DOI QR코드

DOI QR Code

Characterization of Novel Trichoderma asperellum Isolates to Select Effective Biocontrol Agents Against Tomato Fusarium Wilt

  • El_Komy, Mahmoud H. (Department of Plant Protection, College of Food and Agricultural Sciences, King Saud University) ;
  • Saleh, Amgad A. (Department of Plant Protection, College of Food and Agricultural Sciences, King Saud University) ;
  • Eranthodi, Anas (Department of Plant Protection, College of Food and Agricultural Sciences, King Saud University) ;
  • Molan, Younes Y. (Department of Plant Protection, College of Food and Agricultural Sciences, King Saud University)
  • 투고 : 2014.09.02
  • 심사 : 2014.10.14
  • 발행 : 2015.03.01

초록

The use of novel isolates of Trichoderma with efficient antagonistic capacity against Fusarium oxysporum f. sp. lycopersici (FOL) is a promising alternative strategy to pesticides for tomato wilt management. We evaluated the antagonistic activity of 30 isolates of T. asperellum against 4 different isolates of FOL. The production of extracellular cell wall degrading enzymes of the antagonistic isolates was also measured. The random amplified polymorphic DNA (RAPD) method was applied to assess the genetic variability among the T. asperellum isolates. All of the T. asperellum isolates significantly reduced the mycelial growth of FOL isolates but the amount of growth reduction varied significantly as well. There was a correlation between the antagonistic capacity of T. asperellum isolates towards FOL and their lytic enzyme production. Isolates showing high levels of chitinase and ${\beta}$-1,3-glucanase activities strongly inhibited the growth of FOL isolates. RAPD analysis showed a high level of genetic variation among T. asperellum isolates. The UPGMA dendrogram revealed that T. asperellum isolates could not be grouped by their antagonistic behavior or lytic enzymes production. Six isolates of T. asperellum were highly antagonistic towards FOL and potentially could be used in commercial agriculture to control tomato wilt. Our results are consistent with the conclusion that understanding the genetic variation within Trichoderma isolates and their biochemical capabilities are required for the selection of effective indigenous fungal strains for the use as biocontrol agents.

키워드

참고문헌

  1. Abo-Elyousr, K. A. M., Sobhy, I., Abdel-Hafez, I. and Abdel-Rahim, I. 2014. Isolation of Trichoderma and evaluation of their antagonistic potential against Alternaria porri. J. Phytpathol. 162:567-574. https://doi.org/10.1111/jph.12228
  2. Anderson, J. A., Churchill, G. A., Autrique, J. E., Tanksley, S. D. and Sorrells, M. E. 1993. Optimizing parental selection for genetic linkage maps. Genome 36:181-186. https://doi.org/10.1139/g93-024
  3. Arisan-Atac, I., Heidenreich, E. and Kubicek, C. P. 1995. Randomly amplified polymorphic DNA fingerprinting identifies subgroups of Trichoderma viride and other Trichoderma sp. capable of chestnut blight biocontrol. FEMS Microbiol. Lett. 126:249-256. https://doi.org/10.1111/j.1574-6968.1995.tb07426.x
  4. Avis, T. J., Hamelin, R. C. and Belanger, R. R. 2001. Approaches to molecular characterization of fungal biocontrol agents: some case studies. Can. J. Plant Pathol. 23:8-12. https://doi.org/10.1080/07060660109506902
  5. Benitez, T., Rincon, A. M., Limon, M. C. and Codon, A. C. 2004. Biocontrol mechanisms of Trichoderma strains. Int. Microbiol. 7:249-260.
  6. Chaverri, P., Castlebury, L. A., Samuels, C. J. and Geiser, D. M. 2003. Multi locus phylogenetic structure within the Trichoderma harzianum/Hypocrea lixii complex. Mol. Phylogenet. Evol. 27:302-313. https://doi.org/10.1016/S1055-7903(02)00400-1
  7. Chet, I. and Inbar, J. 1994. Biological control of fungal pathogens. Appl. Biochem. Biotechnol. 48:37-43. https://doi.org/10.1007/BF02825358
  8. Consolo, V. F., Monaco, C. I., Cordo, C. A. and Salerno, G. L. 2012. Characterization of novel Trichoderma spp. isolates as a search for effective biocontrollers of fungal diseases of economically important crops in Argentina. World J. Microbiol. Biotechnol. 28:1389-1398. https://doi.org/10.1007/s11274-011-0938-5
  9. Cook, R. J. 1993. Making greater use of introduced micro-organisms for biological control of plant pathogens. Annu. Rev. Phytopathol. 31:53-80. https://doi.org/10.1146/annurev.py.31.090193.000413
  10. Cotxarrera, L., Trillas-Gay, M. I., Steinberg, C. and Alabouvette, C. 2002. Use of sewage sludge compost and Trichoderma asperellum isolates to suppress Fusarium wilt of tomato. Soil Biol. Biochem. 34:467-476. https://doi.org/10.1016/S0038-0717(01)00205-X
  11. Dana, M. M., Limon, M. C., Mejias, R., Mach, R. L., Benitez, T., Pintor-Toro, J. A. and Kubicek, C. P. 2001. Regulation of chitinase 33 (chit33) gene expression in Trichoderma harzianum. Curr. Genet. 38:335-342. https://doi.org/10.1007/s002940000169
  12. de los Santos-Villalobos, S., Guzman-Ortiz, D. A., Gomez-Lim, M. A., Delano-Frier, J. P., de-Folter, S., Sanchez-Garia, P. and Pena-Cabriales, J. J. 2013. Potential use of Trichoderma asperellum (Samuels, Liechfeldt et Nirenberg) T8a as a biological control agent against anthracnose in mango (Mangifera indica L.). Biol. Control 64:37-44. https://doi.org/10.1016/j.biocontrol.2012.10.006
  13. Dubey, S. C., Suresh, M. and Singh, B. 2007. Evaluation of Trichoderma species against Fusarium oxysporum f.sp. ciceris for integrated management of chickpea wilt. Biol. Control 40:118-127. https://doi.org/10.1016/j.biocontrol.2006.06.006
  14. Edington, L. V., Khew, K. L. and Barron, G. I. 1971. Fungitoxic spectrum of benzimidazole compounds. Phytopathology 61:42-44. https://doi.org/10.1094/Phyto-61-42
  15. Elad, Y. and Chet, I. 1983. Improved selective media for isolation of Trichoderma spp. or Fusarium spp. Phytoparasitica 11:55-58. https://doi.org/10.1007/BF02980712
  16. El-Hasan, A., Walker, F. and Buchenauer, H. 2008. Trichoderma harzianum and its metabolite 6-Pentyl-alpha-pyrone suppress fusaric acid produced by Fusarium moniliforme. J. Phytopathol. 156:79-87. https://doi.org/10.1111/j.1439-0434.2007.01330.x
  17. El-Katatny, M. H., Somitsch, W., Robra, K. H., El-Katatny, M. S. and Gubitz, G. M. 2000. Production of Chitinase and ${\beta}$-1,3 glucanase by Trichoderma harzianum for Control of the Phytopathogenic Fungus Sclerotium rolfsii. Food Technol. Biotechnol. 38:173-180.
  18. Gajera, H. P. and Vakharia, D. N. 2010. Molecular and biochemical characterization of Trichoderma isolates inhibiting a phytopathogenic fungi Aspergillus niger Van Tieghem. Physiol. Mol. Plant P. 74:274-282. https://doi.org/10.1016/j.pmpp.2010.04.005
  19. Goes, L. B., Costa, A. B. L., Freire, L. L. C. and Oliveria, N. T. 2002. Randomly amplified polymorphic DNA of Trichoderma isolates and antagonism against Rhizoctonia solani. Braz. Arch. Biol. Technol. 45:151-160. https://doi.org/10.1590/S1516-89132002000500021
  20. Gomez, K. A. and Gomez, A. A. 1984. Statistical Procedures for Agricultural Research, 2nd edn. John Wiley, New York. 680pp.
  21. Gromovykh, T. I., Litovka, Y. A., Gromovykh, V. S. and Makhova, E. G. 2002. Effect of strain Trichoderma asperellum (MG-97) towards fusarioses of Larix sibirica seedlings. Mik Fitopatol. 36:70-75.
  22. Harman, G. E. 2000. Myths and dogmas of biocontrol, Changes in perceptions derived from research on Trichoderma harzianum T- 22. Plant Dis. 84:377-393. https://doi.org/10.1094/PDIS.2000.84.4.377
  23. Hermosa, M. R., Grondona, I., Iturriaga, E. A., Diaz-Minguez, J. M., Castro, C., Monte, E. and Garcia-Acha, I. 2000. Molecular characterization and identification of biocontrol isolates of Trichoderma spp. Appl. Environ. Microbiol. 66:1890-1898. https://doi.org/10.1128/AEM.66.5.1890-1898.2000
  24. Howell, C. R. 2003. Mechanisms employed by Trichoderma species in the biological control of plant diseases, the history and evolution of current concepts. Plant Dis. 87:4-10. https://doi.org/10.1094/PDIS.2003.87.1.4
  25. Jones, J. B., Jones, J. P., Stall, R. E. and Zitter, T. A. 1991. Compendium of tomato diseases. American Phytopathological Society, St. Paul, MN.
  26. Kim, T. G. and Knudsen, G. R. 2013. Relationship between the biocontrol fungus Trichoderma harzianum and the phytopathogenic fungus Fusarium solani f.sp. pisi. Appl. Soil Ecol. 68:57-60. https://doi.org/10.1016/j.apsoil.2013.03.009
  27. Kubicek, C. P., Mach, R. L., Peterbauer, C. K. and Lorito, M. 2001. Trichoderma: from genes to biocontrol. J. Plant Pathol. 83:11-23.
  28. Kullnig, C., Mach, R. L., Lorito, M. and Kubicek, C. P. 2000. Enzyme diffusion from Trichoderma atroviride (T. harzianum P1) to Rhizoctonia solani is a prerequisite for triggering of Trichoderma ech42 gene expression before mycoparasitic contact. Appl. Environ. Microbiol. 66:2232-2234. https://doi.org/10.1128/AEM.66.5.2232-2234.2000
  29. Larkin, R. P. and Fravel, D. R. 1998. Efficacy of various fungal and bacterial biocontrol organisms for control of Fusarium wilt of tomato. Plant Dis. 82:1022-1028. https://doi.org/10.1094/PDIS.1998.82.9.1022
  30. Leslie, J. F. Summerell, B. A. 2006. The Fusarium Laboratory Manual. Blackwell Publishing, Iowa, USA. 388pp.
  31. Lopes, F. A. C., Stendorff, A. S., Geraldine, A. M., Brandao, R. S., Monteiro, V. N., Junior, M. L., Coelho, A. S. G., Ulhon, C. J. and Silva, R. N. 2012. Biochemical and metabolic profiles of Trichoderma strains isolated from common bean crops in the Brazilian Cerrado, and potential antagonism against Sclerotinia sclerotiorum. Fungal Biol. 116:815-824. https://doi.org/10.1016/j.funbio.2012.04.015
  32. Lutz, M. P., Feichtinger, G., Defago, G. and Duffy, B. 2003. Mycotoxigenic Fusarium and deoxynivalenol production repress chitinase gene expression in the biocontrol agent Trichoderma atroviride P1. Appl. Environ. Microbiol. 69:3077-3084. https://doi.org/10.1128/AEM.69.6.3077-3084.2003
  33. Mantel, N. 1967. The detection of disease clustering and a generalized regression approach. Cancer. Res. 27:209-220.
  34. Marcello, C. M., Steindorff, A. S., Silva, S. P., Silva, R. N., Bataus, L. A. M. and Ulhoa, C. J. 2010. Expression analysis of the exo-${\beta}$-1,3-glucanase from the mycoparasitic fungus Trichoderma asperellum. Microbiol. Res. 165:75-81. https://doi.org/10.1016/j.micres.2008.08.002
  35. Markovich, N. A. and Kononova, G. L. 2003. Lytic enzymes of Trichoderma and their role in plant defense from fungal diseases, a review. Appl. Biochem. Microbiol. 39:389-400.
  36. Meyer, S. F. M. and Roberts, D. P. 2002. Combinations of biocontrol agents for management of plant-parasitic nematodes and soilborne plant pathogenic fungi. J. Nematol. 34:1-8.
  37. Miller, G. L. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal. Chem. 31:426-428. https://doi.org/10.1021/ac60147a030
  38. Molano, J., Duram, A. and Cabib, E. 1977. A rapid and sensitive assay for chitinase using tritiated chitin. Anal. Biochem. 83:648-656. https://doi.org/10.1016/0003-2697(77)90069-0
  39. Mondejar, R. L., Ros, M. and Pascual, J. A. 2011. Mycoparasitism-related genes expression of Trichoderma harzianum isolates to evaluate their efficacy as biological control agent. Biol. Control 56:59-66. https://doi.org/10.1016/j.biocontrol.2010.10.003
  40. Monte, E. 2001. Understanding Trichoderma, between biotechnology and microbial ecology. Int. Microbiol. 4:1-4.
  41. Morton, D. J. and Stroube, W. H. 1955. Antagonistic and stimulating effects of soil micro-organism of Sclerotium. Phytopathol. 45:417-420.
  42. Mukherjee, M., Mukherjee, P. K., Horwitz, B. A., Zachow, C., berg, G. and Zeilinger, S. 2012. Trichoderma-Plant-Pathogen Interactions: Advances in Genetics of Biological Control. Indian J. Microbiol. 52:522-529. https://doi.org/10.1007/s12088-012-0308-5
  43. Muthumeenakshi, S., Mills, P. R., Brown, A. E. and Seaby, D. A. 1994. Intraspecific molecular variation among Trichoderma harzianum isolates colonizing mushroom compost in the British Isles. Microbiology 140:769-777. https://doi.org/10.1099/00221287-140-4-769
  44. Qualhato, F. T., Lopes, F. A. C., Steindorff, A. S., Brandao, R. S., Jesuino, R. S. A. and Ulhoa, C. J. 2013. Mycoparasitism studies of Trichoderma species against three phytopathogenic fungi: evaluation of antagonism and hydrolytic enzyme production. Biotechnol. Lett. 35:1461-1468. https://doi.org/10.1007/s10529-013-1225-3
  45. Raeder, U. and Broda, P. 1985. Rapid preparation of DNA from filamentous fungi. Lett. Appl. Microbiol. 1:17-20. https://doi.org/10.1111/j.1472-765X.1985.tb01479.x
  46. Rolf, F. J. 1993. NTSYS-pc Numerical Taxonomy and Multivariate Analysis System, Version 1.8. Exeter Software, Setauket, New York, USA.
  47. Saber, W. I. A., Abd El-Hai, K. M. and Ghoneem, K. M. 2009. Synergistic effect of Trichoderma and Rhizobium on Both Biocontrol of chocolate spot disease and induction of nodulation, physiological activities and productivity of Vicia faba. Res. J. Microbiol. 4:286-300. https://doi.org/10.3923/jm.2009.286.300
  48. Sambrook, H., Fritch, J. and Maniatis, T. 1989. Molecular cloning, A laboratory manual, 2ed Ed., Cold Spring Harbor Laboratory, New York.
  49. SAS Institute Inc., 2003. SAS/STATA Guide for Personal Computers Version 9.1 edition. SAS Institute, Carry NC, USA.
  50. Segarra, G., Casanova, E., Aviles, M. and Trillas, I. 2010. Trichoderma apserellum strain T34 controls Fusarium wilt disease in tomato plants in soilless culture through competition for iron. Microb. Ecol. 59:141-149. https://doi.org/10.1007/s00248-009-9545-5
  51. Sharma, P. 2011. Complexity of Trichoderma-Fusarium interaction and manifestation of biological control. Aust. J. Crop Sci. 5:1027-1038.
  52. Sharma, K., Mishira, A. K. and Misra, R. S. 2009. Morphological, biochemical and molecular characterization of Trichoderma harzianum isolates for their efficacy as biocontrol agents. J. Phytopathol. 157:51-56. https://doi.org/10.1111/j.1439-0434.2008.01451.x
  53. Simon, C. and Sivasithaparam, M. 1988. Interaction among Gaeumannomyces graminum var. tritci, Trichoderma koningii and soil bacteria. Can. J. Microbiol. 34:871-876. https://doi.org/10.1139/m88-150
  54. Sivan, A. and Chet, I. 1989. Degradation of fungal cell walls by lytic enzymes of Trichoderma harzianum. J. General Microbiol. 135:675-682.
  55. Tondje, P. R., Roberts, D. P., Bon, M. C., Widmer, T., Samuels, G. J., Ismaiel, A., Begoude, A. D., Tchana, T., Nyemb-Tshomb, E., Ndoumbe-Nkeng, M., Bateman, R., Fontem, D. and Hebbar, K. P. 2007. Isolation and identification of mycoparasitic isolates of Trichoderma asperellum with potential for suppression of black pod disease of cacao in Cameroon. Biol. Control 43:202-212. https://doi.org/10.1016/j.biocontrol.2007.08.004
  56. Trillas, M. I., Casanova, E., Cotxarrera, L., Ordovas, J., Borrero, C. and Aviles, M. 2006. Composts from agricultural waste and the Trichoderma asperellum strain T-34 suppress Rhizoctonia solani in cucumber seedlings. Biol. Control 39:32-38. https://doi.org/10.1016/j.biocontrol.2006.05.007
  57. Verma, M., Brar, S. K., Tyagi, R. D., Surampalli, R. Y. and Valero, J. R. 2007. Antagonistic fungi, Trichoderma spp., Panoply of biological control. Biochemical Engineering Journal 37:1-20. https://doi.org/10.1016/j.bej.2007.05.012
  58. Viterbo, A., Ramot, O., Chermin, L. Y. and Chet, I. 2002. Significance of lytic enzymes from Trichoderma spp. in the biocontrol of fungal plant pathogens. Antonie van Leeuwenhoek 81:549-556. https://doi.org/10.1023/A:1020553421740
  59. Williams, J. G. K., Kubelik, A. R., Livak, K. J., Rafalski, J. A. and Tingey, S. V. 1990. DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic. Acids Res. 18:6531-6535. https://doi.org/10.1093/nar/18.22.6531
  60. Woo, S. L., Scala, F., Ruocco, M. and Lorito, M. 2006. The molecular biology of the interactions between Trichoderma spp., phytopathogenic fungi, and plants. Phytopathology 96:181-185. https://doi.org/10.1094/PHYTO-96-0181
  61. Zhang, F., Zhu, Z., Yang, X., Ran, W. and Shen, Q. 2013. Trichoderma harzianum T-E5 significantly affects cucumber root exudates and fungal community in the cucumber rhizosphere. Appl. Soil Ecol. 72:41-48. https://doi.org/10.1016/j.apsoil.2013.05.016

피인용 문헌

  1. Trichoderma as biostimulant: exploiting the multilevel properties of a plant beneficial fungus vol.196, 2015, https://doi.org/10.1016/j.scienta.2015.08.043
  2. Biocontrol efficacy of Trichoderma asperellum MSST against tomato wilting by Fusarium oxysporum f. sp. lycopersici vol.50, pp.5-6, 2017, https://doi.org/10.1080/03235408.2017.1287236
  3. Trichoderma asperellum Induces Maize Seedling Growth by Activating the Plasma Membrane H+-ATPase vol.29, pp.10, 2016, https://doi.org/10.1094/MPMI-07-16-0138-R
  4. Trichoderma asperellum strains confer tomato protection and induce its defense-related genes against the Fusarium wilt pathogen vol.41, pp.5, 2016, https://doi.org/10.1007/s40858-016-0098-0
  5. Crop molds and mycotoxins: Alternative management using biocontrol vol.104, 2017, https://doi.org/10.1016/j.biocontrol.2016.10.004
  6. Identification, characterization and phylogenetic analysis of antifungal Trichoderma from tomato rhizosphere vol.5, pp.1, 2016, https://doi.org/10.1186/s40064-016-3657-4
  7. Secretome analysis of Trichoderma atroviride T17 biocontrol of Guignardia citricarpa vol.99, 2016, https://doi.org/10.1016/j.biocontrol.2016.04.009
  8. Trichoderma harzianum T1A constitutively secretes proteins involved in the biological control of Guignardia citricarpa vol.106, 2017, https://doi.org/10.1016/j.biocontrol.2017.01.003
  9. Isolation, Identification And Screening Antibacterial Activity from Marine Sponge-Associated Fungi Against Multidrug-Resistant (MDR)Escherichia coli vol.55, 2017, https://doi.org/10.1088/1755-1315/55/1/012028
  10. Biocontrol potential of Trichoderma harzianum isolate T-aloe against Sclerotinia sclerotiorum in soybean vol.100, 2016, https://doi.org/10.1016/j.plaphy.2015.12.017
  11. Fingerprinting and molecular comparison among two parental strains ofTrichodermaspp. and their corresponding fusants produced by protoplast fusion 2016, https://doi.org/10.1080/13102818.2016.1230478
  12. Antagonistic and Biocontrol Potential of Trichoderma asperellum ZJSX5003 Against the Maize Stalk Rot Pathogen Fusarium graminearum vol.56, pp.3, 2016, https://doi.org/10.1007/s12088-016-0581-9
  13. Trichoderma harzianum-induced resistance against Fusarium oxysporum involves regulation of nuclear DNA content, cell viability and cell cycle-related genes expression in cucumber roots vol.147, pp.1, 2017, https://doi.org/10.1007/s10658-016-0978-7
  14. Distribution and Genetic Variability of Fusarium oxysporum Associated with Tomato Diseases in Algeria and a Biocontrol Strategy with Indigenous Trichoderma spp. vol.9, pp.1664-302X, 2018, https://doi.org/10.3389/fmicb.2018.00282
  15. Trichoderma asperellum isolated from African maize seed directly inhibits Fusarium verticillioides growth in vitro pp.1573-8469, 2019, https://doi.org/10.1007/s10658-018-1530-8
  16. SN16-1 on the rhizosphere bacterial community and growth of tomato vol.166, pp.5, 2018, https://doi.org/10.1111/jph.12690
  17. Fungal Biodiversity and Their Role in Soil Health vol.9, pp.1664-302X, 2018, https://doi.org/10.3389/fmicb.2018.00707