Influence of environmental factors on the production of penitrems A–F by Penicillium crustosum

Toxins

Volumn 9, Issue 7, 2017, Pages

  Kalinina, Svetlana A ^a   Jagels, Annika ^a   Cramer, Benedikt ^a   Geisen, Rolf ^b   Humpf, Hans Ulrich ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

Author keywords

Cheese model medium; Flash chromatography; Liquid chromatography; Micro scale extraction; Penicillium crustosum; Penitrem; Stress factor

Indexed keywords

COPPER SULFATE; GLUCOSE; GLUTAMIC ACID; MYCOTOXIN; NEUROTOXIN; PENITREM A; PENITREM B; PENITREM E; PENITREM F; SODIUM CHLORIDE; UNCLASSIFIED DRUG; HYDROGEN PEROXIDE; TREMORTIN;

ARTICLE; ASPERGILLUS; BIOLOGICAL ACTIVITY; BIOSYNTHESIS; CARBON SOURCE; CHEESE; CULTURE MEDIUM; ENVIRONMENTAL FACTOR; FUNGUS CULTURE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; NONHUMAN; OSMOLARITY; OXIDATIVE STRESS; PENICILLIUM; PENICILLIUM CRUSTOSUM; QUANTITATIVE ANALYSIS; SALT STRESS; SPECTROSCOPY; DRUG EFFECTS; LIGHT; METABOLISM; PH; TEMPERATURE;

COPPER SULFATE; GLUCOSE; GLUTAMIC ACID; HYDROGEN PEROXIDE; HYDROGEN-ION CONCENTRATION; LIGHT; MYCOTOXINS; OXIDATIVE STRESS; PENICILLIUM; SODIUM CHLORIDE; TEMPERATURE;

EID: 85021912144     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins9070210     Document Type: Article

References (63)

1. Steyn, P.S.; Vleggaar, R. Tremorgenic mycotoxins. In Fortschritte der Chemie organischer Naturstoffe/Progress in the Chemistry of Organic Natural Products; Springer: Vienna, Austria, 1985; pp. 1–80.
2. Smith, M.M.; Warren, V.A.; Thomas, B.S.; Brochu, R.M.; Ertel, E.A.; Rohrer, S.; Schaeffer, J.; Schmatz, D.; Petuch, B.R.; Tang, Y.S.; et al. Nodulisporic acid opens insect glutamate‐gated chloride channels: Identification of a new high affinity modulator. Biochemistry 2000, 39, 5543–5554. doi:10.1021/bi992943i. Available online: http://pubs.acs.org/doi/abs/10.1021/bi992943i (accessed on 12 April 2017).
3. Ondeyka, J.G.; Helms, G.L.; Hensens, O.D.; Goetz, M.A.; Zink, D.L.; Tsipouras, A.; Shoop, W.L.; Slayton, L.; Dombrowski, A.W.; Polishook, J.D.; et al. Nodulisporic acid A, a novel and potent insecticide from a Nodulisporium sp. Isolation, structure determination, and chemical transformations. J. Am. Chem. Soc. 1997, 119, 8809–88816. doi:10.1021/ja971664k. Available online: http://dx.doi.org/10.1021/ja971664k (accessed on 12 April 2017).
4. Shoop, W.L.; Zakson‐Aiken, M.; Gregory, L.M.; Michael, B.F.; Pivnichny, J.; Meinke, P.T.; Fisher, M.H.; Wyvratt, M.J.; Pikounis, B.; Schmatz, D.M. Systemic efficacy of nodulisporamides against fleas on dogs. J. Parasitol. 2001, 87, 1150–1154. doi:10.2307/3285249. Available online: http://www.jstor.org/stable/3285249 (accessed on 12 April 2017).
5. De Jesus, A.E.; Gorst-Allman, C.P.; Steyn, P.S.; van Heerden, F.R.; Vleggaar, R.; Wessels, P.L.; Hull, W.E. Tremorgenic mycotoxins from Penicillium crustosum. Biosynthesis of Penitrem A. J. Chem. Soc. Perkin Trans. 1 1983, 8, 1863–1868. doi:10.1039/P19830001863. Available online: http://pubs.rsc.org/is/content/articlelanding/1983/p1/p19830001863#!divAbstract (accessed on 12 April 2017).
6. Byrne, K.M.; Smith, S.K.; Ondeyka, J.G. Biosynthesis of nodulisporic acid A: Precursor studies. J. Am. Chem. Soc. 2002, 124, 7055–7060. doi:10.1021/ja017183p. Available online: https://scholar.google.de/scholar?hl= en&q=3.%09Byrne%2C+K.M.%3B+Smith%2C+S.K.%3B+Ondeyka%2C+J.G.+Biosynthesis+of+nodulisporic +acid+A%3A+Precursor+studies.+J.+Am.+Chem.+Soc.+2002%2C+124%2C+7055–7060.+DOI%3A+10.1021% 2Fja017183p.&btnG=&as_sdt=1%2C5&as_sdtp= (accessed on 12 April 2017).
7. Parker, E.J.; Scott, D.B. Indole‐Diterpene Biosynthesis in Ascomycetous Fungi; Marcel Dekker: New York, NY, USA, 2004; Volume 70, pp. 405–426.
8. Saikia, S.; Nicholson, M.J.; Young, C.; Parker, E.J.; Scott, B. The genetic basis for indole‐diterpene chemical diversity in filamentous fungi. Mycol. Res. 2008, 112, 184–199. doi:10.1016/j.mycres.2007.06.015. Available online: http://www.sciencedirect.com/science/article/pii/S0953756207001566 (accessed on 12 April 2017).
9. Cole, R.J. Tremorgenic mycotoxins: An update. In Antinutrients and Natural Toxins in Foods; Ory, R.L., Ed.; Food and Nutrition Press: Westport, CT, USA, 1980; pp. 17–37.
10. González, M.C.; Lull, C.; Moya, P.; Ayala, I.; Primo, J.; Primo Yúfera, E. Insecticidal activity of penitrems, including penitrem G, a new member of the family isolated from Penicillium crustosum. J. Agric. Food Chem. 2003, 51, 2156–2160. doi:10.1021/jf020983e. Available online: http://pubs.acs.org/doi/abs/10.1021/jf020983e (accessed on 12 April 2017).
11. Laakso, J.A.; Gloer, J.B.; Wicklow, D.T.; Dowd, P.F. A new penitrem analog with antiinsectan activity from the sclerotia of Aspergillus sulphureus. J. Agric. Food Chem. 1993, 41, 973–975. doi:10.1021/jf00030a027. Available online: http://pubs.acs.org/doi/abs/10.1021/jf00030a027 (accessed on 12 April 2017).
12. Moldes‐Anaya, A.; Rundberget, T.; Uhlig, S.; Rise, F.; Wilkins, A.L. Isolation and structure elucidation of secopenitrem D, an indole alkaloid from Penicillium crustosum Thom. Toxicon 2011, 57, 259–265. doi:10.1016/j.toxicon.2010.11.020. Available online: http://dx.doi.org/10.1016/j.toxicon.2010.11.020 (accessed on 12 April 2017).
13. Rundberget, T.; Skaar, I.; O’Brien, O.; Flåøyen, A. Penitrem and thomitrem formation by Penicillium crustosum. Mycopathologia 2004, 157, 349–357. doi:10.1023/B:MYCO.0000024180.99262.b1. Available online: http://link.springer.com/article/10.1023/B:MYCO.0000024180.99262.b1 (accessed on 12 April 2017).
14. Naik, J.T.; Mantle, P.G.; Sheppard, R.N.; Waight, E.S. Penitremones A‐C, Penicillium metabolites containing an oxidized penitrem carbon skeleton giving insight into structure‐tremorgenic relationships. J. Chem. Soc. Perkin Trans. 1 1995, 9, 1121–1125. doi:10.1039/P19950001121. Available online: http://pubs.rsc.org/en/content/articlelanding/1995/p1/p19950001121#!divAbstract (accessed on 12 April 2017).
15. Yamaguchi, T.; Nozawa, K.; Hosoe, T.; Nakajima, S.; Kawai, K. Indoloterpenes related to tremorgenic mycotoxins, penitrems, from Penicillium crustosum. Phytochemistry 1993, 32, 1177–1181. doi:10.1016/S0031‐9422(00)95087‐8. Available online: http://www.sciencedirect.com/science/article/pii/S0031942200950878? via%3Dihub (accessed on 12 April 2017).
16. Sallam, A.A.; Ayoub, N.M.; Foudah, A.I.; Gissendanner, C.R.; Meyer, S.A.; El Sayed, K.A. Indole diterpene alkaloids as novel inhibitors of the Wnt/β‐catenin pathway in breast cancer cells. Eur. J. Med. Chem. 2013, 70, 594–606. doi:10.1016/j.ejmech.2013.09.045. Available online: http://dx.doi.org/10.1016/j.ejmech. 2013.09.045 (accessed on 12 April 2017).
17. Sallam, A.A.; Houssen, W.E.; Gissendanner, C.R.; Orabi, K.Y.; Foudah, A.I.; El Sayed, K.A. Bioguided discovery and pharmacophore modeling of the mycotoxic indole diterpene alkaloids penitrems as breast cancer proliferation, migration, and invasion inhibitors. MedChemComm 2013, 4, 1360–1369. doi:10.1039/C3MD00198A. Available online: https://www.ncbi.nlm.nih.gov/pubmed/24273638 (accessed on 12 April 2017).
18. Norris, P.J.; Smith, C.C.T.; De Belleroche, J.; Bradford, H.F.; Mantle, P.G.; Thomas, A.J.; Penny, R.H.C. Actions of tremorgenic fungal toxins on neurotransmitter release. J. Neurochem. 1980, 34, 33–42. doi:10.1111/j.1471‐4159.1980.tb04618.x. Available online: https://www.ncbi.nlm.nih.gov/pubmed/6108984 (accessed on 12 April 2017).
19. Knaus, H.G.; McManus, O.B.; Lee, S.H.; Schmalhofer, W.A.; Garcia-Calvo, M.; Helms, L.M.; Sanchez, M.; Giangiacomo, K.; Reuben, J.P. Tremorgenic indole alkaloids potently inhibit smooth muscle high‐conductance calcium‐activated potassium channels. Biochemistry 1994, 33, 5819–5828. doi:10.1021/bi00185a021. Available online: https://www.ncbi.nlm.nih.gov/pubmed/7514038 (accessed on 12 April 2017).
20. Eriksen, G.S.; Jäderlund, K.H.; Moldes-Anaya, A.; Schönheit, J.; Bernhoft, A.; Jaeger, G.; Rundberget, T.; Skaar, I. Poisoning of dogs with tremorgenic Penicillium toxins. Med. Mycol. 2010, 48, 188–196. doi:10.3109/13693780903225821. Available online: http://dx.doi.org/10.3109/13693780903225821 (accessed on 12 April 2017).
21. Breton, P.; Bizot, J.C.; Buee, J.; De La Manche, I. Brain neurotoxicity of Penitrem A: electrophysiological, behavioral and histopathological study. Toxicon 1998, 36, 645–655. doi:10.1016/S0041‐0101(97)00084‐6. Available online: http://doi.org/10.1016/S0041‐0101(97)00084‐6 (accessed on 12 April 2017).
22. Richard, J.L.; Arp, L.H. Natural occurrence of the mycotoxin penitrem A in moldy cream cheese. Mycopathologia 1979, 67, 107–109. doi:10.1007/BF00440681. Available online: http://link.springer.com/article/10.1007%2FBF00440681?LI=true (accessed on 12 April 2017).
23. Richard, J.L.; Bacchetti, P.; Arp, L.H. Moldy walnut toxicosis in a dog, caused by the mycotoxin, penitrem A. Mycopathologia 1981, 76, 55–58. doi:10.1007/BF00761899. Available online: http://link.springer.com/article/10.1007/BF00761899 (accessed on 12 April 2017).
24. Hocking, A.D.; Holds, K.; Tobin, N.F. Intoxication by tremorgenic mycotoxin (penitrem A) in a dog. Aust. Vet. J. 1988, 65, 82–85. doi:10.1111/j.1751‐0813.1988.tb07366.x. Available online: http://onlinelibrary. wiley.com/doi/10.1111/j.1751–0813.1988.tb07366.x/full (accessed on 12 April 2017).
25. Boysen, S.R.; Rozanski, E.A.; Chan, D.L.; Grobe, T.L.; Fallon, M.J.; Rush, J.E. Tremorgenic mycotoxicosis in four dogs from a single household. J. Am. Vet. Med. Assoc. 2002, 221, 1441–1444. doi:10.2460/javma.2002.221.1441. Available online: http://www.ncbi.nlm.nih.gov/pubmed/12458614 (accessed on 12 April 2017).
26. Naude, T.W.; O’Brien, O.M.; Rundberget, T.; McGregor, A.D.G.; Roux, C.; Flåøyen, A. Tremorgenic neuromycotoxicosis in 2 dogs ascribed to the ingestion of penitrem A and possibly roquefortine in rice contaminated with Penicillium crustosum: Clinical communication. J. S. Afr. Vet. Assoc. 2002, 73, 211–215. Available online: https://www.ncbi.nlm.nih.gov/pubmed/12665136?dopt=Abstract (accessed on 12 April 2017).
27. Mantle, P.G.; Penny, R.H.C. Tremorgenic mycotoxins and neurological disorders‐a review. Vet. Annu. 1981, 21, 51–62. Available online: http://agris.fao.org/agris‐search/search.do?recordID=US201301309076 (accessed on 12 April 2017).
28. Lewis, P.R.; Donoghue, M.B.; Hocking, A.D.; Cook, L.; Granger, L.V. Tremor syndrome associated with a fungal toxin: Sequelae of food contamination. Med. J. Aust. 2005, 182, 582–584. Available online: https://www.mja.com.au/journal/2005/182/11/tremor‐syndrome‐associated‐fungal‐toxin‐sequelae‐food‐co ntamination (accessed on 12 April 2017).
29. Wilson, B.J.; Wilson, C.H.; Hayes, A.W. Tremorgenic toxin from Penicillium cyclopium grown on food materials. Nature 1968, 220, 77–78. doi:10.1038/220077b0. Available online: http://www.nature.com/nature/journal/v220/n5162/abs/220077b0.html (accessed on 12 April 2017).
30. Mantle, P.G.; Perera, K.P.; Maishman, N.J.; Mundy, G.R. Biosynthesis of penitrems and roquefortine by Penicillium crustosum. Appl. Environ. Microbiol. 1983, 45, 1486–1490. Available online: https://www.ncbi.nlm.nih.gov/pubmed/6870239 (accessed on 12 April 2017).
31. Dorner, J.W.; Cole, R.J.; Hill, R.A. Tremorgenic mycotoxins produced by Aspergillus fumigatus and Penicillium crustosum isolated from molded corn implicated in a natural intoxication of cattle. J. Agric. Food Chem. 1984, 32, 411–413. Available online: http://scholar.google.com/scholar_lookup?title= Tremorgenic%20mycotoxins%20produced%20by%20Aspergillus%20fumigatus%20and%20Penicillium% 20crustosum%20isolated%20from%20moulded%20corn%20implicated%20in%20a%20natural%20intoxica tion%20of%20cattle&author=JW.%20Dorner&author=RJ.%20Cole&author=RA.%20Hill&journal=J%20Agr ic%20Food%20Chem&volume=32&pages=411–413&publication_year=1984 (accessed on 12 April 2017).
32. Hope, R.; Aldred, D.; Magan, N. Comparison of environmental profiles for growth and deoxynivalenol production by Fusarium culmorum and F. graminearum on wheat grain. Lett. Appl. Microbiol. 2005, 40, 295– 300. doi:10.1111/j.1472‐765X.2005.01674.x. Available online: http://onlinelibrary.wiley.com/doi/10.1111/j.1472‐765X.2005.01674.x/full (accessed on 12 April 2017).
33. Karanyi, Z.; Holb, I.; Hornok, L.; Pocsi, I.; Miskei, M. FRSD: Fungal stress response database. Database 2013. doi:10.1093/database/bat037. Available online: http://internal.med.unideb.hu/fsrd/(accessed on 12 April 2017).
34. Wagener, R.E.; Davis, N.D.; Diener, U.L. Penitrem A and roquefortine production by Penicillium commune. Appl. Environ. Microbiol. 1980, 39, 882–887. Available online: https://www.ncbi. nlm.nih.gov/pmc/articles/PMC291438/(accessed on 12 April 2017).
35. Hou, C.T.; Ciegler, A.; Hessseltine, C.W. Tremorgenic toxins from penicillia III. Tremortin production by Penicillium species on various agricultural commodities. Appl. Microbiol. 1971, 21, 1101–1103. Available online: http://aem.asm.org/content/21/6/1101.short (accessed on 12 April 2017).
36. Sumarah, M.W.; Miller, J.D.; Blackwell, B.A. Isolation and metabolite production by Penicillium roqueforti, P. paneum and P. crustosum isolated in Canada. Mycopathologia 2005, 159, 571–577. doi:10.1007/s11046‐005‐5257‐7. Available online: https://www.ncbi.nlm.nih.gov/pubmed/15983744 (accessed on 12 April 2017).
37. El‐Banna, A.A.; Leistner, L. Production of penitrem A by Penicillium crustosum isolated from foodstuffs. Int. J. Food Microbiol. 1988, 7, 9–17. doi:10.1016/0168‐1605(88)90067‐0. Available online: https://www.ncbi. nlm.nih.gov/pubmed/3275314 (accessed on 12 April 2017).
38. Surekha, M.; Reddy, S.M. Effect of carbon and nitrogen sources on the production of penitrem B by Penicillium aurantiogriseum. Folia Microbiol. 1992, 37, 47–49. Available online: https://www.ncbi.nlm.nih.gov/pubmed/1505862 (accessed on 12 April 2017).
39. Surekha, M.; Saini, K.; Advala, N.; Reddy, S.M. Production of penitrem B a tremogenic toxin produced by Penicillium aurantiogriseum. Int. J. Curr. Res. 2012, 4, 37–39. Available online: https://www.journalcra.com (accessed on 12 April 2017).
40. Mantle, P.G.; Laws, I.; Tan, M.J.L.; Tizard, M. A novel process for the production of penitrem mycotoxins by submerged fermentation of Penicillium nigricans. Microbiology 1984, 130, 1293–1298. doi:10.1099/00221287‐130‐5‐1293. Available online: http://mic.microbiologyresearch.org/content/journal/micro/10.1099/00221287‐130‐5‐1293 (accessed on 12 April 2017).
41. Liu, C.; Tagami, K.; Minami, A.; Matsumoto, T.; Frisvad, J.C.; Suzuki, H.; Ishikawa, J.; Gomi, K.; Oikawa, H. Reconstitution of biosynthetic machinery for the synthesis of the highly elaborated indole diterpene penitrem. Angew. Chem. Int. Ed. 2015, 54, 5748–5752. doi:10.1002/anie.201501072. Available online: http://orbit.dtu.dk/en/publications/reconstitution‐of‐biosynthetic‐machinery‐for‐the‐synthesis‐of‐the‐highly-elaborated‐indole‐diterpene‐penitrem(3941efe6–6cf1–4efa‐b550‐a5a92e08a27a).html (accessed on 12 April 2017).
42. De Jesus, A.E.; Steyn, P.S.; van Heerden, F.R.; Vleggaar, R.; Wessels, P.L.; Hull, W.E. Tremorgenic mycotoxins from Penicillium crustosum: Isolation of penitrems A–F and the structure elucidation and absolute configuration of penitrem A. J. Chem. Soc. Perkin Trans. 1 1983, 1847–1856. doi:10.1039/P19830001847 Available online: http://pubs.rsc.org/en/content/articlelanding/1983/p1/p19830001847#!divAbstract (accessed on 12 April 2017).
43. De Jesus, A.E.; Steyn, P.S.; van Heerden, F.R.; Vleggaar, R.; Wessels, P.L.; Hull, W.E. Structure and biosynthesis of the penitrems A–F, six novel tremorgenic mycotoxins from Penicillium crustosum. J. Chem. Soc. Chem. Commun. 1981, 6, 289–291. doi:10.1039/C39810000289. Available online: http://pubs.rsc.org/is/content/articlelanding/1981/c3/c39810000289#!divAbstract (accessed on 12 April 2017).
44. Mantle, P.G. The role of tryptophan as a biosynthetic precursor of indole‐diterpenoid fungal metabolites: Continuing a debate. Phytochemistry 2009, 70, 7–10. doi:10.1016/j.phytochem.2008.11.004. Available online: https://www.ncbi.nlm.nih.gov/pubmed/19136126 (accessed on 12 April 2017).
45. Magan, N.; Cayley, G.R.; Lacey, J. Effect of water activity and temperature on mycotoxin production by Alternaria alternata in culture and on wheat grain. Appl. Environ. Microbiol. 1984, 47, 1113–1117. Available online: https://www.ncbi.nlm.nih.gov/pubmed/6540067 (accessed on 12 April 2017).
46. Schmidt‐Heydt, M.; Graf, E.; Stoll, D.; Geisen, R. The biosynthesis of ochratoxin A by Penicillium as one mechanism for adaptation to NaCl rich foods. Food Microbiol. 2012, 29, 233–241. doi:10.1016/j.fm.2011.08.003. Available online: https://www.ncbi.nlm.nih.gov/pubmed/22202878 (accessed on 12 April 2017).
47. Walter, S.L. Acute penitrem A and roquefortine poisoning in a dog. Can. Vet. J. 2002, 43, 372–274. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC339273/(accessed on 12 April 2017).
48. Felsöciova, S.; Rybarik, L.; Tancinova, D.; Maskova, Z.; Kacaniova, M. Microfungi and mycotoxins of grapes from Tokaj wine region. J. Microbiol. Biotechnol. Food Sci. 2015, 4, 16–18. doi:10.15414/jmbfs.2015.4.special1. 16‐18. Available online: http://www.jmbfs.org/issue/february‐2015‐vol‐4‐special‐issue‐1‐microbiology/felsociova2/?issue_id=3715&article_id=3 (accessed on 12 April 2017).
49. Atoui, A.; Kastner, C.; Larey, C.M.; Thokala, R.; Etxebeste, O.; Espeso, E.A.; Fischer, R.; Calvo, A.M. Cross‐talk between light and glucose regulation controls toxin production and morphogenesis in Aspergillus nidulans. Fungal Genet. Biol. 2010, 47, 962–972. doi:10.1016/j.fgb.2010.08.007. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2982864/(accessed on 12 April 2017).
50. Kawakami, A.; Nakajima, T.; Hirayae, K. Effects of carbon sources and amines on induction of trichothecene production by Fusarium asiaticum in liquid culture. FEMS Microbiol. Lett. 2014, 352, 204–212. doi:10.1111/1574‐6968.12386. Available online: http://onlinelibrary.wiley.com/store/10.1111/1574‐6968. 12386/asset/fml12386.pdf?v=1&t=j1l3m1ps&s=0f69cbf249acd343ee0071f3e99e890579571e17&systemMessa ge=Pay+Per+View+on+Wiley+Online+Library+will+be+unavailable+on+Saturday+15th+April+from+12%3 A00–09%3A00+EDT+for+essential+maintenance.++Apologies+for+the+inconvenience. (accessed on 12 April 2017).
51. Tudzynski, B. Nitrogen regulation of fungal secondary metabolism in fungi. Front. Microbiol. 2014, 5, 1–15. doi:10.3389/fmicb.2014.00656. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4246892/(accessed on 12 April 2017).
52. Medina, A.; Mateo, E.M.; Valle‐Algarra, F.M.; Mateo, F.; Mateo, R.; Jimenez, M. Influence of nitrogen and carbon sources on the production of ochratoxin A by ochratoxigenic strains of Aspergillus spp. isolated from grapes. Int. J. Food Microbiol. 2008, 122, 93–99. doi:10.1016/j.ijfoodmicro.2007.11.055. Available online: https://www.ncbi.nlm.nih.gov/pubmed/18164776 (accessed on 12 April 2017).
53. Buchanan, R.L.; Stahl, H.G. Ability of various carbon sources to induce and support aflatoxin synthesis by Aspergillus parasiticus. J. Food Saf. 1984, 6, 271–279. doi:10.1111/j.1745‐4565.1984.tb00488.x. Available online: http://onlinelibrary.wiley.com/doi/10.1111/j.1745‐4565.1984.tb00488.x/full (accessed on 12 April 2017).
54. Brzonkalik, K.; Herrling, T.; Syldatk, C.; Neumann, A. The influence of different nitrogen and carbon sources on mycotoxin production in Alternaria alternata. Int. J. Food Micribiol. 2011, 147, 120–126. doi:10.1016/j.ijfoodmicro.2011.03.016. Available online: http://dx.doi.org/10.1016/j.ijfoodmicro.2011.03.016 (accessed on 12 April 2017).
55. Jayashree, T.; Subramanyam, C. Oxidative stress as a prerequisite for aflatoxin production by Aspergillus parasiticus. Free Radic. Biol. Med. 2000, 29, 981–985. doi:10.1016/S0891‐5849(00)00398‐1. Available online: https://www.ncbi.nlm.nih.gov/pubmed/11084286 (accessed on 12 April 2017).
56. 2. J. Agric. Food Chem. 2015, 63, 4879–4885. doi:10.1021/acs.jafc.5b00113. Available online: http://www.scopus.com/inward/record.url?eid=2‐s2.0‐84930225548&partnerID=tZOtx3y1 (accessed on 12 April 2017).
57. Schmidt‐Heydt, M.; Rüfer, C.; Raupp, F.; Bruchmann, A.; Perrone, G.; Geisen, R. Influence of light on food relevant fungi with emphasis on ochratoxin producing species. Int. J. Food Microbiol. 2011, 145, 229–237. doi:10.1016/j.ijfoodmicro.2010.12.022. Available online: http://www.sciencedirect.com/science/article/pii/S0168160510007129 (accessed on 12 April 2017).
58. Malir, F.; Ostry, V.; Pfohl-Leszkowicz, A.; Malir, J.; Toman, J. Ochratoxin A: 50 Years of Research. Toxins 2016, 8, 1–49. doi:10.3390/toxins8070191. Available online: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4963825/(accessed on 12 April 2017).
59. Pose, G.; Patriara, A.; Kyanko, V.; Pardo, A.; Fernández Pinto, V. Water activity and temperature effects on mycotoxin production by Alternaria alternata on a synthetic tomato medium. Int. J. Food Micribiol. 2010, 142, 348–353. doi:10.1016/j.ijfoodmicro.2010.07.017. Available online: http://dx.doi.org/10.1016/j.ijfoodmicro. 2010.07.017 (accessed on 12 April 2017).
60. Samson, R.A.; van Reenen‐Hoekstra, E.S. Introduction to Food‐Borne Fungi, 3rd Ed.; Centraalbureau voor Schimmelcutures: Baarn, The Netherlands, 1988.
61. Samson, R.A.; Hoekstra, E.S.; Frisvad, J.C.; Filtenborg, O. Introduction to Food‐Borne Fungi, 5rd Ed.; Centraalbureau voor Schimmelcutures: Baarn, The Netherlands, 1996.
62. Kokkonen, M.; Jestoi, M.; Rizzo, A. The effect of substrate on mycotoxin production of selected Penicillium strains. Int. J. Food Micribiol. 2005, 99, 207–214. doi:10.1016/j.ijfoodmicro.2004.08.014. Available online: http://europepmc.org/abstract/med/15734568 (accessed on 12 April 2017).
63. Smedsgaard, J. Micro‐scale extraction procedure for standardized screening of fungal metabolite production in cultures. J. Chromatogr. A 1997, 760, 264–270. doi:10.1016/S0021‐9673(96)00803‐5. Available online: https://scholar.google.com/scholar_lookup?title=Micro‐scale%20extraction%20procedure%20for% 20standardized%20screening%20of%20fungal%20metabolite%20production%20in%20cultures&author=S medsgaard,+J.&publication_year=1997&journal=J.+Chromatogr.+A&volume=760&pages=264‐270&doi=10. 1016/S0021‐9673(96)00803‐5 (accessed on 12 April 2017).