druzhinina IS, editors. Environmental and microbial relationships. The Mycota. Vol. 4. Heidelberg: Springer; 2007. p. 147-157.
  40. Moosavi MR, Zare R. Fungi as biological control agents of plant-parasitic nematodes. In: Merillon J, Ramawat K, editors. Plant defence: biological control. Progress in biological control. Vol. 12. Dordrecht: Springer; 2012. p. 67-107.
  41. Favre-Bonvin J, Ponchet M, Djian C, et al. Acetic acid: a selective nematicidal metabolite from culture filtrates of Paecilomyces lilacinus (Thom) Samson and Trichoderma longibrachiatum Rifai. Nematology. 1991;37:101-112. https://doi.org/10.1163/187529291X00105
  42. Kwok OCH, Plattner R, Weisleder D, et al. A nematicidal toxin from Pleurotus ostreatus NRRL 3526. J Chem Ecol. 1992;18:127-136. https://doi.org/10.1007/BF00993748
  43. Hallmann J, Sikora RA. Occurrence of plant parasitic nematodes and non-pathogenic species of Fusarium in tomato plants in Kenya and their role as mutualistic synergists for biological control of root-knot nematodes. Int J Pest Manage. 1994;40:321-325. https://doi.org/10.1080/09670879409371907