Skip to main content
SpringerLink
Log in

Application of Fungal Metabolites Against Mycotoxins Production

  • Reference work entry
  • First Online:
Fungal Metabolites

Part of the book series: Reference Series in Phytochemistry ((RSP))

Abstract

Mycotoxins are toxic substances produced by fungi that contaminate various food and feedstuffs. There are about 100 different types of mycotoxins which are produced by a wide range of fungal species. The variety of their toxicity is linked to the diversity of their chemical structure. Amongst them, three biosynthesis origins are mostly studied: the polyketides (e.g., aflatoxins, fumonisins), the terpenes (e.g., trichothecenes), and the ergot alkaloids (e.g., ergotamine). In this chapter we present those biosynthetic origins and focus on the mycotoxins threatening human health. Their biosynthesis, producing fungi, toxicity, and regulation are succinctly presented. In the second part of the chapter, we focus our attention on fungal metabolites as a potential source of biocontrol, being antifungal, impacting both fungal growth and mycotoxins production and preventing mycotoxins biosynthesis. We finally conclude on the wide diversity of mycotoxins origins and the need to pursue the discovery of new fungal metabolites to counteract mycotoxins production.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Institutional subscriptions

References

  1. Online Etymology Dictionary (2014) Mycotoxin. http://www.etymonline.com/index.php. Accessed 9 Nov 2015

  2. Van Dongen PWJ, De Groot ANJA (1995) History of ergot alkaloids from ergotism to ergometrine. Eur J Obstet Gynecol Reprod Biol 60:109–116

    Article  Google Scholar 

  3. Cole RJ (1986) Etiology of Turkey “X” disease in retrospect: a case for the involvement of cyclopiazonic acid. Mycotoxin Res 2:3–7

    Article  CAS  Google Scholar 

  4. Nesbitt BF, O’kelly J, Sargeant K, Sheridan A (1962) Aspergillus flavus and Turkey X disease: toxic metabolites of Aspergillus flavus. Nature 195:1062–1063

    Article  CAS  Google Scholar 

  5. International Agency for Research on Cancer (2012) IARC publications list. http://www.iarc.fr/en/publications/list/. Accessed 9 Nov 2015

  6. Ross RK, Yu MC, Henderson BE, Yuan J-M, Qian G-S, Tu J-T, Gao Y-T, Wogan GN, Groopman JD (1992) Urinary aflatoxin biomarkers and risk of hepatocellular carcinoma. Lancet 339:943–946

    Article  CAS  Google Scholar 

  7. Qian GS, Ross RK, Yu MC, Yuan JM, Gao YT, Henderson BE, Wogan GN, Groopman JD (1994) A follow-up study of urinary markers of aflatoxin exposure and liver cancer risk in Shanghai, People’s Republic of China. Cancer Epidemiol Biomarkers Prev 3:3–10

    CAS  Google Scholar 

  8. Wang LY, Hatch M, Chen CJ, Levin B, You SL, Lu SN, Wu MH, Wu WP, Wang LW, Wang Q, Huang GT, Yang PM, Lee HS, Santella RM (1996) Aflatoxin exposure and risk of hepatocellular carcinoma in Taiwan. Int J Cancer 67:620–625

    Article  CAS  Google Scholar 

  9. Bennett JW, Klich M (2003) Mycotoxins. Clin Microbiol Rev 16:497–516

    Article  CAS  Google Scholar 

  10. Boudergue C, Burel C, Dragacci S, Favrot M-C, Fremy J-M, Massimi C, Prigent P, Debongnie P, Pussemier L, Boudra H, Morgavi D, Oswald IP, Perez A, Avantaggiato G (2009) External scientific report: review of mycotoxin-detoxifying agents used as feed additives: mode of action, efficacy and feed/food safety. http://www.efsa.europa.eu/fr/supporting/pub/22e.htm. Accessed 9 Nov 2015

  11. Holmquist GU, Walker HW, Stahr HM (1983) Influence of temperature, pH water activity and antifungal agents on growth of Aspergillus flavus and A. parasiticus. J Food Sci 48:778–782

    Article  CAS  Google Scholar 

  12. Riba A, Bouras N, Mokrane S, Mathieu F, Lebrihi A, Sabaou N (2010) Aspergillus section Flavi and aflatoxins in Algerian wheat and derived products. Food Chem Toxicol 48:2772–2777

    Article  CAS  Google Scholar 

  13. El Mahgubi A, Puel O, Bailly S, Tadrist S, Querin A, Ouadia A, Oswald IP, Bailly JD (2013) Distribution and toxigenicity of Aspergillus section Flavi in spices marketed in Morocco. Food Control 32:143–148

    Article  CAS  Google Scholar 

  14. Taniwaki MH, Teixeira AA, Teixeira ARR, Copetti MV, Iamanaka BT (2014) Ochratoxigenic fungi and ochratoxin A in defective coffee beans. Food Res Int 61:161–166

    Article  CAS  Google Scholar 

  15. Ostry V, Malir F, Dofkova M, Skarkova J, Pfohl-Leszkowicz A, Ruprich J (2015) Ochratoxin A dietary exposure of ten population groups in the Czech Republic: comparison with data over the World. Toxins 7:3608–3635

    Article  CAS  Google Scholar 

  16. Aït Mimoune N, Riba A, Verheecke C, Mathieu F, Sabaou N (2015) Fungal contamination and mycotoxin production by Aspergillus spp. isolated from dried fruits and sesames seeds. J Microbiol Biotechn Food Sci 5:301–305

    Google Scholar 

  17. Nordkvist E, Häggblom P (2014) Fusarium mycotoxin contamination of cereals and bedding straw at Swedish pig farms. Anim Feed Sci Technol 198:231–237

    Article  CAS  Google Scholar 

  18. Van De Perre E, Deschuyffeleer N, Jacxsens L, Vekeman F, Van Der Hauwaert W, Asam S, Rychlik M, Devlieghere F, De Meulenaer B (2014) Screening of moulds and mycotoxins in tomatoes, bell peppers, onions, soft red fruits and derived tomato products. Food Control 37:165–170

    Article  CAS  Google Scholar 

  19. Oliveira PM, Zannini E, Arendt EK (2014) Cereal fungal infection, mycotoxins, and lactic acid bacteria mediated bioprotection: from crop farming to cereal products. Food Microbiol 37:78–95

    Article  CAS  Google Scholar 

  20. Cunha SC, Faria MA, Pereira VL, Oliveira TM, Lima AC, Pinto E (2014) Patulin assessment and fungi identification in organic and conventional fruits and derived products. Food Control 44:185–190

    Article  CAS  Google Scholar 

  21. Grenier B, Loureiro-Bracarense A-P, Leslie JF, Oswald IP (2014) Physical and chemical methods for mycotoxin decontamination in maize. In: Leslie JF, Logrieco A (eds) Mycotoxin reduction in grain chains, 1st edn. Wiley, New York

    Google Scholar 

  22. Jard G, Liboz T, Mathieu F, Guyonvarc’h A, Lebrihi A (2011) Review of mycotoxin reduction in food and feed: from prevention in the field to detoxification by adsorption or transformation. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 28:1590–1609

    Article  CAS  Google Scholar 

  23. Gallo A, Ferrara M, Perrone G (2013) Phylogenetic study of polyketide synthases and nonribosomal peptide synthetases involved in the biosynthesis of mycotoxins. Toxins 5:717–742

    Article  CAS  Google Scholar 

  24. Watanabe CMH, Townsend CA (2002) Initial characterization of a type I fatty acid synthase and polyketide synthase multienzyme complex NorS in the biosynthesis of aflatoxin B1. Chem Biol 9:981–988

    Article  CAS  Google Scholar 

  25. Ehrlich KC (2009) Predicted roles of the uncharacterized clustered genes in aflatoxin biosynthesis. Toxins 1:37–58

    Article  CAS  Google Scholar 

  26. Yu J (2012) Current understanding on aflatoxin biosynthesis and future perspective in reducing aflatoxin contamination. Toxins 4:1024–1057

    Article  CAS  Google Scholar 

  27. Georgianna DR, Payne GA (2009) Genetic regulation of aflatoxin biosynthesis: from gene to genome. Fungal Genet Biol 46:113–125

    Article  CAS  Google Scholar 

  28. Dorner JW, Cole RJ, Diener UL (1984) The relationship of Aspergillus flavus and Aspergillus parasiticus with reference to production of aflatoxins and cyclopiazonic acid. Mycopathologia 87:13–15

    Article  CAS  Google Scholar 

  29. Kurtzman CP, Horn BW, Hesseltine CW (1987) Aspergillus nomius, a new aflatoxin-producing species related to Aspergillus flavus and Aspergillus tamarii. Antonie Van Leeuwenhoek 53:147–158

    Article  CAS  Google Scholar 

  30. Schmidt-Heydt M, Häckel S, Rüfer C, Geisen R (2009) A strain of Fusarium kyushuense is able to produce aflatoxin B1 and G1. Mycotoxin Res 25:141–147

    Article  CAS  Google Scholar 

  31. Ehrlich K, Yu J, Cotty P (2005) Aflatoxin biosynthesis gene clusters and flanking regions. J Appl Microbiol 99:518–527

    Article  CAS  Google Scholar 

  32. Roze LV, Chanda A, Linz JE (2011) Compartmentalization and molecular traffic in secondary metabolism: a new understanding of established cellular processes. Fungal Genet Biol 48:35–48

    Article  CAS  Google Scholar 

  33. Peers FG, Linsell CA (1977) Dietary aflatoxins and human primary liver cancer. Ann Nutr Aliment 31:1005–1017

    CAS  Google Scholar 

  34. Williams JH, Phillips TD, Jolly PE, Stiles JK, Jolly CM, Aggarwal D (2004) Human aflatoxicosis in developing countries: a review of toxicology, exposure, potential health consequences, and interventions. Am J Clin Nutr 80:1106–1122

    CAS  Google Scholar 

  35. International Agency for Research on Cancer (2012) A review of human carcinogens: chemical agents and related occupations. http://monographs.iarc.fr/ENG/Monographs/vol100F/mono100F-23.pdf. Accessed 9 Nov 2015

  36. Food and Drug Administration (2012) Natural toxins: aflatoxins. In: FDA (ed) Bad bug book, foodborne pathogenic microorganisms and natural toxins, 2nd edn. FDA, Silver Spring

    Google Scholar 

  37. Lizárraga-Paulín EG, Moreno-Martínez E, Miranda-Castro SP (2011) Aflatoxins and their impact on human and animal health: an emerging problem. In: Guevara-Gonzalez RG (ed) Aflatoxins biochemistry and molecular biology, 1st edn. InTech, Rijeka

    Google Scholar 

  38. Krishnamachari KAVR, Nagarajan V, Bhat R, Tilak TBG (1975) Hepatitis due to aflatoxicosis: an outbreak in Western India. Lancet 305:1061–1063

    Article  Google Scholar 

  39. Nyikal J, Misore A, Nzioka C, Njuguna C, Muchiri E, Njau J, Maingi S, Njoroge J, Mutiso J, Onteri J, Langat A, Kilei IK, Nyamongo J, Ogana G, Muture B, Tukei P, Onyango C, Ochieng W, Tetteh C, Likimani S, Nguku P, Galgalo T, Kibet S, Manya A, Dahiye A, Mwihia J, Mugoya I, Onsongo J, Ngindu A, DeCock KM, Lindblade K, Slutsker L, Amornkul P, Rosen D, Feiken D, Thomas T, Mensah P, Eseko N, Nejjar A, Onsongo M, Kessel F, Njapau H, Park DL, Lewis L, Luber G, Rogers H, Backer L, Rubin C, Gieseker KE, Azziz-Baumgartner E, Chege W, Bowen A (2004) Outbreak of aflatoxin poisoning – Eastern and Central Provinces, Kenya. Morbidity and Mortality Weekly Report. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5334a4.htm. Accessed 9 Nov 2015

  40. Wu HC, Wang Q, Yang H-I, Ahsan H, Tsai W-Y, Wang L-Y, Chen S-Y, Chen C-J, Santella RM (2009) Aflatoxin B1 exposure, hepatitis B virus infection, and hepatocellular carcinoma in Taiwan. Cancer Epidemiol Biomarkers Prev 18:846–853

    Article  CAS  Google Scholar 

  41. Jiang Y, Jolly PE, Ellis WO, Wang J-S, Phillips TD, Williams JH (2005) Aflatoxin B1 albumin adduct levels and cellular immune status in Ghanaians. Int Immunol 17:807–814

    Article  CAS  Google Scholar 

  42. Jolly PE, Shuaib FM, Jiang Y, Preko P, Baidoo J, Stiles JK, Wang J-S, Phillips TD, Williams JH (2011) Association of high viral load and abnormal liver function with high aflatoxin B1–albumin adduct levels in HIV-positive Ghanaians: preliminary observations. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 28:1224–1234

    Article  CAS  Google Scholar 

  43. Gong Y, Hounsa A, Egal S, Turner PC, Sutcliffe AE, Hall AJ, Cardwell K, Wild CP (2004) Postweaning exposure to aflatoxin results in impaired child growth: a longitudinal study in Benin, West Africa. Environ Health Perspect 112:1334–1338

    Article  CAS  Google Scholar 

  44. Ibeh IN, Uraih N, Ogonar JI (1994) Dietary exposure to aflatoxin in human male infertility in Benin City, Nigeria. Int J Fertil Menopausal Stud 39:208–214

    CAS  Google Scholar 

  45. European Union (2006) Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs. European Union laws and publications. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2006:364:0005:0024:EN:PDF. Accessed 9 Nov 2015

  46. Shimizu T, Kinoshita H, Ishihara S, Sakai K, Nagai S, Nihira T (2005) Polyketide synthase gene responsible for citrinin biosynthesis in Monascus purpureus. Appl Environ Microbiol 71:3453–3457

    Article  CAS  Google Scholar 

  47. Hetherington AC, Raistrick H (1931) On the production and chemical constitution of a new yellow colouring matter, citrinin, produced from glucose by Penicillium citrinum Thom. Philos Trans R Soc Lond B Biol Sci 220:269–295

    Article  Google Scholar 

  48. Dame Z, Suwannarach N, Lumyong S, Laatsch H (2015) A new citrinin dimer isolated from Aspergillus terreus strain ZDF21. Nat Prod Commun 10:623–624

    Google Scholar 

  49. Frisvad JC, Smedsgaard J, Larsen TO, Samson RA (2004) Mycotoxins, drugs and other extrolites produced by species in Penicillium subgenus Penicillium. Stud Mycol 49:201–241

    Google Scholar 

  50. Visagie CM, Houbraken J, Frisvad JC, Hong S-B, Klaassen CHW, Perrone G, Seifert KA, Varga J, Yaguchi T, Samson RA (2014) Identification and nomenclature of the genus Penicillium. Stud Mycol 78:343–371

    Article  CAS  Google Scholar 

  51. Houbraken J, Frisvad JC, Samson RA (2011) Taxonomy of Penicillium section Citrina. Stud Mycol 70:53–138

    Article  CAS  Google Scholar 

  52. Samson RA, Peterson SW, Frisvad JC, Varga J (2011) New species in Aspergillus section Terrei. Stud Mycol 69:39–55

    Article  CAS  Google Scholar 

  53. Blanc PJ, Loret MO, Goma G (1995) Production of citrinin by various species of Monascus. Biotechnol Lett 17:291–294

    Article  CAS  Google Scholar 

  54. EFSA Panel on Contaminants in the Food Chain (CONTAM) (2012) Scientific opinion on the risks for public and animal health related to the presence of citrinin in food and feed. EFSA J 10:2605

    Article  CAS  Google Scholar 

  55. Li Y, Xu Y, Huang Z (2011) Isolation and characterization of the citrinin biosynthetic gene cluster from Monascus aurantiacus. Biotechnol Lett 34:131–136

    Article  CAS  Google Scholar 

  56. IARC (1987) IARC monographs on the evaluation of carcinogenic risks to humans – volume 40: some naturally occurring and synthetic food components, furocoumarins and ultraviolet radiation. http://monographs.iarc.fr/ENG/Monographs/vol1-42/mono40.pdf. Accessed 9 Nov 2015

  57. Mehdi NAQ, Carlton WW, Tuite J (1983) Acute toxicity of citrinin in turkeys and ducklings. Avian Pathol 12:221–233

    Article  CAS  Google Scholar 

  58. Reddy RV, Maruya K, Wallace Hayes A, Bernd WO (1982) Embryocidal teratogenic and fetotoxic effects of citrinin in rats. Toxicology 25:151–160

    Article  CAS  Google Scholar 

  59. Flajs D, Peraica M (2009) Toxicological properties of citrinin. Arh Hig Rada Toksikol 60:457–464

    Article  CAS  Google Scholar 

  60. Knasmuller S, Cavin C, Chakraborty A, Darroudi F, Majer BJ, Huber WW, Ehrlich VA (2004) Structurally related mycotoxins ochratoxin A, ochratoxin B, and citrinin differ in their genotoxic activities and in their mode of action in human-derived liver (HepG2) cells: implications for risk assessment. Nutr Cancer 50:190–197

    Article  Google Scholar 

  61. Braunberg RC, Barton CN, Gantt OO, Friedman L (1994) Interaction of citrinin and ochratoxin A. Nat Toxins 2:124–131

    Article  CAS  Google Scholar 

  62. Proctor RH, Desjardins AE, Plattner RD, Hohn TM (1999) A polyketide synthase gene required for biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal Genet Biol 27:100–112

    Article  CAS  Google Scholar 

  63. Bojja RS, Cerny RL, Proctor RH, Du L (2004) Determining the biosynthetic sequence in the early steps of the fumonisin pathway by use of three gene-disruption mutants of Fusarium verticillioides. J Agric Food Chem 52:2855–2860

    Article  CAS  Google Scholar 

  64. Rheeder JP, Marasas WFO, Vismer HF (2002) Production of fumonisin analogs by Fusarium species. Appl Environ Microbiol 68:2101–2105

    Article  CAS  Google Scholar 

  65. Frisvad JC, Smedsgaard J, Samson RA, Larsen TO, Thrane U (2007) Fumonisin B2 production by Aspergillus niger. J Agric Food Chem 55:9727–9732

    Article  CAS  Google Scholar 

  66. Varga J, Kocsubé S, Szigeti G, baranyi N, Toth B (2015) Aspergillus mycotoxins. In: Paterson RRM, Lima N (eds) Molecular biology of food and water borne mycotoxigenic and mycotic fungi, 1st edn. Taylor and Francis, Brighton

    Google Scholar 

  67. Sewram V, Mshicileli N, Shephard GS, Vismer HF, Rheeder JP, Lee Y-W, Leslie JF, Marasas WFO (2005) Production of fumonisin B and C analogues by several Fusarium species. J Agric Food Chem 53:4861–4866

    Article  CAS  Google Scholar 

  68. Proctor RH, Plattner RD, Brown DW, Seo J-A, Lee Y-W (2004) Discontinuous distribution of fumonisin biosynthetic genes in the Gibberella fujikuroi species complex. Mycol Res 108:815–822

    Article  CAS  Google Scholar 

  69. Proctor RH, Busman M, Seo J-A, Lee YW, Plattner RD (2008) A fumonisin biosynthetic gene cluster in Fusarium oxysporum strain O-1890 and the genetic basis for B versus C fumonisin production. Fungal Genet Biol 45:1016–1026

    Article  CAS  Google Scholar 

  70. IARC (2002) IARC monographs on the evaluation of carcinogenic risks to humans – volume 82: some traditional herbal medicines, some mycotoxins, naphthalene and styrene. http://monographs.iarc.fr/ENG/Monographs/vol82/mono82.pdf. Accessed 9 Nov 2015

  71. Ross PF, Nelson PE, Owens DL, Rice LG, Nelson HA, Wilson TM (1994) Fumonisin B2 in cultured Fusarium proliferatum, M-6104, causes equine leukoencephalomalacia. J Vet Diagn Invest 6:263–265

    Article  CAS  Google Scholar 

  72. Rheeder JP, Marasas WFO, Theil PG, Sydenham EW, Shephard GS, Van Schalkwyk DJ (1992) Fusarium moniliforme and fumonisins in corn in relation to human esophageal cancer in Transkei. Phytopathology 82:353–357

    Article  Google Scholar 

  73. Yoshizawa T, Yamashita A, Luo Y (1994) Fumonisin occurrence in corn from high- and low-risk areas for human esophageal cancer in China. Appl Environ Microbiol 60:1626–1629

    CAS  Google Scholar 

  74. D’Mello JPF, Placinta CM, Macdonald AMC (1999) Fusarium mycotoxins: a review of global implications for animal health, welfare and productivity. Anim Feed Sci Technol 80:183–205

    Article  Google Scholar 

  75. Atoui A, Phong Dao H, Mathieu F, Lebrihi A (2006) Amplification and diversity analysis of ketosynthase domains of putative polyketide synthase genes in Aspergillus ochraceus and Aspergillus carbonarius producers of ochratoxin A. Mol Nutr Food Res 50:488–493

    Article  CAS  Google Scholar 

  76. Bacha N, Atoui A, Mathieu F, Liboz T, Lebrihi A (2009) Aspergillus westerdijkiae polyketide synthase gene “aoks1” is involved in the biosynthesis of ochratoxin A. Fungal Genet Biol 46:77–84

    Article  CAS  Google Scholar 

  77. Wang L, Wang Y, Wang Q, Liu F, Selvaraj JN, Liu L, Xing F, Zhao Y, Zhou L, Liu Y (2015) Functional characterization of new polyketide synthase genes involved in ochratoxin A biosynthesis in Aspergillus ochraceus fc-1. Toxins 7:2723–2738

    Article  CAS  Google Scholar 

  78. Gil-Serna J, Vázquez C, Sardiñas N, González-Jaén MT, Patiño B (2011) Revision of ochratoxin A production capacity by the main species of Aspergillus section Circumdati. Aspergillus steynii revealed as the main risk of OTA contamination. Food Control 22:343–345

    Article  CAS  Google Scholar 

  79. Gil-Serna J, Vazquez C, Sandino FG, Valle AM, Gonzalez-Jaen MT, Patino B (2014) Evaluation of growth and ochratoxin A production by Aspergillus steynii and Aspergillus westerdijkiae in green-coffee based medium under different environmental conditions. Food Res Int 61:127–131

    Article  CAS  Google Scholar 

  80. Covarelli L, Beccari G, Marini A, Tosi L (2012) A review on the occurrence and control of ochratoxigenic fungal species and ochratoxin A in dehydrated grapes, non-fortified dessert wines and dried vine fruit in the Mediterranean area. Food Control 26:347–356

    Article  CAS  Google Scholar 

  81. Joosten HMLJ, Goetz J, Pittet A, Schellenberg M, Bucheli P (2001) Production of ochratoxin A by Aspergillus carbonarius on coffee cherries. Int J Food Microbiol 65:39–44

    Article  CAS  Google Scholar 

  82. Cabañes FJ, Bragulat MR, Castellá G (2010) Ochratoxin A producing species in the genus Penicillium. Toxins 2:1111–1120

    Article  CAS  Google Scholar 

  83. Pitt JI (1987) Penicillium viridicatum, Penicillium verrucosum, and production of ochratoxin A. Appl Environ Microbiol 53:266–269

    CAS  Google Scholar 

  84. IARC (1993) IARC monographs on the evaluation of carcinogenic risks to humans – volume 56: some naturally occurring substances: food items and constituents, heterocyclic aromatic amines and mycotoxins. http://monographs.iarc.fr/ENG/Monographs/vol56/mono56.pdf. Accessed 9 Nov 2015

  85. Ringot D, Chango A, Schneider Y-J, Larondelle Y (2006) Toxicokinetics and toxicodynamics of ochratoxin A, an update. Chem Biol Interact 159:18–46

    Article  CAS  Google Scholar 

  86. World Health Organization (1990) International programme on chemical safety. The international programme on chemical safety. http://www.inchem.org/documents/ehc/ehc/ehc105.htm. Accessed 9 Nov 2015

  87. Batuman V (2006) Fifty years of Balkan endemic nephropathy: daunting questions, elusive answers. Kidney Int 69:644–646

    Article  CAS  Google Scholar 

  88. Hayes AW, Hood RD, Lee HL (1974) Teratogenic effects of ochratoxin A in mice. Teratology 9:93–97

    Article  CAS  Google Scholar 

  89. Boorman GA, Mcdonald MR, Imoto S, Persing R (1992) Renal lesions induced by ochratoxin A exposure in the F344 rat. Toxicol Pathol 20:236–245

    Article  CAS  Google Scholar 

  90. Castegnaro M, McGregor D (1998) Carcinogenic risk assessment of mycotoxins. Rev Med Vet (France) 149:671–678

    CAS  Google Scholar 

  91. Al-Anati L, Petzinger E (2006) Immunotoxic activity of ochratoxin A. J Vet Pharmacol Ther 29:79–90

    Article  CAS  Google Scholar 

  92. Palma N, Cinelli S, Sapora O, Wilson SH, Dogliotti E (2007) Ochratoxin A-induced mutagenesis in mammalian cells is consistent with the production of oxidative stress. Chem Res Toxicol 20:1031–1037

    Article  CAS  Google Scholar 

  93. Birch A, Massy-Westropp R, Moye C (1955) Studies in relation to biosynthesis. VII. 2-Hydroxy-6-methylbenzoic acid in Penicillium griseofulvum Dierckx. Aus J Chem 8:539–544

    Article  CAS  Google Scholar 

  94. Moake MM, Padilla-Zakour OI, Worobo RW (2005) Comprehensive review of patulin control methods in foods. Compr Rev Food Sci Food Saf 4:8–21

    Article  CAS  Google Scholar 

  95. Varga J, Due M, Frisvad JC, Samson RA (2007) Taxonomic revision of Aspergillus section Clavati based on molecular, morphological and physiological data. Stud Mycol 59:89–106

    Article  CAS  Google Scholar 

  96. Artigot MP, Loiseau N, Laffitte J, Mas-Reguieg L, Tadrist S, Oswald IP, Puel O (2009) Molecular cloning and functional characterization of two CYP619 cytochrome P450s involved in biosynthesis of patulin in Aspergillus clavatus. Microbiology 155:1738–1747

    Article  CAS  Google Scholar 

  97. Puel O, Galtier P, Oswald IP (2010) Biosynthesis and toxicological effects of patulin. Toxins (Basel) 2:613–631

    Article  CAS  Google Scholar 

  98. Pfohl-Leszkowicz A (1999) Mycotoxins in food: evaluation and risk management. In: Ministère de l’emploi et de la solidarité (ed) Les mycotoxines dans l’alimentation: évaluation et gestion du risque, 1st edn. Technique et Documentation Lavoisier, Paris

    Google Scholar 

  99. Osswald H, Frank HK, Komitowski D, Winter H (1978) Long-term testing of patulin administered orally to Sprague–Dawley rats and swiss mice. Food Cosmet Toxicol 16:243–247

    Article  CAS  Google Scholar 

  100. Paucod J, Krivobok S, Vidal D (1989) Immunotoxicity testing of mycotoxins T-2 and patulin on Balb/c mice. Acta Microbiol Hung 37:331–339

    Google Scholar 

  101. Llewellyn GC, McCay JA, Brown RD, Musgrove DL, Butterworth LF, Munson AE, White KL Jr (1998) Immunological evaluation of the mycotoxin patulin in female b6C3F1 mice. Food Chem Toxicol 36:1107–1115

    Article  CAS  Google Scholar 

  102. 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 58:1102–1113

    Article  CAS  Google Scholar 

  103. Steele JA, Lieberman JR, Mirocha CJ (1974) Biogenesis of zearalenone (F-2) by Fusarium roseum ‘Graminearum’. Can J Microbiol 20:531–534

    Article  CAS  Google Scholar 

  104. Stob M, Baldwin RS, Tuite J, Andrews FN, Gillette KG (1962) Isolation of an anabolic, uterotrophic compound from corn infected with Gibberella zeae. Nature 196:1318

    Article  CAS  Google Scholar 

  105. Zinedine A, Soriano JM, Moltó JC, Mañes J (2007) Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: an oestrogenic mycotoxin. Food Chem Toxicol 45:1–18

    Article  CAS  Google Scholar 

  106. Fitzpatrick DW, Picken CA, Murphy LC, Buhr MM (1989) Measurement of the relative binding affinity of zearalenone, α-zearalenol and β-zearalenol for uterine and oviduct estrogen receptors in swine, rats and chickens: an indicator of estrogenic potencies. Comp Biochem Physiol C 94:691–694

    Article  CAS  Google Scholar 

  107. Ouanes Z, Abid S, Ayed I, Anane R, Mobio T, Creppy EE, Bacha H (2003) Induction of micronuclei by zearalenone in vero monkey kidney cells and in bone marrow cells of mice: protective effect of Vitamin E. Mutat Res 538:63–70

    Article  CAS  Google Scholar 

  108. de Rodriguez CAS, Bongiovanni AM, de Borrego LC (1985) An epidemic of precocious development in Puerto Rican children. J Pediatr 107:393–396

    Article  Google Scholar 

  109. Keller NP, Turner G, Bennett JW (2005) Fungal secondary metabolism – from biochemistry to genomics. Nat Rev Microbiol 3:937–947

    Article  CAS  Google Scholar 

  110. Hohn TM, Vanmiddlesworth F (1986) Purification and characterization of the sesquiterpene cyclase trichodiene synthetase from Fusarium sporotrichioides. Arch Biochem Biophys 251:756–761

    Article  CAS  Google Scholar 

  111. Shank RA, Foroud NA, Hazendonk P, Eudes F, Blackwell BA (2011) Current and future experimental strategies for structural analysis of trichothecene mycotoxins – a prospectus. Toxins (Basel) 3:1518–1553. doi:10.3390/toxins3121518

    Article  CAS  Google Scholar 

  112. McCormick SP, Stanley AM, Stover NA, Alexander NJ (2011) Trichothecenes: from simple to complex mycotoxins. Toxins (Basel) 3:802–814

    Article  CAS  Google Scholar 

  113. Cole RJ, Schweikert MA, Jarvis BB (2003) Handbook of secondary fungal metabolites, 3-volume set. Academic, London

    Google Scholar 

  114. Strub C, Pocaznoi D, Lebrihi A, Fournier R, Mathieu F (2010) Influence of barley malting operating parameters on T-2 and HT-2 toxinogenesis of Fusarium langsethiae, a worrying contaminant of malting barley in Europe. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 27:1247–1252

    Article  CAS  Google Scholar 

  115. Picot A, Hourcade-Marcolla D, Barreau C, Pinson-Gadais L, Caron D, Richard-Forget F, Lannou C (2012) Interactions between Fusarium verticillioides and Fusarium graminearum in maize ears and consequences for fungal development and mycotoxin accumulation. Plant Pathol 61:140–151

    Article  CAS  Google Scholar 

  116. Brown DW, Dyer RB, McCormick SP, Kendra DF, Plattner RD (2004) Functional demarcation of the Fusarium core trichothecene gene cluster. Fungal Genet Biol 41:454–462

    Article  CAS  Google Scholar 

  117. Brown DW, McCormick SP, Alexander NJ, Proctor RH, Desjardins AE (2001) A genetic and biochemical approach to study trichothecene diversity in Fusarium sporotrichioides and Fusarium graminearum. Fungal Genet Biol 32:121–133

    Article  CAS  Google Scholar 

  118. Brown DW, Proctor RH, Dyer RB, Plattner RD (2003) Characterization of a Fusarium 2-gene cluster involved in trichothecene C-8 modification. J Agric Food Chem 51:7936–7944

    Article  CAS  Google Scholar 

  119. Kimura M, Kaneko I, Komiyama M, Takatsuki A, Koshino H, Yoneyama K, Yamaguchi I (1998) Trichothecene 3-O-acetyltransferase protects both the producing organism and transformed yeast from related mycotoxins. Cloning and characterization of Tri101. J Biol Chem 273:1654–1661

    Article  CAS  Google Scholar 

  120. Proctor RH, McCormick SP, Alexander NJ, Desjardins AE (2009) Evidence that a secondary metabolic biosynthetic gene cluster has grown by gene relocation during evolution of the filamentous fungus Fusarium. Mol Microbiol 74:1128–1142

    Article  CAS  Google Scholar 

  121. Proctor RH, Hohn TM, McCormick SP, Desjardins AE (1995) Tri6 encodes an unusual zinc finger protein involved in regulation of trichothecene biosynthesis in Fusarium sporotrichioides. Appl Environ Microbiol 61:1923–1930

    CAS  Google Scholar 

  122. Tag AG, Garifullina GF, Peplow AW, Ake C, Phillips TD, Hohn TM, Beremand MN (2001) A novel regulatory gene, Tri10, controls trichothecene toxin production and gene expression. Appl Environ Microbiol 67:5294–5302

    Article  CAS  Google Scholar 

  123. Li Y, Wang Z, Beier RC, Shen J, Smet DD, De Saeger S, Zhang S (2011) T-2 toxin, a trichothecene mycotoxin: review of toxicity, metabolism, and analytical methods. J Agric Food Chem 59:3441–3453

    Article  CAS  Google Scholar 

  124. Pestka JJ (2007) Deoxynivalenol: toxicity, mechanisms and animal health risks. Anim Feed Sci Technol 137:283–298

    Article  CAS  Google Scholar 

  125. Burel C, Dragacci S, Etienne M, Fremy J-M, Grosjean F, Jouany J-P, Galtier P, Guerre P, Le Bizec B, Leblanc J-C, Paragon B-M, Parent-Massin D, Oswald IP, Thouvenot D, Tard A (2009) Evaluation des risques liés à la présence de mycotoxines dans les chaînes alimentaires humaine et animale. Afssa. https://www.anses.fr/fr/system/files/RCCP-Ra-Mycotoxines2009.pdf. Accessed 9 Nov 2015

  126. Sobrova P, Adam V, Vasatkova A, Beklova M, Zeman L, Kizek R (2010) Deoxynivalenol and its toxicity. Interdiscip Toxicol 3:94–99

    Article  CAS  Google Scholar 

  127. Verstraete F (2013) Presentation on European Union opinions on mycotoxins. In: ISM-MycoRed international conference Europe 2013, Martina-Franca

    Google Scholar 

  128. Dijksterhuis J, Samson RA (2007) Food mycology: a multifaceted approach to fungi and food. CRC Press, New York

    Book  Google Scholar 

  129. Lorenz N, Haarmann T, Pažoutová S, Jung M, Tudzynski P (2009) The ergot alkaloid gene cluster: functional analyses and evolutionary aspects. Phytochemistry 70:1822–1832

    Article  CAS  Google Scholar 

  130. Wallwey C, Li S-M (2011) Ergot alkaloids: structure diversity, biosynthetic gene clusters and functional proof of biosynthetic genes. Nat Prod Rep 28:496–510

    Article  CAS  Google Scholar 

  131. Haarmann T, Machado C, Lübbe Y, Correia T, Schardl CL, Panaccione DG, Tudzynski P (2005) The ergot alkaloid gene cluster in Claviceps purpurea: extension of the cluster sequence and intra species evolution. Phytochemistry 66:1312–1320

    Article  CAS  Google Scholar 

  132. Cornière A (2014) Les alcaloïdes de l’ergot: mycotoxines ré-émergentes? Toxinogénèse et toxicité pour l’homme et les animaux. Dissertation, Ecole Nationale Vétérinaire de Toulouse

    Google Scholar 

  133. European Commission (2008) Commission Regulation (EC) No 687/2008 of 18 July 2008 establishing procedures for the taking-over of cereals by intervention agencies or paying agencies and laying down methods of analysis for determining the quality of cereals (Codified version)

    Google Scholar 

  134. Rosada LJ, Sant’anna JR, Franco CCS, Esquissato GNM, Santos PASR, Yajima JPRS, Ferreira FD, Machinski M, Corrêa B, Castro-Prado MAA (2013) Identification of Aspergillus flavus isolates as potential biocontrol agents of aflatoxin contamination in crops. J Food Prot 76:1051–1055

    Article  CAS  Google Scholar 

  135. Dorner JW (2009) Biological control of aflatoxin contamination in corn using a nontoxigenic strain of Aspergillus flavus. J Food Prot 72:801–804

    Article  CAS  Google Scholar 

  136. Atehnkeng J, Ojiambo PS, Ikotun T, Sikora RA, Cotty PJ, Bandyopadhyay R (2008) Evaluation of atoxigenic isolates of Aspergillus flavus as potential biocontrol agents for aflatoxin in maize. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 25:1264–1271

    Article  CAS  Google Scholar 

  137. Verheecke C, Liboz T, Anson P, Zhu Y, Mathieu F (2015) Streptomyces-Aspergillus flavus interactions: impact on aflatoxin B accumulation. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 32:572–576

    Article  CAS  Google Scholar 

  138. Verheecke C, Liboz T, Darriet M, Sabaou N, Mathieu F (2014) In vitro interaction of actinomycetes isolates with Aspergillus flavus: impact on aflatoxins B1 and B2 production. Lett Appl Microbiol 58:597–603

    Article  CAS  Google Scholar 

  139. Abbas HK, Zablotowicz RM, Horn BW, Phillips NA, Johnson BJ, Jin X, Abel CA (2011) Comparison of major biocontrol strains of non-aflatoxigenic Aspergillus flavus for the reduction of aflatoxins and cyclopiazonic acid in maize. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 28:198–208

    Article  CAS  Google Scholar 

  140. Ponsone ML, Chiotta ML, Palazzini JM, Combina M, Chulze S (2012) Control of ochratoxin A production in grapes. Toxins (Basel) 4:364–372

    Article  CAS  Google Scholar 

  141. Chulze SN, Palazzini JM, Torres AM, Barros G, Ponsone ML, Geisen R, Schmidt-Heydt M, Köhl J (2015) Biological control as a strategy to reduce the impact of mycotoxins in peanuts, grapes and cereals in Argentina. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 32:471–479

    Article  CAS  Google Scholar 

  142. Pitt JI, Hocking AD (2006) Mycotoxins in Australia: biocontrol of aflatoxin in peanuts. Mycopathologia 162:233–243

    Article  CAS  Google Scholar 

  143. Skrobek A, Boss D, Défago G, Butt TM, Maurhofer M (2006) Evaluation of different biological test systems to assess the toxicity of metabolites from fungal biocontrol agents. Toxicol Lett 161:43–52

    Article  CAS  Google Scholar 

  144. Oh SU, Yun BS, Lee SJ, Kim JH, Yoo ID (2002) Atroviridins A-C and neoatroviridins A-D, novel peptaibol antibiotics produced by Trichoderma atroviride F80317. I. Taxonomy, fermentation, isolation and biological activities. J Antibiot 55:557–564

    Article  CAS  Google Scholar 

  145. Degenkolb T, Fog Nielsen K, Dieckmann R, Branco-Rocha F, Chaverri P, Samuels GJ, Thrane U, von Döhren H, Vilcinskas A, Brückner H (2015) Peptaibol, secondary-metabolite, and hydrophobin pattern of commercial biocontrol agents formulated with species of the Trichoderma harzianum complex. Chem Biodivers 12:662–684

    Article  CAS  Google Scholar 

  146. Wicklow DT, Poling SM (2009) Antimicrobial activity of pyrrocidines from Acremonium zeae against endophytes and pathogens of maize. Phytopathology 99:109–115

    Article  CAS  Google Scholar 

  147. Wicklow DT, Roth S, Deyrup ST, Gloer JB (2005) A protective endophyte of maize: Acremonium zeae antibiotics inhibitory to Aspergillus flavus and Fusarium verticillioides. Mycol Res 109:610–618

    Article  CAS  Google Scholar 

  148. Liu M, Liu J, Wang WM (2012) Isolation and functional analysis of Thmfs1, the first major facilitator superfamily transporter from the biocontrol fungus Trichoderma harzianum. Biotechnol Lett 34:1857–1862

    Article  Google Scholar 

  149. Delgado J, Owens RA, Doyle S, Asensio MA, Núñez F (2015) Impact of the antifungal protein PgAFP from Penicillium chrysogenum on the protein profile in Aspergillus flavus. Appl Microbiol Biotechnol 99:8701–8715

    Article  CAS  Google Scholar 

  150. Kaiserer L, Oberparleiter C, Weiler-Görz R, Burgstaller W, Leiter E, Marx F (2003) Characterization of the Penicillium chrysogenum antifungal protein PAF. Arch Microbiol 180:204–210

    Article  CAS  Google Scholar 

  151. Marx F (2004) Small, basic antifungal proteins secreted from filamentous ascomycetes: a comparative study regarding expression, structure, function and potential application. Appl Microbiol Biotechnol 65:133–142

    Article  CAS  Google Scholar 

  152. Chang PK, Hua SST, Sarreal SBL, Li RW (2015) Suppression of aflatoxin biosynthesis in Aspergillus flavus by 2-phenylethanol is associated with stimulated growth and decreased degradation of branched-chain amino acids. Toxins (Basel) 7:3887–3902

    Article  CAS  Google Scholar 

  153. Hua SST, Beck JJ, Sarreal SBL, Gee W (2014) The major volatile compound 2-phenylethanol from the biocontrol yeast, Pichia anomala, inhibits growth and expression of aflatoxin biosynthetic genes of Aspergillus flavus. Mycotoxin Res 30:71–78

    Article  CAS  Google Scholar 

  154. Masoud W, Poll L, Jakobsen M (2005) Influence of volatile compounds produced by yeasts predominant during processing of Coffea arabica in East Africa on growth and ochratoxin A (OTA) production by Aspergillus ochraceus. Yeast 22:1133–1142

    Article  CAS  Google Scholar 

  155. Scarpari M, Bello C, Pietricola C, Zaccaria M, Bertocchi L, Angelucci A, Ricciardi MR, Scala V, Parroni A, Fabbri AA, Reverberi M, Zjalic S, Fanelli C (2014) Aflatoxin control in maize by Trametes versicolor. Toxins (Basel) 6:3426–3437

    Article  CAS  Google Scholar 

  156. Zjalic S, Reverberi M, Ricelli A, Mario Granito V, Fanelli C, Adele Fabbri A (2006) Trametes versicolor: a possible tool for aflatoxin control. Int J Food Microbiol 107:243–249

    Article  CAS  Google Scholar 

  157. Tolaini V, Zjalic S, Reverberi M, Fanelli C, Fabbri AA, Del Fiore A, De Rossi P, Ricelli A (2010) Lentinula edodes enhances the biocontrol activity of Cryptococcus laurentii against Penicillium expansum contamination and patulin production in apple fruits. Int J Food Microbiol 138:243–249

    Article  CAS  Google Scholar 

  158. Reverberi M, Fabbri AA, Zjalic S, Ricelli A, Punelli F, Fanelli C (2005) Antioxidant enzymes stimulation in Aspergillus parasiticus by Lentinula edodes inhibits aflatoxin production. Appl Microbiol Biotechnol 69:207–215

    Article  CAS  Google Scholar 

  159. Ma J, Mo H, Chen Y, Ding D, Hu L (2014) Inhibition of aflatoxin synthesis in Aspergillus flavus by three structurally modified lentinans. Int J Mol Sci 15:3860–3870

    Article  CAS  Google Scholar 

  160. Calistru C, McLean M, Berjak P (1997) In vitro studies on the potential for biological control of Aspergillus flavus and Fusarium moniliforme by Trichoderma species. A study of the production of extracellular metabolites by Trichoderma species. Mycopathologia 137:115–124

    Article  CAS  Google Scholar 

  161. Fiori S, Urgeghe PP, Hammami W, Razzu S, Jaoua S, Migheli Q (2014) Biocontrol activity of four non- and low-fermenting yeast strains against Aspergillus carbonarius and their ability to remove ochratoxin A from grape juice. Int J Food Microbiol 189:45–50

    Article  CAS  Google Scholar 

  162. Li C, Zhang H, Yang Q, Komla MG, Zhang X, Zhu S (2014) Ascorbic acid enhances oxidative stress tolerance and biological control efficacy of Pichia caribbica against postharvest blue mold decay of apples. J Agric Food Chem 62:7612–7621

    Article  CAS  Google Scholar 

  163. Barberis C, Astoreca A, Fernandez-Juri MG, Dalcero AM, Magnoli C (2010) Effect of antioxidant mixtures on growth and ochratoxin a production of Aspergillus section Nigri species under different water activity conditions on peanut meal extract agar. Toxins (Basel) 2:1399–1413

    Article  CAS  Google Scholar 

  164. Etcheverry M, Torres A, Ramirez ML, Chulze S, Magan N (2002) In vitro control of growth and fumonisin production by Fusarium verticillioides and F. proliferatum using antioxidants under different water availability and temperature regimes. J Appl Microbiol 92:624–632

    Article  CAS  Google Scholar 

  165. Passone MA, Rosso LC, Etcheverry M (2012) Influence of sub-lethal antioxidant doses, water potential and temperature on growth, sclerotia, aflatoxins and aflD (=nor-1) expression by Aspergillus flavus RCP08108. Microbiol Res 167:470–477

    Article  CAS  Google Scholar 

  166. Kozarski M, Klaus A, Jakovljevic D, Todorovic N, Vunduk J, Petrović P, Niksic M, Vrvic MM, van Griensven L (2015) Antioxidants of edible mushrooms. Molecules 20:19489–19525

    Article  CAS  Google Scholar 

  167. Choque E, El Rayess Y, Raynal J, Mathieu F (2015) Fungal naphtho-γ-pyrones-secondary metabolites of industrial interest. Appl Microbiol Biotechnol 99:1081–1096

    Article  CAS  Google Scholar 

  168. Cubaiu L, Abbas H, Dobson ADW, Budroni M, Migheli Q (2012) A Saccharomyces cerevisiae wine strain inhibits growth and decreases ochratoxin A biosynthesis by Aspergillus carbonarius and Aspergillus ochraceus. Toxins (Basel) 4:1468–1481

    Article  CAS  Google Scholar 

  169. Gastélum-Martínez E, Compant S, Taillandier P, Mathieu F (2012) Control of T-2 toxin in Fusarium langsethiae and Geotrichum candidum co-culture. Arh Hig Rada Toksikol 63:447–456

    Article  CAS  Google Scholar 

  170. Lutz MC, Lopes CA, Rodriguez ME, Sosa MC, Sangorrín MP (2013) Efficacy and putative mode of action of native and commercial antagonistic yeasts against postharvest pathogens of pear. Int J Food Microbiol 164:166–172

    Article  CAS  Google Scholar 

  171. Bluma R, Amaiden MR, Daghero J, Etcheverry M (2008) Control of Aspergillus section Flavi growth and aflatoxin accumulation by plant essential oils. J Appl Microbiol 105:203–214

    Google Scholar 

  172. Zabka M, Pavela R (2013) Antifungal efficacy of some natural phenolic compounds against significant pathogenic and toxinogenic filamentous fungi. Chemosphere 93:1051–1056

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire de Génie Chimique, Université de Toulouse, CNRS, INPT, UPS, Toulouse, France

    Carol Verheecke, Elodie Choque & Florence Mathieu

Authors
  1. Carol Verheecke
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elodie Choque
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Florence Mathieu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Florence Mathieu .

Editor information

Editors and Affiliations

  1. Faculty of Pharmaceutical Sciences, University of Bordeaux, Bordeaux, France

    Jean-Michel Mérillon

  2. Botany Department, M.L.Sukhadia University, Udaipur, Rajasthan, India

    Kishan Gopal Ramawat

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing Switzerland

About this entry

Cite this entry

Verheecke, C., Choque, E., Mathieu, F. (2017). Application of Fungal Metabolites Against Mycotoxins Production. In: Mérillon, JM., Ramawat, K. (eds) Fungal Metabolites. Reference Series in Phytochemistry. Springer, Cham. https://doi.org/10.1007/978-3-319-25001-4_31

Download citation

Publish with us

Policies and ethics

Search

Navigation