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Applied Microbiology and Biotechnology

, Volume 100, Issue 12, pp 5257–5272 | Cite as

Relationship between mycoparasites lifestyles and biocontrol behaviors against Fusarium spp. and mycotoxins production

  • Seon Hwa Kim
  • Vladimir Vujanovic
Mini-Review

Abstract

Global food security research is seeking eco-friendly solutions to control mycotoxins in grain infected by fungi (molds). In particular, mycotoxigenic Fusarium spp. outbreak is a chronic threat for cereal grain production, human, and animal health. In this review paper, we discuss up-to-date biological control strategies in applying mycoparasites as biological control agents (BCA) to prevent plant diseases in crops and mycotoxins in grain, food, and feed. The aim is to increase food safety and to minimize economic losses due to the reduced grain yield and quality. However, recent papers indicate that the study of the BCA specialists with biotrophic lifestyle lags behind our understanding of the BCA generalists with necrotrophic lifestyle. We examine critical behavioral traits of the two BCA groups of mycoparasites. The goal is to highlight their major characteristics in the context of future research towards an efficient biocontrol strategy against mycotoxin-producing Fusarium species. The emphasis is put on biocontrol of Fusarium graminearum, F. avenaceum, and F. culmorum causing Fusarium head blight (FHB) in cereals and their mycotoxins.

Keywords

Biological control agents Mycoparasites Fusarium Mycotoxins 

Notes

Acknowledgments

This research was financially supported by Natural Sciences and Engineering Research Council of Canada–Discovery Grant to Dr. V. Vujanovic.

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Almassi F, Ghisalberti EL, Narbey MJ, Sivasithamparam K (1991) New antibiotics from strains of Trichoderma harzianum. J Nat Prod 54(2):396–402. doi: 10.1021/np50074a008 CrossRefGoogle Scholar
  2. Awad WA, Ghareeb K, Bohm J, Zentek J (2010) Decontamination and detoxification strategies for the Fusarium mycotoxin deoxynivalenol in animal feed and the effectiveness of microbial biodegradation. Food Addit Contam Part A, Chem Anal Control, Expo Risk Assess 27(4):510–520. doi: 10.1080/19440040903571747 CrossRefGoogle Scholar
  3. Ayers TT (1935) Parasitism of Dispira cornuta. Mycologia 27(3):235–261. doi: 10.2307/3754148 CrossRefGoogle Scholar
  4. Bamburg JR, Strong FM (1969) Mycotoxins of the trichothecane family produced by Fusarium tricinctum and Trichoderma lignorum. Phytochemistry 8(12):2405–2410. doi: 10.1016/S0031-9422(00)88162-5 CrossRefGoogle Scholar
  5. Barnett HL (1963) The nature of mycoparasitism by fungi. Annu Rev Microbiol 17(1):1–14. doi: 10.1146/annurev.mi.17.100163.000245 CrossRefGoogle Scholar
  6. Benoni H, Taraz K, Korth H, Pulverer G (1990) Characterization of 6-pentyl-α-pyrone from the soil fungus Trichoderma koningii. Sci Nat 77(11):539–540. doi: 10.1007/BF01139267 CrossRefGoogle Scholar
  7. Boosalis MG (1964) Hyperparasitism. Annu Rev Phytopathol 2(1):363–376. doi: 10.1146/annurev.py.02.090164.002051 CrossRefGoogle Scholar
  8. Borrego-Benjumea A, Basallote-Ureba MJ, Melero-Vara JM, Abbasi PA (2014) Characterization of Fusarium isolates from asparagus fields in Southwestern Ontario and influence of soil organic amendments on Fusarium crown and root rot. Phytopathology 104(4):403–415PubMedCrossRefGoogle Scholar
  9. Brian P (1944) Production of gliotoxin by Trichoderma viride. Nature 154:667–668CrossRefGoogle Scholar
  10. Brian P, McGowan J (1945) Viridin: a highly fungistatic substance produced by Trichoderma viride. Nature 156(3953):144–145CrossRefGoogle Scholar
  11. Burka LT, Doran J, Wilson BJ (1982) Enzyme inhibition and the toxic action of moniliformin and other vinylogous α-ketoacids. Biochem Pharmacol 31(1):79–84. doi: 10.1016/0006-2952(82)90240-4 PubMedCrossRefGoogle Scholar
  12. Butler EE (1957) Rhizoctonia solani as a parasite of fungi. Mycologia 49(3):354–373. doi: 10.2307/3755685 CrossRefGoogle Scholar
  13. Butt TM, Jackson C, Magan N (2001) Fungi as biocontrol agents progress, problems and potential. CABI Pub, Oxon, UK; New YorkCrossRefGoogle Scholar
  14. Caldwell RW, Tuite J, Stob M, Baldwin R (1970) Zearalenone production by Fusarium species. Appl Microbiol 20(1):31–34PubMedPubMedCentralGoogle Scholar
  15. Cardoza RE, Malmierca MG, Hermosa MR, Alexander NJ, McCormick SP, Proctor RH, Tijerino AM, Rumbero A, Monte E, Gutierrez S (2011) Identification of loci and functional characterization of trichothecene biosynthesis genes in filamentous fungi of the genus Trichoderma. Appl Environ Microbiol 77(14):4867–4877. doi: 10.1128/aem.00595-11 PubMedPubMedCentralCrossRefGoogle Scholar
  16. CEMA (2015) European agrilculture machinery. Global food security: recognizing smart farm machinery as a key enabling technology to produce more food more sustainably & feed a growing world population. http://cema-agri.org/sites/default/files/Global%20Food%20Security%20-%20the%20role%20of%20smart%20machinery.pdf. Accessed 29 Dec 2015
  17. Choi SU, Choi EJ, Kim KH, Kim NY, Kwon BM, Kim SU, Bok SH, Lee SY, Lee CO (1996) Cytotoxicity of trichothecenes to human solid tumor cells in vitro. Arch Pharm Res 19(1):6–11. doi: 10.1007/bf02976812 CrossRefGoogle Scholar
  18. Chapagan BP, Wiesman Z, Tsror L (2007) In vitro study of the antifungal activity of saponin-rich extracts against prevalent phytopathogenic fungi. Ind Crop Prod 26(2):109–115. doi: 10.1016/j.indcrop.2007.02.005 CrossRefGoogle Scholar
  19. Claydon N, Allan M, Hanson JR, Avent AG (1987) Antifungal alkyl pyrones of Trichoderma harzianum. Trans Br Mycol Soc 88(4):503–513. doi: 10.1016/S0007-1536(87)80034-7 CrossRefGoogle Scholar
  20. Collins RP, Halim AF (1972) Characterization of the major aroma constituent of the fungus Trichoderma viride. J Agric Food Chem 20(2):437–438. doi: 10.1021/jf60180a010 CrossRefGoogle Scholar
  21. Cooney JM, Lauren DR (1998) Trichoderma/pathogen interactions: measurement of antagonistic chemicals produced at the antagonist/pathogen interface using a tubular bioassay. Lett Appl Microbiol 27(5):283–286PubMedCrossRefGoogle Scholar
  22. Corley DG, Miller-Wideman M, Durley RC (1994) Isolation and structure of harzianum A: a new trichothecene from Trichoderma harzianum. J Nat Prod 57(3):422–425PubMedCrossRefGoogle Scholar
  23. Covarelli L, Beccari G, Prodi A, Generotti S, Etruschi F, Juan C, Ferrer E, Manes J (2015) Fusarium species, chemotype characterisation and trichothecene contamination of durum and soft wheat in an area of Central Italy. J Sci Food Agric 95(3):540–551. doi: 10.1002/jsfa.6772 PubMedCrossRefGoogle Scholar
  24. Cutler HG, Cox RH, Crumley FG, Cole PD (1986) 6-pentyl-α-pyrone from Trichoderma harzianum: its plant growth inhibitory and antimicrobial properties. Agric Biol Chem 50(11):2943–2945Google Scholar
  25. Cutler HG, Himmelsbach DS, Arrendale RF, Cole PD, Cox RH (1989) Koninginin A: a novel plant growth regulator from Trichoderma koningii. Agric Biol Chem 53(10):2605–2611Google Scholar
  26. Da Cruz CL, Fernández Pinto V, Patriarca A (2013) Application of plant derived compounds to control fungal spoilage and mycotoxin production in foods. Int J Food Microbiol 166(1):1–14. doi: 10.1016/j.ijfoodmicro.2013.05.026 CrossRefGoogle Scholar
  27. De Vrije T, Antoine N, Buitelaar RM, Bruckner S, Dissevelt M, Durand A, Gerlagh M, Jones EE, Luth P, Oostra J, Ravensberg WJ, Renaud R, Rinzema A, Weber FJ, Whipps JM (2001) The fungal biocontrol agent Coniothyrium minitans: production by solid-state fermentation, application and marketing. Appl Microbiol Biotechnol 56(1–2):58–68PubMedCrossRefGoogle Scholar
  28. Desjardins AE, Hohn TM, McCormick SP (1993) Trichothecene biosynthesis in Fusarium species: chemistry, genetics, and significance. Microbiol Rev 57(3):595–604PubMedPubMedCentralGoogle Scholar
  29. Di Pietro A, Lorito M, Hayes C, Broadway R, Harman G (1993) Endochitinase from Gliocladium virens: isolation, characterization, and synergistic antifungal activity in combination with gliotoxin. Phytopathology 83(3):308–313CrossRefGoogle Scholar
  30. Doi K, Uetsuka K (2011) Mechanisms of mycotoxin-induced neurotoxicity through oxidative stress-associated pathways. Int J Mol Sci 12(8):5213–5237. doi: 10.3390/ijms12085213 PubMedPubMedCentralCrossRefGoogle Scholar
  31. Ehrlich KC, Daigle KW (1987) Protein synthesis inhibition by 8-oxo-12,13-epoxytrichothecenes. Biochim Biophys Acta 923(2):206–213PubMedCrossRefGoogle Scholar
  32. El-Sharkawy S, Abul-Hajj YJ (1988) Microbial cleavage of zearalenone. Xenobiotica Fate Foreign Compounds Biol Syst 18(4):365–371. doi: 10.3109/00498258809041672 CrossRefGoogle Scholar
  33. Elmer WH, Summerell BA, Burgess LW, Nigh EL Jr (1999) Vegetative compatibility groups in Fusarium proliferatum from Asparagus in Australia. Mycologia 91(4):650–654. doi: 10.2307/3761251 CrossRefGoogle Scholar
  34. Fernandez M, Jefferson P (2004) Fungal populations in roots and crowns of common and durum wheat in Saskatchewan. Can J Plant Pathol 26(3):325–334CrossRefGoogle Scholar
  35. Fernandez MR, Basnyat P, Zentner RP (2007) Response of wheat root pathogens to crop management in Eastern Saskatchewan. Can J Plant Sci 87(4):953–963. doi: 10.4141/CJPS07005 CrossRefGoogle Scholar
  36. Franck B, Breipohl G (1984) Biosynthesis of moniliformin, a fungal toxin with cyclobutanedione structure. Angew Chem Int Ed Engl 23(12):996–998. doi: 10.1002/anie.198409961 CrossRefGoogle Scholar
  37. Fravel DR (1988) Role of antibiosis in the biocontrol of plant diseases. Annu Rev Phytopathol 26(1):75–91. doi: 10.1146/annurev.py.26.090188.000451 CrossRefGoogle Scholar
  38. Gaffoor I, Trail F (2006) Characterization of two polyketide synthase genes involved in zearalenone biosynthesis in Gibberella zeae. Appl Environ Microbiol 72(3):1793–1799PubMedPubMedCentralCrossRefGoogle Scholar
  39. Gallo A, Mulè G, Favilla M, Altomare C (2004) Isolation and characterisation of a trichodiene synthase homologous gene in Trichoderma harzianum. Physiol Mol Plant Pathol 65(1):11–20CrossRefGoogle Scholar
  40. García-Martínez J, Ádám AL, Avalos J (2012) Adenylyl cyclase plays a regulatory role in development, stress resistance and secondary metabolism in Fusarium fujikuroi. PLoS One 7(1):e28849. doi: 10.1371/journal.pone.0028849 PubMedPubMedCentralCrossRefGoogle Scholar
  41. Gardiner DM, Osborne S, Kazan K, Manners JM (2009) Low pH regulates the production of deoxynivalenol by Fusarium graminearum. Microbiology (Reading, England) 155(9):3149–3156CrossRefGoogle Scholar
  42. Gathercole PS, Thiel PG, Hofmeyr JH (1986) Inhibition of pyruvate dehydrogenase complex by moniliformin. Biochem J 233(3):719–723PubMedPubMedCentralCrossRefGoogle Scholar
  43. Gelderblom WCA, Kriek NPJ, Marasas WFO, Thiel PG (1991) Toxicity and carcinogenicity of the Fusarium monitiforme metabolite, fumonisin B1, in rats. Carcinogenesis 12(7):1247–1251PubMedCrossRefGoogle Scholar
  44. Gelderblom WCA, Snyman SD, Lebepe-Mazur S, van der Westhuizen L, Kriek NPJ, Marasas WFO (1996) The cancer-promoting potential of fumonisin B1 in rat liver using diethylnitrosamine as a cancer initiator. Cancer Lett 109(1–2):101–108. doi: 10.1016/S0304-3835(96)04431-X PubMedCrossRefGoogle Scholar
  45. Gerlagh M, Goossen-van de Geijn HM, Fokkema NJ, Vereijken PFG (1999) Long-term biosanitation by application of Coniothyrium minitans on Sclerotinia sclerotiorum-infected crops. Phytopathology 89(2):141–147. doi: 10.1094/PHYTO.1999.89.2.141 PubMedCrossRefGoogle Scholar
  46. Glister G, Williams T (1944) Production of gliotoxin by Aspergillus fumigatus mut. Helvola Yuill. Nature 153:651CrossRefGoogle Scholar
  47. Gnanamanickam SS, Vasudevan P, Reddy MS, Defago G, Kloepper J (2002) Principles of biological control. Biological Control of Crop Diseases:1–9Google Scholar
  48. Godtfredsen W, Vangedal S (1964) Trichodermin new antibiotic related to trichothecin. Proceedings of the Chemical Society, p 188–189Google Scholar
  49. Goh YK, Vujanovic V (2010a) Ascospore germination patterns revealed ascomycetous biotrophic mycoparasite specificity to Fusarium hosts. Botany 88(12):1033–1043. doi: 10.1139/b10-074 CrossRefGoogle Scholar
  50. Goh YK, Vujanovic V (2010b) Biotrophic mycoparasitic interactions between Sphaerodes mycoparasitica and phytopathogenic Fusariums species. Biocontrol Sci Tech 20(9):891–902. doi: 10.1080/09583157.2010.489147 CrossRefGoogle Scholar
  51. Goh YK, Vujanovic V (2010c) Sphaerodes quadrangularis biotrophic mycoparasitism on Fusarium avenaceum. Mycologia 102(4):757–762. doi: 10.3852/09-171 PubMedCrossRefGoogle Scholar
  52. Haggag WM, Mohamed HAA (2002) Enhancement of antifungal metabolite production from gamma-ray induced mutants of some Trichoderma species for control onion white rot disease. Plant Pathol Bull 11(1):45–56Google Scholar
  53. Harrison LR, Colvin BM, Greene JT, Newman LE, Cole JR (1990) Pulmonary edema and hydrothorax in swine produced by fumonisin B1, a toxic metabolite of Fusarium moniliforme. J Vet Diagn Investig 2(3):217–221CrossRefGoogle Scholar
  54. Harveson RM, Kimbrough JW (2001) Parasitism and measurement of damage to Fusarium oxysporum by species of Melanospora, Sphaerodes, and Persiciospora. Mycologia 93(2):249–257CrossRefGoogle Scholar
  55. Harveson RM, Kimbrough JW, Hopkins DL (2002) Novel use of a Pyrenomycetous mycoparasite for management of Fusarium wilt of watermelon. Plant Dis 86(9):1025–1030. doi: 10.1094/pdis.2002.86.9.1025 CrossRefGoogle Scholar
  56. Hashioka Y, Nakai Y (1980) Ultrastructure of pycnidial development and mycoparasitism of Ampelomyces quisqualis parasitic on Erysiphales. Trans Mycol Soc Jpn 21(3):329–338Google Scholar
  57. Hatvani L, Antal Z, Manczinger L, Szekeres A, Druzhinina IS, Kubicek CP, Nagy A, Nagy E, Vágvölgyi C, Kredics L (2007) Green mold diseases of Agaricus and Pleurotus spp. are caused by related but phylogenetically different Trichoderma species. Phytopathology 97(4):532–537. doi: 10.1094/PHYTO-97-4-0532 PubMedCrossRefGoogle Scholar
  58. Howell C, Stipanovic R (1984) Phytotoxicity to crop plants and herbicidal effects on weeds of viridiol produced by Gliocladium virens. Phytopathology 74(11):1346–1349CrossRefGoogle Scholar
  59. Howell CR (2003) Mechanisms employed by Trichoderma species in the biological control of plant diseases: the history and evolution of current concepts. Plant Dis 87(1):4–10. doi: 10.1094/pdis.2003.87.1.4 CrossRefGoogle Scholar
  60. Iqbal SZ, Asi MR, Jinap S, Rashid U (2014) Detection of aflatoxins and zearalenone contamination in wheat derived products. Food Control 35(1):223–226. doi: 10.1016/j.foodcont.2013.06.048 CrossRefGoogle Scholar
  61. Jagadeesan V, Rukmini C, Vijayaraghavan M, Tulpule PG (1982) Immune studies with T-2 toxin: effect of feeding and withdrawal in monkeys. Food Chem Toxicol 20(1):83–87. doi: 10.1016/S0278-6915(82)80014-8 PubMedCrossRefGoogle Scholar
  62. Jeffries P (1995) Biology and ecology of mycoparasitism. Can J Bot 73(S1):1284–1290. doi: 10.1139/b95-389 CrossRefGoogle Scholar
  63. Jensen B, Knudsen IB, Jensen D (2000) Biological seed treatment of cereals with fresh and long-term stored formulations of Clonostachys rosea: biocontrol efficacy against Fusarium culmorum. Eur J Plant Pathol 106(3):233–242. doi: 10.1023/A:1008794626600 CrossRefGoogle Scholar
  64. Jensen B, Knudsen IM, Madsen M, Jensen DF (2004) Biopriming of infected carrot seed with an antagonist, Clonostachys rosea, selected for control of seedborne Alternaria spp. Phytopathology 94(6):551–560PubMedCrossRefGoogle Scholar
  65. Jestoi M (2008) Emerging fusarium-mycotoxins fusaproliferin, beauvericin, enniatins, and moniliformin: a review. Crit Rev Food Sci Nutr 48(1):21–49. doi: 10.1080/10408390601062021 PubMedCrossRefGoogle Scholar
  66. Jurado M, Vázquez C, Marín S, Sanchis V, Teresa González-Jaén M (2006) PCR-based strategy to detect contamination with mycotoxigenic Fusarium species in maize. Syst Appl Microbiol 29(8):681–689. doi: 10.1016/j.syapm.2006.01.014 PubMedCrossRefGoogle Scholar
  67. Kabak B (2010) Prevention and management of mycotoxins in food and feed. In: Rai M, Varma A (eds) Mycotoxins in food. Feed and Bioweapons. Springer, Berlin Heidelberg, pp. 201–227Google Scholar
  68. Karlovsky P (2011) Biological detoxification of the mycotoxin deoxynivalenol and its use in genetically engineered crops and feed additives. Appl Microbiol Biotechnol 91(3):491–504. doi: 10.1007/s00253-011-3401-5 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Karlsson M, Durling MB, Choi J, Kosawang C, Lackner G, Tzelepis GD, Nygren K, Dubey MK, Kamou N, Levasseur A, Zapparata A, Wang J, Amby DB, Jensen B, Sarrocco S, Panteris E, Lagopodi AL, Pöggeler S, Vannacci G, Collinge DB, Hoffmeister D, Henrissat B, Lee Y-H, Jensen DF (2015) Insights on the evolution of mycoparasitism from the genome of Clonostachys rosea. Genome Biol Evol 7(2):465–480. doi: 10.1093/gbe/evu292 PubMedPubMedCentralCrossRefGoogle Scholar
  70. Katzenellenbogen BS, Katzenellenbogen JA, Mordecai D (1979) Zearalenones: characterization of the estrogenic potencies and receptor interactions of a series of fungal β-resorcylic acid lactones. Endocrinology 105(1):33–40PubMedCrossRefGoogle Scholar
  71. Keinath A, Fravel D, Papavizas G (1991) Potential of Gliocladium roseum for biocontrol of Verticillium dahliae. Phytopathology 81(6):644–648CrossRefGoogle Scholar
  72. Kellerman TS, Marasas W, Thiel P, Gelderblom W, Cawood M, Coetzer J (1990) Leukoencephalomalacia in two horses induced by oral dosing of fumonisin B1. The Onderstepoort Journal of Veterinary Research 57(4):269–275PubMedGoogle Scholar
  73. Kim K, Fravel D, Papavizas G (1988) Identification of a metabolite produced by Talaromyces flavus as glucose oxidase and its role in the biocontrol of Verticillium dahliae. Phytopathology 78:488–492CrossRefGoogle Scholar
  74. Kim KK-A, Fravel DR, Papavizas GC (1990) Glucose oxidase as the antifungal principle of talaron from Talaromyces flavus. Can J Microbiol 36(11):760–764. doi: 10.1139/m90-131 PubMedCrossRefGoogle Scholar
  75. Kim YT, Lee YR, Jin J, Han KH, Kim H, Kim JC, Lee T, Yun SH, Lee YW (2005) Two different polyketide synthase genes are required for synthesis of zearalenone in Gibberella zeae. Mol Microbiol 58(4):1102–1113PubMedCrossRefGoogle Scholar
  76. Knudsen IMB, Hockenhull J, Jensen DF (1995) Biocontrol of seedling diseases of barley and wheat caused by Fusarium culmorum and Bipolaris sorokiniana: effects of selected fungal antagonists on growth and yield components. Plant Pathol 44(3):467–477. doi: 10.1111/j.1365-3059.1995.tb01669.x CrossRefGoogle Scholar
  77. Kokkonen M, Ojala L, Parikka P, Jestoi M (2010) Mycotoxin production of selected Fusarium species at different culture conditions. Int J Food Microbiol 143(1–2):17–25. doi: 10.1016/j.ijfoodmicro.2010.07.015 PubMedCrossRefGoogle Scholar
  78. Kordic B, Pribicevic S, Muntanola-Cvetkovic M, Nikolic P, Nikolic B (1992) Experimental study of the effects of known quantities of zearalenone on swine reproduction. J Environ Pathol Toxicol Oncol Off Organ Int Soc Environ Toxicol Cancer 11(2):53–55Google Scholar
  79. Kosawang C, Karlsson M, Vélëz H, Rasmussen PH, Collinge DB, Jensen B, Jensen DF (2014) Zearalenone detoxification by zearalenone hydrolase is important for the antagonistic ability of Clonostachys rosea against mycotoxigenic Fusarium graminearum. Fungal Biol 118(4):364–373. doi: 10.1016/j.funbio.2014.01.005 PubMedCrossRefGoogle Scholar
  80. Kredics L, Kocsube S, Nagy L, Komon-Zelazowska M, Manczinger L, Sajben E, Nagy A, Vagvolgyi C, Kubicek CP, Druzhinina IS, Hatvani L (2009) Molecular identification of Trichoderma species associated with Pleurotus ostreatus and natural substrates of the oyster mushroom. FEMS Microbiol Lett 300(1):58–67. doi: 10.1111/j.1574-6968.2009.01765.x PubMedCrossRefGoogle Scholar
  81. Kriek NP, Marasas WF, Steyn PS, van Rensburg SJ, Steyn M (1977) Toxicity of a moniliformin-producing strain of Fusarium moniliforme var. subglutinans isolated from maize. Food Cosmetics Toxicol 15(6):579–587CrossRefGoogle Scholar
  82. Kuiper GG, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, Gustafsson JA (1997) Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors α and β. Endocrinol 138(3):863–870Google Scholar
  83. Kulik T, Buśko M, Pszczółkowska A, Perkowski J, Okorski A (2014) Plant lignans inhibit growth and trichothecene biosynthesis in Fusarium graminearum. Lett Appl Microbiol 59(1):99–107. doi: 10.1111/lam.12250 PubMedCrossRefGoogle Scholar
  84. Lee HB, Kim Y, Jin HZ, Lee JJ, Kim CJ, Park JY, Jung HS (2005) A new Hypocrea strain producing harzianum a cytotoxic to tumour cell lines. Lett Appl Microbiol 40(6):497–503. doi: 10.1111/j.1472-765X.2005.01719.x PubMedCrossRefGoogle Scholar
  85. Leslie JF, Logrieco A (2014) Mycotoxin reduction in grain chains. Wiley-Blackwell, Ames, Iowa, USACrossRefGoogle Scholar
  86. Liu C, Xu W, Liu F, Jiang S (2007) Fumonisins production by Fusarium proliferatum strains isolated from asparagus crown. Mycopathologia 164(3):127–134. doi: 10.1007/s11046-007-9017-8 PubMedCrossRefGoogle Scholar
  87. Lorito M, Peterbauer C, Hayes CK, Harman GE (1994) Synergistic interaction between fungal cell wall degrading enzymes and different antifungal compounds enhances inhibition of spore germination. Microbiol (Reading, England) 140(3):623–629. doi: 10.1099/00221287-140-3-623 CrossRefGoogle Scholar
  88. Lumsden R, Beily B (1998) Direct effects of Trichoderma and Gliocladium on plant growth and resistance to pathogens. In: Harman G, Kubicek C, Ondik K (eds) Trichoderma and Gliocladium: enzymes, biological control and commercial applications, vol 2. CRC Press, New York, pp. 185–204Google Scholar
  89. Lumsden R, Locke J, Adkins S, Walter J, Ridout C (1992) Isolation and localization of the antibiotic gliotoxin produced by Gliocladium virens from alginate prill in soil and soilless media. Phytopathology 82(2):230–235CrossRefGoogle Scholar
  90. Lysøe E, Klemsdal SS, Bone KR, Frandsen RJN, Johansen T, Thrane U, Giese H (2006) The PKS4 gene of Fusarium graminearum is essential for zearalenone production. Appl Environ Microbiol 72(6):3924–3932. doi: 10.1128/aem.00963-05 PubMedPubMedCentralCrossRefGoogle Scholar
  91. Madi L, Katan T, Katan J, Henis Y (1997) Biological control of Sclerotium rolfsii and Verticillium dahliae by Talaromyces flavus is mediated by different mechanisms. Phytopathology 87(10):1054–1060. doi: 10.1094/PHYTO.1997.87.10.1054 PubMedCrossRefGoogle Scholar
  92. Malir F, Ostry V, Pfohl-Leszkowicz A, Novotna E (2013) Ochratoxin A: developmental and reproductive toxicity—an overview. Birth Defects Res Part B: Dev Reprod Toxicol 98(6):493–502. doi: 10.1002/bdrb.21091 CrossRefGoogle Scholar
  93. Malmierca MG, Cardoza RE, Alexander NJ, McCormick SP, Hermosa R, Monte E, Gutierrez S (2012) Involvement of Trichoderma trichothecenes in the biocontrol activity and induction of plant defense-related genes. Appl Environ Microbiol 78(14):4856–4868. doi: 10.1128/aem.00385-12 PubMedPubMedCentralCrossRefGoogle Scholar
  94. Martins ML, Martins HM (2002) Influence of water activity, temperature and incubation time on the simultaneous production of deoxynivalenol and zearalenone in corn (Zea mays) by Fusarium graminearum. Food Chem 79(3):315–318. doi: 10.1016/S0308-8146(02)00147-4 CrossRefGoogle Scholar
  95. McCormick SP (2013) Microbial detoxification of mycotoxins. J Chem Ecol 39(7):907–918. doi: 10.1007/s10886-013-0321-0 PubMedCrossRefGoogle Scholar
  96. McCormick SP, Stanley AM, Stover NA, Alexander NJ (2011) Trichothecenes: from simple to complex mycotoxins. Toxins 3(7):802–814. doi: 10.3390/toxins3070802 PubMedPubMedCentralCrossRefGoogle Scholar
  97. McLaren D, Huang H, Rimmer SR (1996) Control of apothecial production oí Sclerotinia sclerotiorum by Coniothyrium minitans and Talaromyces flavus. Plant Dis 80:1373–1378CrossRefGoogle Scholar
  98. McLaren DL, Huang HC, Kozub GC, Rimmer SR (1994) Biological control of Sclerotinia wilt of sunflower with Talaromyces flavus and Coniothyrium minitans. Plant Dis 78(3):231–235CrossRefGoogle Scholar
  99. McNeil J, Cotnoir PA, Leroux T, Laprade R, Schwartz JL (2010) A Canadian national survey on the public perception of biological control. BioControl 55(4):445–454. doi: 10.1007/s10526-010-9273-2 CrossRefGoogle Scholar
  100. Menzies JG (1993) A strain of Trichoderma viride pathogenic to germinating seedlings of cucumber, pepper and tomato. Plant Pathol 42(5):784–791. doi: 10.1111/j.1365-3059.1993.tb01565.x CrossRefGoogle Scholar
  101. Merrill AH Jr, Sullards MC, Wang E, Voss KA, Riley RT (2001) Sphingolipid metabolism: roles in signal transduction and disruption by fumonisins. Environ Health Perspect 109(Suppl 2):283PubMedPubMedCentralCrossRefGoogle Scholar
  102. Middlebrook JL, Leatherman DL (1989) Binding of T-2 toxin to eukaryotic cell ribosomes. Biochem Pharmacol 38(18):3103–3110PubMedCrossRefGoogle Scholar
  103. Miyake T, Kato A, Tateishi H, Teraoka T, Arie T (2012) Mode of action of Talaromyces sp KNB422, a biocontrol agent against rice seedling diseases. J Pestic Sci 37(1):56–61. doi: 10.1584/jpestics.D11-002 CrossRefGoogle Scholar
  104. Mullbacher A, Waring P, Eichner RD (1985) Identification of an agent in cultures of Aspergillus fumigatus displaying anti-phagocytic and immunomodulating activity in vitro. J Gen Microbiol 131(5):1251–1258PubMedGoogle Scholar
  105. Murray F, Llewellyn D, McFadden H, Last D, Dennis E, Peacock WJ (1999) Expression of the Talaromyces flavus glucose oxidase gene in cotton and tobacco reduces fungal infection, but is also phytotoxic. Mol Breed 5(3):219–232. doi: 10.1023/A:1009625801909 CrossRefGoogle Scholar
  106. Murray FR, Llewellyn DJ, Peacock WJ, Dennis ES (1997) Isolation of the glucose oxidase gene from Talaromyces flavus and characterisation of its role in the biocontrol of Verticillium dahliae. Curr Genet 32(5):367–375. doi: 10.1007/s002940050290 PubMedCrossRefGoogle Scholar
  107. Nicol RW, Traquair JA, Bernards MA (2002) Ginsenosides as host resistance factors in American ginseng (Panax quinquefolius). Canadian J Bot 80:557–562. doi: 10.1139/B02-034 CrossRefGoogle Scholar
  108. Nobre SAM, Maffia LA, Mizubuti ESG, Cota LV, Dias APS (2005) Selection of Clonostachys rosea isolates from Brazilian ecosystems effective in controlling Botrytis cinerea. Biol Control 34(2):132–143. doi: 10.1016/j.biocontrol.2005.04.011 CrossRefGoogle Scholar
  109. Osborne LE, Stein JM (2007) Epidemiology of Fusarium head blight on small-grain cereals. Int J Food Microbiol 119(1–2):103–108. doi: 10.1016/j.ijfoodmicro.2007.07.032 PubMedCrossRefGoogle Scholar
  110. Pal KK, Gardener BM (2006) Biological control of plant pathogens. Plant Health Instructor 2:1117–1142Google Scholar
  111. Papavizas G (1985) Trichoderma and Gliocladium: biology, ecology, and potential for biocontrol. Annu Rev Phytopathol 23(1):23–54CrossRefGoogle Scholar
  112. Parry DW, Jenkinson P, McLeod L (1995) Fusarium ear blight (scab) in small grain cereals-a review. Plant Pathol 44(2):207–238. doi: 10.1111/j.1365-3059.1995.tb02773.x CrossRefGoogle Scholar
  113. Paterson RRM, Lima N (2010) How will climate change affect mycotoxins in food? Food Res Int 43(7):1902–1914. doi: 10.1016/j.foodres.2009.07.010 CrossRefGoogle Scholar
  114. Paulitz TC, Bélanger RR (2001) Biological control in greenhouse systems. Annu Rev Phytopathol 39(1):103–133. doi: 10.1146/annurev.phyto.39.1.103 PubMedCrossRefGoogle Scholar
  115. Pertot I, Zasso R, Amsalem L, Baldessari M, Angeli G, Elad Y (2004) Use of biocontrol agents against powdery mildew in integrated strategies for reducing pesticide residues on strawberry: evaluation of efficacy and side effects. IOBC WORS Bulletin 27(8):109–113Google Scholar
  116. Pestka JJ, Smolinski AT (2005) Deoxynivalenol: toxicology and potential effects on humans. J Toxicol Environ Health, Part B 8(1):39–69. doi: 10.1080/10937400590889458 CrossRefGoogle Scholar
  117. Ponts N, Pinson-Gadais L, Boutigny A-L, Barreau C, Richard-Forget F (2011) Cinnamic-derived acids significantly affect Fusarium graminearum growth and in vitro synthesis of type B trichothecenes. Phytopathology 101(8):929–934. doi: 10.1094/PHYTO-09-10-0230 PubMedCrossRefGoogle Scholar
  118. Reino J, Guerrero R, Hernández-Galán R, Collado I (2008) Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem Rev 7(1):89–123. doi: 10.1007/s11101-006-9032-2 CrossRefGoogle Scholar
  119. Riley RT, Enongene E, Voss KA, Norred WP, Meredith FI, Sharma RP, Spitsbergen J, Williams DE, Carlson DB, Merrill AH Jr (2001) Sphingolipid perturbations as mechanisms for fumonisin carcinogenesis. Environ Health Perspect 109:301–308. doi: 10.2307/3435022 PubMedPubMedCentralCrossRefGoogle Scholar
  120. Rodríguez MA, Cabrera G, Gozzo FC, Eberlin MN, Godeas A (2011) Clonostachys rosea BAFC3874 as a Sclerotinia sclerotiorum antagonist: mechanisms involved and potential as a biocontrol agent. J Appl Microbiol 110(5):1177–1186. doi: 10.1111/j.1365-2672.2011.04970.x PubMedCrossRefGoogle Scholar
  121. Roush WR, Russo-Rodriguez S (1987) Trichothecene degradation studies. 3. Synthesis of 12,13-deoxy-12,13-methanoanguidine and 12-epianguidine, two optically active analogs of the epoxytrichothecene mycotoxin anguidine. J Organic Chem 52(4):603–606. doi: 10.1021/jo00380a022 CrossRefGoogle Scholar
  122. Rousseau A, Benhamou N, Chet I, Piché Y (1996) Mycoparasitism of the extramatrical phase of Glomus intraradices by Trichoderma harzianum. Phytopathology 86(5):434–443CrossRefGoogle Scholar
  123. Samapundo S, Devlieghere F, De Meulenaer B, Geeraerd AH, Van Impe JF, Debevere JM (2005) Predictive modelling of the individual and combined effect of water activity and temperature on the radial growth of Fusarium verticilliodes and F. proliferatum on corn. Int J Food Microbiol 105(1):35–52. doi: 10.1016/j.ijfoodmicro.2005.06.007 PubMedCrossRefGoogle Scholar
  124. Samuels GJ, Dodd SL, Gams W, Castlebury LA, Petrini O (2002) Trichoderma species associated with the green mold epidemic of commercially grown Agaricus bisporus. Mycologia 94(1):146–170PubMedCrossRefGoogle Scholar
  125. Sandmeyer LS, Vujanovic V, Petrie L, Campbell JR, Bauer BS, Allen AL, Grahn BH (2015) Optic neuropathy in a herd of beef cattle in Alberta associated with consumption of moldy corn. Canadian Vet J 56(3):249–256Google Scholar
  126. Schmidt-Heydt M, Parra R, Geisen R, Magan N (2011) Modelling the relationship between environmental factors, transcriptional genes and deoxynivalenol mycotoxin production by strains of two Fusarium species. J Royal Soc Interface Royal Soc 8(54):117–126. doi: 10.1098/rsif.2010.0131 CrossRefGoogle Scholar
  127. Schütt F, Nirenberg H, Demi G (1998) Moniliformin production in the genus Fusarium. Mycotoxin Res 14(1):35–40. doi: 10.1007/BF02945091 PubMedCrossRefGoogle Scholar
  128. Sewram V, Mshicileli N, Shephard GS, Vismer HF, Rheeder JP, Lee YW, Leslie JF, Marasas WF (2005) Production of fumonisin B and C analogues by several Fusarium species. J Agric Food Chem 53(12):4861–4866. doi: 10.1021/jf050307n PubMedCrossRefGoogle Scholar
  129. Shier WT, Shier AC, Xie W, Mirocha CJ (2001) Structure-activity relationships for human estrogenic activity in zearalenone mycotoxins. Toxicon 39(9):1435–1438. doi: 10.1016/S0041-0101(00)00259-2 PubMedCrossRefGoogle Scholar
  130. Singh S, Dureja P, Tanwar R, Singh A (2005) Production and antifungal activity of secondary metabolites of Trichoderma virens. Pestic Res J 17(2):26–29Google Scholar
  131. Slifkin MK (1961) Parasitism of Olpidiopsis incrassata on members of the Saprolegniaceae. I. Host range and effects of light, temperature, and stage of host on infectivity. Mycologia 53(2):183–193. doi: 10.2307/3756236 CrossRefGoogle Scholar
  132. Soriano JM, González L, Catalá AI (2005) Mechanism of action of sphingolipids and their metabolites in the toxicity of fumonisin B1. Prog Lipid Res 44(6):345–356. doi: 10.1016/j.plipres.2005.09.001 PubMedCrossRefGoogle Scholar
  133. Sundheim L (1982) Control of cucumber powdery mildew by the hyperparasite Ampelomyces quisqualis and fungicides. Plant Pathol 31(3):209–214. doi: 10.1111/j.1365-3059.1982.tb01270.x CrossRefGoogle Scholar
  134. Sundheim L, Krekling T (1982) Host-parasite relationships of the hyperparasite Ampelomyces quisqualis and its powdery mildew host Sphaerotheca fuliginea. J Phytopathol 104(3):202–210CrossRefGoogle Scholar
  135. Takahashi-Ando N, Kimura M, Kakeya H, Osada H, Yamaguchi I (2002) A novel lactonohydrolase responsible for the detoxification of zearalenone: enzyme purification and gene cloning. Biochem J 365(Pt 1):1–6. doi: 10.1042/bj20020450 PubMedPubMedCentralCrossRefGoogle Scholar
  136. Tijerino A, Hermosa R, Cardoza RE, Moraga J, Malmierca MG, Aleu J, Collado IG, Monte E, Gutierrez S (2011) Overexpression of the Trichoderma brevicompactum tri5 gene: effect on the expression of the trichodermin biosynthetic genes and on tomato seedlings. Toxins 3(9):1220–1232. doi: 10.3390/toxins3091220 PubMedPubMedCentralCrossRefGoogle Scholar
  137. Tsitsigiannis DI, Dimakopoulou M, Antoniou PP, Tjamos EC (2012) Biological control strategies of mycotoxigenic fungi and associated mycotoxins in Mediterranean basin crops. Phytopathologia Mediterranea. doi: 10.14601/Phytopathol_Mediterr-9497 Google Scholar
  138. Ueno Y, Nakajima M, Sakai K, Ishii K, Sato N, Shimada N (1973) Comparative toxicology of Trichothec mycotoxins: inhibition of protein synthesis in animal cells. J Biochem 74(2):285–296PubMedGoogle Scholar
  139. Vargas WA, Mukherjee PK, Laughlin D, Wiest A, Moran-Diez ME, Kenerley CM (2014) Role of gliotoxin in the symbiotic and pathogenic interactions of Trichoderma virens. Microbiology (Reading, England) 160(10):2319–2330. doi: 10.1099/mic.0.079210-0 CrossRefGoogle Scholar
  140. Voss KA, Smith GW, Haschek WM (2007) Fumonisins: Toxicokinetics, mechanism of action and toxicity. Anim Feed Sci Technol 137(3–4):299–325. doi: 10.1016/j.anifeedsci.2007.06.007 CrossRefGoogle Scholar
  141. Vujanovic V, Chau HW (2012) Monitoring Fusarium complex mycelia replacement by mycopathogenic Sphaerodes using alcohol percentage test, qRT-PCR and HPLC. Physiol Mol Plant Pathol 80:28–34. doi: 10.1016/j.pmpp.2012.07.004 CrossRefGoogle Scholar
  142. Vujanovic V, Goh YK (2009) Sphaerodes mycoparasitica sp. nov., a new biotrophic mycoparasite on Fusarium avenaceum, F. graminearum and F. oxysporum. Mycol Res 113:1172–1180. doi: 10.1016/j.mycres.2009.07.018 PubMedCrossRefGoogle Scholar
  143. Vujanovic V, Goh YK (2010) Sphaerodes mycoparasites and new Fusarium hosts for S. mycoparasitica. Mycotaxon 114(1):179–191CrossRefGoogle Scholar
  144. Vujanovic V, Goh YK (2011a) Mycoparasites of Fusarium pathogens on wheat: from taxonomy, genomics and proteomics to biotechnology. In: Wheat: genetics, crops and food production. Agriculture issues and policies. Nova Science Publishers, Hauppauge, NY, USA, pp. 297–314Google Scholar
  145. Vujanovic V, Goh YK (2011b) Sphaerodes mycoparasitica biotrophic mycoparasite of 3-acetyldeoxynivalenol- and 15-acetyldeoxynivalenol-producing toxigenic Fusarium graminearum chemotypes. FEMS Microbiol Lett 316(2):136–143. doi: 10.1111/j.1574-6968.2010.02201.x PubMedCrossRefGoogle Scholar
  146. Vujanovic V, Goh YK (2012) qPCR quantification of Sphaerodes mycoparasitica biotrophic mycoparasite interaction with Fusarium graminearum: in vitro and in planta assays. Arch Microbiol. doi: 10.1007/s00203-012-0807-0 PubMedGoogle Scholar
  147. Weindling R (1934) Studies on a lethal principle effective in the parasitic action of Trichoderma lignorum on Rhizoctonia solani and other soil fungi. Phytopathology 24(1):153–151Google Scholar
  148. Westerberg UB, Bolcsfoldi G, Eliasson E (1976) Control of transfer RNA synthesis in the presence of inhibitors of protein synthesis. Biochim Biophys Acta 447(2):203–213PubMedCrossRefGoogle Scholar
  149. Whipps JM, Gerlagh M (1992) Biology of Coniothyrium minitans and its potential for use in disease biocontrol. Mycol Res 96(11):897–907. doi: 10.1016/S0953-7562(09)80588-1 CrossRefGoogle Scholar
  150. Wilcoxson R, Kommedahl T, Ozmon E, Windels C (1988) Occurrence of Fusarium species in scabby wheat from Minnesota and their pathogenicity to wheat. Phytopathology 78(5):586–589CrossRefGoogle Scholar
  151. Wright JM (1952) Production of gliotoxin in unsterilized soil. Nature 170(4329):673–674CrossRefGoogle Scholar
  152. Xue AG (2003) Biological control of pathogens causing root rot complex in Field pea using Clonostachys rosea strain ACM941. Phytopathology 93(3):329–335. doi: 10.1094/PHYTO.2003.93.3.329 PubMedCrossRefGoogle Scholar
  153. Yazar S, Omurtag GZ (2008) Fumonisins, trichothecenes and zearalenone in cereals. Int J Mol Sci 9(11):2062–2090. doi: 10.3390/ijms9112062 PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Food and Bioproduct SciencesUniversity of SaskatchewanSaskatoonCanada

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