SEARCH WITHIN CONTENT
Citation Information : Polish Journal of Microbiology. VOLUME 66 , ISSUE 1 , ISSN (Online) 2544-4646, DOI: 10.5604/17331331.1234996, March 2017
License : (CC BY-NC-ND 4.0)
Received Date : 25-February-2016 / Accepted: 05-December-2016 / Published Online: 30-March-2017
The aim of the present study was to examine the abilities of twenty-four isolates belonging to ten different Trichoderma species (i.e., Trichoderma atroviride, Trichoderma citrinoviride, Trichoderma cremeum, Trichoderma hamatum, Trichoderma harzianum, Trichoderma koningiopsis, Trichoderma longibrachiatum, Trichoderma longipile, Trichoderma viride and Trichoderma viridescens) to inhibit the mycelial growth and mycotoxin production by five Fusarium strains (i.e., Fusarium avenaceum, Fusarium cerealis, Fusarium culmorum, Fusarium graminearum and Fusarium temperatum). Dual-culture bioassay on potato dextrose agar (PDA) medium clearly documented that all of the Trichoderma strains used in the study were capable of influencing the mycelial growth of at least four of all five Fusarium species on the fourth day after co-inoculation, when there was the first apparent physical contact between antagonist and pathogen. The qualitative evaluation of the interaction between the colonies after 14 days of co-culturing on PDA medium showed that ten Trichoderma strains completely overgrew and sporulated on the colony at least one of the tested Fusarium species. Whereas, the microscopic assay provided evidence that only T. atroviride AN240 and T. viride AN255 formed dense coils around the hyphae of the pathogen from where penetration took place. Of all screened Trichoderma strains, T. atroviride AN240 was also found to be the most efficient (69–100% toxin reduction) suppressors of mycotoxins (deoxynivalenol, 3-acetyl-deoxynivalenol, 15-acetyl-deoxynivalenol, nivalenol, zearalenone, beauvericin, moniliformin) production by all five Fusarium species on solid substrates. This research suggests that T. atroviride AN240 can be a promising candidate for the biological control of toxigenic Fusarium species.
Almeida F.B., F.M. Cerqueira, N. Silva Rdo, C.J. Ulhoa and A.L. Lima. 2007. Mycoparasitism studies of Trichoderma harzianum strains against Rhizoctonia solani: evaluation of coiling and hydrolytic enzyme production. Biotechnol. Lett. 29: 1189–1193.
Altinok H.H. 2009. In vitro production of fumonisin B1 and B2 by Fusarium moniliforme and the biocontrol activity of Trichoderma harzianum. Ann. Microbiol. 59: 509–516.
Amarasinghe C.C., S.A. Tittlemier and W.G.D. Fernando. 2014. Nivalenol-producing Fusarium cerealis associated with fusarium head blight in winter wheat in Manitoba, Canada. Plant Pathol. 64: 988–995.
Amin F., V.K. Razdanm, F.A. Mohidm, K.A. Bhat and S. Bandaym. 2010. Potential of Trichoderma species as biocontrol agents of soil borne fungal propagules. J. Phytopathol. 10: 38–41.
Anees M., A. Tronsmo, V. Edel-Hermann, L.G. Hjeljord, C. Héraud and C. Steinberg. 2010. Characterization of field isolates of Trichoderma antagonistic against Rhizoctonia solani. Fungal Biol. 141: 691–701.
Benítez T., A.M. Ricón, C.M Limón and A.C. Codón. 2004. Biocontrol mechanisms of Trichoderma strains. Int. Microbiol. 7: 249–260.
Bennett J.W. and M. Klich. 2003. Mycotoxins. Clin. Microbiol. Rev. 16: 497–516.
Bily A.C., L.M. Reid, M.E. Savard, R. Reddy, B.A. Blackwell, C.M. Campbell, A. Krantis, T. Durst, B.J. Philogène, J.T. Arnason and others. 2004. Analysis of Fusarium graminearum mycotoxins in different biological matrices by LC/MS. Mycopathologia 157: 117–126.
Błaszczyk L., D. Popiel, J. Chełkowski, G. Koczyk, G.J. Samuels, K. Sobieralski and M. Siwulski. 2011. Species diversity of Trichoderma in Poland. J. Appl. Genet. 52: 233–243.
Bottalico A. and G. Perrone. 2002. Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe. Eur. J. Plant Pathol. 108: 611–624.
Buśko M., J. Chełkowski, D. Popiel and J. Perkowsk. 2008. Solid substrate bioassay to evaluate impact of Trichoderma on trichothecene mycotoxin production by Fusarium species. J. Sci. Food Agr. 88: 536–541.
Cooney J.M., D.R. Lauren and M.E. Menna. 2001. Impact of competitive fungi on trichothecene production by Fusarium graminearum. J. Agric. Food Chem. 49: 522–526.
Czembor E., Ł. Stępień and A. Waśkiewicz. 2014. Fusarium temperatum as a new species causing ear rot on maize in Poland. Plant Dis. 98: 1001.
Druzhinina I.S., V. Seidl-Seiboth, A. Herrera-Estrella, B.A. Hor-witz, C.M. Kenerley, E. Monte, P.K. Mukherjee, S. Zeilinger, I.V. Grigoriev and C.P. Kubicek. 2011. Trichoderma: the genomics of opportunistic success. Nat. Rev. Microbiol. 16: 749–759.
Dubey S., M. Suresh and B. Singh. 2007. Evaluation of Trichoderma species against Fusarium oxysporum f. sp. ciceris for integrated management of chickpea wilt. Biol. Control 40: 118–127.
Edington L.V., K.L. Khew and G. Barron. 1971. Fungitoxic spectrum of benzimidazole compounds. Phytopathol. 61: 42–44.
Elmholt S. 2008. Mycotoxins in the soil environment, pp. 167–203. In: P. Karlovsky (ed.). Secondary metabolites in soil ecology. Springer- Verlag, Heidelberg, Berlin.
Ferrigo D., A. Raiola, E. Piccolo, C. Scopel and R. Causin. 2014a. Trichoderma harzianum T22 induces in maize systemic resistance against Fusarium verticillioides. J. Plant Pathol. 96: 133–142.
Ferrigo D., A. Raiola, R. Rasera and R. Causin. 2014b. Trichoderma harzianum seed treatment controls Fusarium verticillioides colonization and fumonisin contamination in maize under field conditions. Crop Prot. 65: 51–56.
Glenn A.E. 2007. Mycotoxigenic Fusarium species in animal feed. Anim. Feed Sci. Tech. 137: 213–240.
Goertz A., S. Zühlke, M. Spiteller, U. Steiner, H.W. Dehne, C. Waalwijk, P.M. de Vries and E.C. Oerke. 2010. Fusarium species and mycotoxin profiles on commercial maize hybrids in Germany. Eur. J. Plant Pathol. 128: 101–111.
Gromadzka K., J. Chełkowski, D. Popiel, P. Kachlicki, M. Kostecki and P. Goliński. 2009. Solid substrate bioassay to evaluate the effect of Trichoderma and Clonostachys on the production of zearalenone by Fusarium species. World Mycotoxin J. 2: 45–52.
Harman G.E., C.R. Howell, A. Viterbo, I. Chet and M. Lorito. 2004. Trichoderma species–opportunistic, avirulent plant symbionts. Nat. Rev. Microbiol. 2: 43–56.
Hermosa R., A. Viterbo, I. Chet and E. Monte. 2012. Plantbeneficial effects of Trichoderma and of its genes. Microbiology 158: 17–25.
Inbar J. and I. Chet. 1992. Biomimics of fungal cell-cell recognition by use of lectin–coated nylon fibers. J. Bacteriol. 174: 1055–1059.
Inch S. and J. Gilbert. 2007. Effect of Trichoderma harzianum on perithecial production of Gibberella zeae on wheat straw. Biocontrol Sci. Techn. 17: 635–646.
Jeleń H., L. Błaszczyk, J. Chełkowski, K. Rogowicz and J. Strakowska. 2014. Formation of 6-n-pentyl-2H-pyran-2-one (6-PAP) and other volatiles by different Trichoderma species. Mycol. Prog. 13: 589–600.
Jestoi M., M. Rokka, T. Yli-Mattila, P. Parikka, A. Rizzo and K. Peltonen. 2004. Presence and concentrations of the Fusarium-related mycotoxins beauvericin, eniatins and moniliformin in Finnish grain samples. Food Addit. Contam. 21: 794–802.
Jestoi M.N., S. Paavanen-Huhtala, P. Parikka and T. Yli-Mattila. 2008. In vitro and in vivo mycotoxin production of Fusarium species isolated from Finnish grains. Arch. Phytopathology Plant Protect. 41: 545–558.
Kostecki M., H. Wiśniewska, G. Perrone, A. Ritieni, P. Golinski, J. Chełkowski and A. Logrieco. 1999. The effects of cereal substrate and temperature on production of beauvericin, moniliformin and fusaproliferin by Fusarium subglutinans ITEM – 1434. Food Addit. Contam. 16: 361–365.
Kubicek C.P., M. Komon-Żelazowska and I.S. Druzhinina. 2008. Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity. J. Zhejiang Univ. Sci. B. 9: 753–763.
Logrieco A., G. Mulè, A. Moretti and A. Bottalico. 2002a. Toxigenic Fusarium species and mycotoxins associated with maize ear rot in Europe. Eur. J. Plant Pathol. 108: 597–609.
Logrieco A., A. Rizzo, R. Ferracane and A. Ritieni. 2002b. Occurrence of beauvericin and enniatins in wheat affected by Fusarium avenaceum head blight. Appl. Environ. Microbiol. 68: 82–85.
Logrieco A., A. Bottalico, G. Mule, A. Moretti and G. Perrone. 2003. Epidemiology of toxigenic fungi and their associated mycotoxins for some Mediterranean crops. Eur. J. Plant Pathol. 109: 645–667.
Mańka K. 1974. Fungal communities as criterion for estimating the effect of the environment of plant diseases in Poland. ZPPNR, PAN. 160: 9–23.
Matarese F., S. Sarrocco, S. Gruber, V. Seidl-Seiboth and G. Vannacci. 2012. Biocontrol of Fusarium head blight: interactions between Trichoderma and mycotoxigenic Fusarium. Microbiology 158: 98–106.
Nawrocka J. and U. Małolepsza. 2013. Diversity in plant systemic resistance induced by Trichoderma. Biol. Control 67: 149–156.
Nayakaa S.C, S.R. Niranjanaa, A.C. Uday, S. Shankara, R. Niranjan, M.S. Reddyb, H.S. Prakasha and C.N. Mortensenc. 2008. Seed biopriming with novel strain of Trichoderma harzianum for the control of toxigenic Fusarium verticillioides and fumonisins in maize. Arch Phytopathology Plant Protect 43:1–19.
Qualhato T.F., F.A.C. Lopes, A.S. Steindorff R.S. Brandão, R.S. Jesuino and C.J. Ulhoa. 2013. Mycoparasitism studies of Trichoderma species against three phytopathogenic fungi: evaluation of antagonism and hydrolytic enzyme production. Biotechnol. Lett. 35: 1461–1468.
Palazzini J.M., M.L. Ramirez, A.M. Torres and S.N. Chulze. 2007. Potential biocontrol agents for Fusarium head blight and deoxynivalenol production in wheat. Crop Prot. 26: 1702–1710.
Popiel D., H. Kwaśna, J. Chełkowski, Ł. Stępień and M. Laskowska. 2008. Impact of selected antagonistic fungi on Fusarium species – toxigenic cereal pathogens. Acta Mycol. 43: 29–40.
Samuels G.J. 2006. Trichoderma: systematics, the sexual state, and ecology. Phytopathology 96: 95–206.
Scauflaire J., M. Gourgue, A. Callebaut and F. Munaut. 2012. Fusarium temperatum, a mycotoxin-producing pathogen of maize. Eur. J. Plant Pathol. 133: 911–922.
Schöneberg A., T. Musa, R.T. Voegele and S. Vogelgsang. 2015. The potential of antagonistic fungi for control of Fusarium graminearum and Fusarium crookwellense varies depending on the experi-mental approach. J. Appl. Microbiol. 118: 1165–1179.
Shaigan S., A. Seraji and S.A.M. Moghaddam. 2008. Identification and investigation on antagonistic effect of Trichoderma spp on tea seedlings white foot and root rot (Sclerotium rolfsii Sacc.) in vitro condition. Pak. J. Biol. Sci. 19:2346–2350.
Stępień Ł., G. Koczyk and A. Waśkiewicz. 2011. FUM cluster divergence in fumonisins-producing Fusarium species. Fungal Biol. 115: 112–123.
Strakowska J., L. Błaszczyk and J. Chełkowski. 2014. The significance of cellulolytic enzymes produced by Trichoderma in opportunistic lifestyle of this fungus. J. Basic. Microbiol. 54: S2–S13.
Tomczak M., H. Wiśniewska, L. Stępień, M. Kostecki, J. Chełkowski and P. Goliński. 2002. Deoxynivalenol, nivalenol and moniliformin in wheat samples with head blight (scab) symptoms in Poland (1998–2000). Eur. J. Plant Pathol. 108: 625–630.
Verma M., S.K. Brar, R.D. Tyagi, R.Y. Surampalli and J.R. Valéro. 2007. Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochem. Eng. J. 37:1–20.
Vinale F., K. Sivasithamparam, E.L. Ghisalberti, R. Marra, M.J. Barbetti, H. Li, S.L. Woo and M. Lorito. 2008a. A novel role for Trichoderma secondary metabolites in the interactions with plants. Physiol. Mol. Plant. Path. 72: 80–86.
Vinale F., K. Sivasithamparam, E.L. Ghisalberti, R. Marra, S.L. Woo and M. Lorito. 2008b. Trichoderma–plant–pathogen interactions. Soil Biol. Biochem. 40: 1–10.
Visconti A. and M. Pascale. 1998. Determination of zearalenone in corn by means of immunoaffinity clean-up and high-performance liquid chromatography with fluorescence detector. J. Chromatogr. A. 815: 133–140.
Wagacha J. and Muthomi J. 2007. Fusarium culmorum: infection process, mechanisms of mycotoxin production and their role in pathogenesis in wheat. Crop Prot. 26: 877–885.
Wiśniewska H., Ł. Stępień, A. Waśkiewicz, M. Beszterda, T. Góral and J. Belter. 2014. Toxigenic Fusarium species infecting wheat heads in Poland. Cent. Eur. J. Biol. 9: 163–172.
Woo S.L., M. Ruocco, F. Vinale, M. Nigro, R. Marra, N. Lombardi, A. Pascale, S. Lanzuise, G. Manganiello and M. Lorito. 2014. Trichoderma-based products and their widespread use in agriculture. TOMYCJ. 8: 71–126.
Yang D., Z.M. Geng, J.B. Yao, X. Zhang, P.P. Zhang and H.X. Ma. 2013. Simultaneous determination of deoxynivalenol, and 15- and 3-acetyldeoxynivalenol in cereals by HPLC-UV detection. World Mycotoxin J. 6: 117–125.