International Journal of Innovative Approaches in Agricultural Research
Abbreviation: IJIAAR | ISSN (Online): 2602-4772 | DOI: 10.29329/ijiaar

Original article | International Journal of Innovative Approaches in Agricultural Research 2018, Vol. 2(3) 226-243

Fungicide Tolerance and Effect of Environmental Conditions on Growth of Trichoderma spp. with Antagonistic Activity Against Sclerotinia sclerotiorum Causing White Mold of Common Bean (Phaseolus vulgaris)

Marie Amperes Bedıne Boat, Beatrice Iacomı, Modeste Lambert Sameza & Fabrice Fekam Boyom

pp. 226 - 243   |  DOI:

Published online: September 26, 2018  |   Number of Views: 146  |  Number of Download: 412


The present study was conducted to evaluate in vitro compatibility of commonly used agrochemicals as well as the effect of temperature, pH and salt on the growth of six Trichoderma spp. with antagonistic activity against S. sclerotiorum responsible for white mold of common bean. The results revealed that in dual culture, the mycelial growth inhibition of S. sclerotiorum ranged from 83.4 to 87.4 %.  The highest inhibition (87.4 %) was obtained with isolate T. erinaceum It-58, while the lowest inhibition (83.4 %) was caused by T. koningiopsis It-21.  Except T. asperellum It-13, antagonistic fungi were able to fully colonized pathogen in five days reaching class I antagonism according to Bell scale. The maximum inhibition percentage of volatile (54.07 %) and non-volatile compounds (68.89 %) on pathogen was respectively caused by T. asperellum It-13 and T. harzianum P-11. Fungicides affect the growth of Trichoderma differently. No growth was observed while testing compatibility of T. asperellum It-13 and T. erinaceum It-58 with Mancozeb as well as T. asperellum It-13 and T. afroharzianum P-8 with Methyl thiophanate illustrating the absence of compatibility. The excellent growth rate of Trichoderma was found at temperature range of 25–30˚C and pH range 4.5-5.5. Apart from T. asperellum It-13, all the isolates were able to grow at NaCl concentrations up to 1000 µM and were identified as superior salt-tolerant isolates.

Keywords: Antagonistic, S. sclerotiorum, Trichoderma, biological control, fungicide tolerance.

How to Cite this Article?

APA 6th edition
Boat, M.A.B., Iacomi, B., Sameza, M.L. & Boyom, F.F. (2018). Fungicide Tolerance and Effect of Environmental Conditions on Growth of Trichoderma spp. with Antagonistic Activity Against Sclerotinia sclerotiorum Causing White Mold of Common Bean (Phaseolus vulgaris). International Journal of Innovative Approaches in Agricultural Research, 2(3), 226-243. doi: 10.29329/ijiaar.2018.151.8

Boat, M., Iacomi, B., Sameza, M. and Boyom, F. (2018). Fungicide Tolerance and Effect of Environmental Conditions on Growth of Trichoderma spp. with Antagonistic Activity Against Sclerotinia sclerotiorum Causing White Mold of Common Bean (Phaseolus vulgaris). International Journal of Innovative Approaches in Agricultural Research, 2(3), pp. 226-243.

Chicago 16th edition
Boat, Marie Amperes Bedine, Beatrice Iacomi, Modeste Lambert Sameza and Fabrice Fekam Boyom (2018). "Fungicide Tolerance and Effect of Environmental Conditions on Growth of Trichoderma spp. with Antagonistic Activity Against Sclerotinia sclerotiorum Causing White Mold of Common Bean (Phaseolus vulgaris)". International Journal of Innovative Approaches in Agricultural Research 2 (3):226-243. doi:10.29329/ijiaar.2018.151.8.

  1. Abo-Elyousr, K. A. M., I. Sobhy, I. Abdel-Hafez and I. Abdel-Rahim (2014). Isolation of Trichoderma and evaluation of their antagonistic potential against Alternaria porri. J. Phytopath., 162, 567-574.   [Google Scholar]
  2. Agrios, G. N (2005). Plant Pathology (5th Ed.). Elsevier Academic Press, Burlington. [Google Scholar]
  3. Akrami, M., G. Hadi and A. Masoud (2011). Evaluation of different combinations of Trichoderma species for controlling Fusarium rot of lentil. Afr. J. Biotech., 10(14), 2653-2658. [Google Scholar]
  4. Anthony, A. (1998). Molecular biology of salt tolerance in the context of whole-plant physiology. J. Exp. Bot., 49, 915-929. [Google Scholar]
  5. Baker, R and T. C. Paulitz (1996). Theoretical basis for microbial interactions leading to biological control of soil borne plant pathogens In: Hall R., (ed.). Principles and Practice of Managing Soilborne Plant Pathogens. Am. Phytopathol. Soc. St. Paul, MN. pp. 50-79. [Google Scholar]
  6. Belanger, R. R., N. Dufour, J. Caron and N. Benhamou (1995). Chronological events associated with the antagonistic properties of Trichoderma harzianum against Botrytis cinerea: indirect evidence for sequential role of antibiosis and parasitism. Bio. Sci. Tech., 5, 41-53. [Google Scholar]
  7. Bell, D. K., H. D. Wells and C. R. Markham (1982). In vitro antagonism of Trichoderma species against six fungal pathogens. Phytopath, 72, 379-382.   [Google Scholar]
  8. Benitez, T., A. M. Rincon, M. C. Limon and A. C. Codon (2004). Biocontrol mechanisms of Trichoderma strains. Int. J. Microbiol., 7, 249-260. [Google Scholar]
  9. Bhale, U. N. and J. N. Rajkonda (2015). Compatibility of fungicides and antagonistic activity of Trichoderma spp against plant pathogens. Biosci. Meth., 6(3), 1-9. [Google Scholar]
  10. Bheemaraya, M. B., R. Patil, K. Vendan, Y. S. Tamil and R. K, Amaresh (2012). Compatibility of Trichoderma spp. with commonly used fungicides, insecticides and plant extracts. Ind. J. Plant Prot., 40(2), 118-122. [Google Scholar]
  11. Borneman, J., P. W. Skroch and K. M. O'Sullivan (1996). Molecular microbial diversity of an agricultural soil in Wisconsin. Appl. Environ. Microbiol., 62, 1935-1943. [Google Scholar]
  12. Brito, J. P .C., H. S. Marcelo, M. T. Q. Ramada, L. P. de Magalhães and J. U. Cirano (2014). Peptaibols from Trichoderma asperellum TR356 strain isolated from Brazilian soil. Springer Plus, 3, 600-612. [Google Scholar]
  13. Chaparro, A. P., H. C. Lilliana and O. Sergio (2011). Fungicide tolerance of Trichoderma asperelloides and T. harzianum strains. Agri. Sci, 2(3), 301-307. [Google Scholar]
  14. Chet, I (1987). Trichoderma application, mode of action, and potential as biocontrol agent of soilborne plant pathogenic fungi. Innovative approaches to plant disease control. Wiley & Sons Inc., New York, NY, United State, pp. 137-160. [Google Scholar]
  15. De Castro, A. M., M. C. Ferreira, J. C. Da Cruz, K. C. Pedro, D. F. Carvalho, S. G. Leite and   [Google Scholar]
  16. J. N. Pereira (2010). High-yield endoglucanase production by Trichoderma harzianum IOC-3844 cultivated in pretreated sugarcane mill byproduct. Enz. Res., 1(1), 1-8. [Google Scholar]
  17. Dennis, C. and J. Webster (1971). Antagonistic properties of species groups of Trichoderma: I. Production of non-volatile antibiotics. Trans. Br. Mycol. Soc., 57, 25-39. [Google Scholar]
  18. Dluzneiwska, J (2003). Reaction of fungi of Trichoderma genus to selected abiotic factors, Elec. J. Pol Agri. Univ., 6 (2), 239-242. [Google Scholar]
  19. Domingues, F. M. V. P., K. E. de Moura, D. Salomão, E. L. Mecatti and R. A. P. Flávia (2015). Effect of temperature on mycelial growth of Trichoderma, Sclerotinia minor and S. sclerotiorum, as well as on mycoparasitism. Sum. Phytopath., (42), 1-5. [Google Scholar]
  20. Dubey, S. C., M. Suresh and B. Singh (2007). Evaluation of Trichoderma species against Fusarium oxysporum f.sp. ciceris for integrated management of chickpea wilt. Biol. Cont., 40, 118-127. [Google Scholar]
  21. El-Hassan, S. A., S. R. Gowen and B. Pembroke (2013). Use of Trichoderma hamatum for biocontrol of lentil vascular wilt disease: efficacy, mechanisms of interaction and future prospects. J. Plant Prot. Res., 53 (1), 12-26. [Google Scholar]
  22. El-Katatny, M. H., M. Gudelj and K. H. Robra, (2001). Characterization of a chitinase and an endo-beta-1,3-glucanase from Trichoderma harzianum Rifai T24 involved in control of the phytopathogen Sclerotium rolfsii. App. Microbiol. Biotech., 56, 137-143. [Google Scholar]
  23. Elshahawy, I. E., K. H. E. Haggag, and H. Abd-El-Khair (2016). Compatibility of Trichoderma spp. with seven chemical fungicides used in the control of soil borne plant pathogens. Res. J. Pharm. Bio. Chem. Sci., 7, 1771-1785. [Google Scholar]
  24. Gunde-Cimerman, N., J. Ramos and A. Plemenitaš (2009). Halotolerant and halophilic fungi. Myc. Res., 113, 1231-1241. [Google Scholar]
  25. Hamed Eman, R., M. A. Hassan, E. A. Ghazi, N. G. El-Gamal and H. S. Shehata (2015). Trichoderma sp. isolated from salinity soil using rice straw waste as biocontrol agent for cowpea plant pathogens. J. Appl Pharm. Sci., 5, 91-98. [Google Scholar]
  26. Harman, G. E., C. R. Howell, A. Viterbo, I. Chet, and M. Lorito (2004). Trichoderma species opportunistic avirulent plant symbionts. Nat. Rev. Microbiol., 2(1), 43–56. [Google Scholar]
  27. Hjeljord, L., and Tronsmo, A., (1998). Trichoderma and Gliocladium in biological control: An overview. In: Trichoderma and Gliocladium-Enzymes, Biological Control and Commercial Applications (Eds.: G.E. Harma and C.P. Kubicek). Taylor & Francis Ltd., London, pp. 131-151 [Google Scholar]
  28. 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. [Google Scholar]
  29. Hua, S. S. T., J. J. Beck, S. B. L. Sarreal and G., Wai (2014). The major volatile compound 2- phenylethanol from the biocontrol yeast, Pichia anomala, inhibits growth and expression of aflatoxin biosynthetic genes of Aspergilus flavus. Mycotoxin Res. 30 (2), 71–78. [Google Scholar]
  30. Kredics, L., L. Manczinger, Z. Antal, Z. Penzes, A. Szekeres, F. Kevel and E. Nagy (2004). In vitro water activity and pH dependence of mycelial growth and extracellular enzyme activities of Trichoderma strains with biocontrol potential. J. Appl. Microbiol., 96, 491-498. [Google Scholar]
  31. Kredics, L., Z. Antal, L. Manczinger, A. Szerkeres, F. Kevei and E. Nagy (2003). Influence of environmental parameters on Trichoderma strains with biocontrol potential. Food. Tech. Biotech., 41, 37-42. [Google Scholar]
  32. Manoj, K. M., S. Mukesh, S. Anuradha, P. Sonika and R. Ved (2017). Effect of different temperature and culture media on the mycelia growth of Trichoderma viride isolates. Int. J. Curr. Microbio. App. Sci., 6 (2), 266-269. [Google Scholar]
  33. Morath, S. U., R. Hung and J. W. Bennett (2012). Fungal volatile organic compounds: A review with emphasis on their biotechnological potential. Fun. Biol. Rev., 26, 73–83. [Google Scholar]
  34. Morton, D. J and W. H. Stroube (1955). Antagonistic and stimulating effects of soil microorganisms upon sclerotium. Phytopath., 45, 417-420.  [Google Scholar]
  35. Mukherjee, M., P. K. Mukherjee, B. A. Horwitz, C. Zachow, G. Berg and S. Zeilinger (2012). Trichoderma-plant pathogen interactions: advances in genetics of biological control. Ind. J. Microbiol., 52, 522-29. [Google Scholar]
  36. Nadeesha, B. S., M. Reddikumar and R. N. P. Eswara (2013). Evaluation of different fungicides and their compatibility with potential Trichoderma spp. for the management of Aspergillus niger, incitant of collar rot of groundnut. Asian. J. Biol. Life Sci., 2(1), 59-63. [Google Scholar]
  37. Nene, Y. L., and P. N., Thapliyal (1993). Fungicides in Plant Disease Control.  Oxford and IBH Publishing Co., New Delhi, India.  [Google Scholar]
  38. Parmar, H. J., N. P. Bodar, N. H. Lakhani, S. V. Patel, V. V. Umrania and M. M. Hassan (2015). Production of lytic enzymes by Trichoderma strains during in vitro antagonism with Sclerotium rolfsii, the causal agent of stem rot of groundnut. Afr. J. Microbiol. Res., 9(6), 365-372. [Google Scholar]
  39. Pedreschi, F., J. M. Aguilera, E. Agosin, M. R. San (1997). Induction of trehalose in spores of the biocontrol agent Trichoderma harzianum. Biopro. Eng., 17, 317-322. [Google Scholar]
  40. Poosapati, S., P. D. Ravulapalli, N. Tippirishetty, D. K. Vishwanathaswamy, and S. Chunduri, (2014). Selection of high temperature and salinity tolerant Trichoderma isolates with antagonistic activity against Sclerotium rolfsii. Springer plus, 3, 641-647. [Google Scholar]
  41. Rifai, M. A (1969). A revision of the genus Trichoderma. Mycological Papers, 116, 1-56. [Google Scholar]
  42. Ruijter, G. J. G., M. Bax, H. Patel, S. J. Flitter, P. J. I. van de Vondervoort, R. P. De Vries, P. A. Van Kuyk and J. Visser (2003). Mannitol is required for stress tolerance in Aspergillus niger conidiospores. Eukaryot Cell, 4, 690-698. [Google Scholar]
  43. Ruocco, M., S. Lanzuise, F. Vinale, R. Marra, D. Turrà, S. L Woo and M. Lorito (2009). Identification of a new biocontrol gene in Trichoderma atroviride: the role of an ABC transporter membrane pump in the interaction with different plant-pathogenic fungi. Mol. Plant. Micro. Inter., 22, 291–301. [Google Scholar]
  44. Samuels G. J., P. Chaverri, D. F.Farr and E. B. McCray (2004). Trichoderma Online. Systematic Botany & Mycology Laboratory, ARS, USDA. Re-trieved August 31, 2004, from [Accessed: 16 February 2017]. [Google Scholar]
  45. Samuels, G. J (2006). Trichoderma: Systematics, the Sexual State, and Ecology. Phytopathol., 96, 195-206 [Google Scholar]
  46. Samuels, G.J., O. Petrini and S. Manguin (1994). Morphological and macromolecular [Google Scholar]
  47. characterization of Hypocrea schweinitzii and its Trichoderma anamorph. Mycologia, 86, 421-435. [Google Scholar]
  48. Saran, S. M., T. Vinodhkumar and G. Ramanathan (2013).  Evaluation of antifungal activity of metabolites from Trichoderma species against fungal phytopathogens. Int. J. Sci. Innov. Disc., 3 (5), 528- 538. [Google Scholar]
  49. Schlesinger, M. J., G. Aliperti, and P. M. Kelley (1982). The response of cells to heat shock. Trend. Biochem. Sci., 1, 222-225. [Google Scholar]
  50. Sharma, P (2011). Complexity of Trichoderma Fusarium interaction and manifestation of biological control. Aus. J. Crop. Sci., 5(8), 1027-1038. [Google Scholar]
  51. Singh, A., M. Shahid, M. Srivastava, S. Pandey, A. Sharma and V. Kumar (2014). Optimal physical parameters for growth of Trichoderma species at varying pH, temperature and agitation. Virology and Mycology, 3(1), 127–134. [Google Scholar]
  52. Singh, S. P and H. F. Schwartz (2010). Breeding common bean for resistance to disease: a review. Crop. Sci, 50, 2199-2223. [Google Scholar]
  53. Soliman, H. G., H. H. El–Sheikh and I. F. Lashine (1994). Influence of salt stress on certain metabolic activities of Aspergillus terreus and A. tamarii isolated from the Mediterranean Sea water. Al-Azhar J. Microbioly, 4. 46-57. [Google Scholar]
  54. Spiegel, Y and Chet, I (1998). Evaluation of Trichoderma spp. as a biocontrol agent against soilborne fungi and plant-parasitic nematodes in Israel. Int. Pest Man. Rev., 3, 169-175. [Google Scholar]
  55. Ting, A. S. Y (2014). Biosourcing endophytes as biocontrol agents of wilt diseases. In: Verma, V.C., Gange, A.C. (Eds.), Advances in Endophytic Research. Springer India, pp. 283–300. [Google Scholar]
  56. Triveni, S., R. Prasanna, A., Kumar, N., Bidyarani, R., Singh and Saxena, A. K (2015). Evaluating the promise of Trichoderma and Anabaena based biofilms as multifunctional agents in Macrophomina phaseolina-infected cotton crop. Biocont. Sci. Technol., 25, 656-670.  [Google Scholar]
  57. Upadhyay, R. S and B. Rai (1979). Ecological survey of Indian soil fungi with special reference to Aspergilli, Penicillia and Trichoderma. Rev. Ecol. Biol. Sol., 16, 39-49. [Google Scholar]
  58. Viera, R. F., T. J. Paula Junior and H. Teixeira (2010). White mold management in common bean by increasing within-row distance between plants. Plant Dis., 94 (3), 362-367. [Google Scholar]
  59. Vierling, E., (1991). The roles of heat shock proteins in plants. Ann. Rev. Plant Physiol. Mol Biol, 42, 579-620. [Google Scholar]
  60. Vinale, F., K. Sivasithamparam, E. L. Ghisalberti, R. Marra, M. J. Barbetti, H. Li, S. L. Woo, and M. Lorito (2008). A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol. Mol. Plant. Path., 72, 80-86. [Google Scholar]
  61. Viterbo, A., U. Landau, S. Kim, L. Chernin and I. Chet (2010). Characterization of ACC deaminase from the biocontrol and plant growth-promoting agent Trichoderma asperellum T203. FEMS. Microbiol. Lett., 3, 42-8. [Google Scholar]
  62. Watanabe, N (1984). Antagonism by various kind of Trichoderma fungi to soil born plant [Google Scholar]
  63. pathogen. Bulletin of Faculty of Agriculture, Maiji University, Japan. [Google Scholar]
  64. Zang, S. W., Y. T. Gan and B. L. Xu (2016). Application of plant-growth-promoting fungi Trichoderma longibrachiatum T6 enhances tolerance of wheat to salt stress through improvement of antioxydative defense system and gene expression. Front. Plant. Sci., 7, 1405 [Google Scholar]
  65. Zehra, A., M. K. Dubey, M. Meena and R. S. Upadhyay (2017). Effect of different environmental conditions on growth and sporulation of some Trichoderma species. J. Env. Biol., 38, 197-203. [Google Scholar]
  66. Zhang, G., F. Wang, J. Qin, D. Wang, J. Zhang, Y. Zhang, S. Zhang and H. Pan (2013). Efficacy assessment of antifungal metabolites from Chaetomium globosum No. 05, a new biocontrol agent against Setosphaeria turcica. Biol. Cont., 64, 90-98. [Google Scholar]