Several studies have explored in depth the biochemistry and genetics of the pigments present in Fusarium graminearum, but there is a need to discuss their relationship with the mold’s observable surface color pattern variation throughout its lifecycle. Furthermore, they require basic cataloguing, including a description of their major features known so far. Colors are a viable alternative to size measurement in growth studies. When grown on yeast extract agar (YEA) at 25 °C, F. graminearum initially exhibits a whitish mycelium, developing into a yellow-orange mold by the sixth day and then turning into wine-red. The colors are likely due to accumulation of the golden yellow polyketide aurofusarin and the red rubrofusarin, but the carotenoid neurosporaxanthin also possibly plays a major role in the yellow or orange coloration. Torulene might contribute to red tones, but it perhaps ends up being converted into neurosporaxanthin. Culmorin is also present, but it does not contribute to the color, though it was initially isolated in pigment studies. Additionally, there is the 5-deoxybostrycoidin-based melanin, but it mostly occurs in the teleomorph’s perithecium. There is still a need to chemically quantify the pigments throughout the lifecycle, and analyze their relationships and how much each impacts F. graminearum’s surface color.
Keywords: Fusarium graminearum; color; pigments; polyketides; carotenoids.
1. Kim, J.-E.; Jin, J.; Kim, H.; Kim, J.-C.; Yun, S.-H.; Lee, Y.-W. Gip2, a putative transcription factor that regulates the aurofusarin biosynthetic gene cluster in gibberella zeae. Appl. Environ. Microbiol. 2006, 72, 1645–1652. [CrossRef] [PubMed]
2. Malz, S.; Grell, M.N.; Thrane, C.; Maier, F.J.; Rosager, P.; Felk, A.; Albertsen, K.S.; Salomon, S.; Bohn, L.; Schäfer, W. Identification of a gene cluster responsible for the biosynthesis of aurofusarin in the fusarium graminearum species complex. Fungal Genet. Biol. 2005, 42, 420–433. [CrossRef] [PubMed]
3. Garcia-Cela, E.; Kiaitsi, E.; Medina, A.; Sulyok, M.; Krska, R.; Magan, N. Interacting environmental stress factors affects targeted metabolomic profiles in stored natural wheat and that inoculated with F. Graminearum. Toxins 2018, 10, 56. [CrossRef] [PubMed]
4. Weidenbörner, M. Encyclopedia of Food Mycotoxins, 1st ed.; Springer-Verlag: Berlin Heidelberg: Berlin, Germany, 2001; p. 294.
5. Yoshizawa, T. Thirty-five years of research on deoxynivalenol, a trichothecene mycotoxin: With special reference to its discovery and co-occurrence with nivalenol in Japan. Food Saf. 2013, 1, 2013002. [CrossRef]
6. Hueza, I.M.; Raspantini, P.C.F.; Raspantini, L.E.R.; Latorre, A.O.; Górniak, S.L. Zearalenone, an estrogenic mycotoxin, is an immunotoxic compound. Toxins 2014, 6, 1080–1095. [CrossRef] [PubMed]
7. Lysoe, E.; Klemsdal, S.S.; Bone, K.R.; Frandsen, R.J.; Johansen, T.; Thrane, U.; Giese, H. The PKS4 gene of Fusarium graminearum is essential for zearalenone production. Appl. Environ. Microbiol. 2006, 72, 3924–3932. [CrossRef] [PubMed]
8. Ashley, J.N.; Hobbs, B.C.; Raistrick, H. Studies in the biochemistry of micro-organisms: The crystalline colouring matters of Fusarium culmorum (W.G. Smith) Sacc. and related forms. Biochem. J. 1937, 31, 385–397. [CrossRef] [PubMed]
9. Stout, G.H.; Jensen, L.H. Rubrofusarin: A structure determination using direct phase calculation. Acta Crystallogr. 1962, 15, 451–457. [CrossRef]
10. Baker, P.M.; Roberts, J.C. Studies in mycological chemistry. Part XXI. The structure of aurofusarin, a metabolite of some fusarium species. J. Chem. Soc. C: Org. 1966, 2234–2237. [CrossRef]
11. Barton, D.H.R.; Werstiuk, N.H. The constitution and stereochemistry of culmorin. Chem. Commun. (London) 1967, 1, 30–31. [CrossRef]
12. Shibata, S.; Morishita, E.; Takeda, T.; Sakata, K. Metabolic products of fungi. XXVIII. The structure of aurofusarin. (1). Chem. Pharm. Bull. (Tokyo) 1968, 16, 405–410. [CrossRef]
13. Frandsen, R.J.N.; Nielsen, N.J.; Maolanon, N.; Sørensen, J.C.; Olsson, S.; Nielsen, J.; Giese, H. The biosynthetic pathway for aurofusarin in fusarium graminearum reveals a close link between the naphthoquinones and naphthopyrones. Mol. Microbiol. 2006, 61, 1069–1080. [CrossRef] [PubMed]
14. Dufosse, L.; Fouillaud, M.; Caro, Y.; Mapari, S.A.; Sutthiwong, N. Filamentous fungi are large-scale producers of pigments and colorants for the food industry. Curr. Opin. Biotechnol. 2014, 26, 56–61. [CrossRef] [PubMed]
15. Avalos, J.; Pardo-Medina, J.; Parra-Rivero, O.; Ruger-Herreros, M.; Rodríguez-Ortiz, R.; Hornero-Méndez, D.; Limón, M.C. Carotenoid biosynthesis in Fusarium. J. Fungi (Basel) 2017, 3, 39. [CrossRef] [PubMed]
16. Kim, H.; Son, H.; Lee, Y.W. Effects of light on secondary metabolism and fungal development of Fusarium graminearum. J. Appl. Microbiol. 2014, 116, 380–389. [CrossRef] [PubMed]
17. Cambaza, E.; Koseki, S.; Kawamura, S. The use of colors as an alternative to size in Fusarium graminearum growth studies. Foods 2018, 7, 100. [CrossRef] [PubMed]
18. Liu, Y.; Liu, N.; Yin, Y.; Chen, Y.; Jiang, J.; Ma, Z. Histone H3K4 methylation regulates hyphal growth, secondary metabolism and multiple stress responses in Fusarium graminearum. Environ. Microbiol. 2015, 17, 4615–4630. [CrossRef] [PubMed]
19. Medentsev, A.G.; Arinbasarova, A.; Akimenko, V.K. Biosynthesis of naphthoquinone pigments by fungi of the genus fusarium. Appl. Biochem. Microbiol. 2005, 41, 503–507. [CrossRef]
20. Shibata, S.; Morishita, E.; Takeda, T.; Sakata, K. The structure of Aurofusarin. Tetrahedron Lett. 1966, 7, 4855–4860. [CrossRef]
21. Jin, J.-M.; Lee, J.; Lee, Y.-W. Characterization of carotenoid biosynthetic genes in the ascomycete gibberella zeae. FEMS Microbiol. Lett. 2009, 302, 197–202. [CrossRef] [PubMed]
22. Leeper, F.J.; Staunton, J. The biosynthesis of rubrofusarin, a polyketide naphthopyrone from Fusarium culmorum: 13C nmr assignments and incorporation of 13C-and 2H-labelled acetates. J. Chem. Soc., Perkin Trans. 1 1984, 2919–2925. [CrossRef]
23. Proctor, R.H.; Butchko, R.A.; Brown, D.W.; Moretti, A. Functional characterization, sequence comparisons and distribution of a polyketide synthase gene required for perithecial pigmentation in some fusarium species. Food Addit. Contam. 2007, 24, 1076–1087. [CrossRef] [PubMed]
24. Sugiura, Y. Gibberella zeae (schwabe) petch. In JCM Catalogue; Japan Collection of Microorganisms, Ed.; Microbe Division (JCM): Tsukuba, Japan, 1996.
25. Sigma-Aldrich. 01497 yeast extract agar. Available online: https://www.sigmaaldrich.com/content/dam/ sigma-aldrich/docs/Sigma-Aldrich/Datasheet/1/01497dat.pdf (4 September 2018).
26. Sorensen, J.L.; Sondergaard, T.E. The effects of different yeast extracts on secondary metabolite production in fusarium. Int. J. Food Microbiol. 2014, 170, 55–60. [CrossRef] [PubMed]
27. Dufossé, L.; Caro, Y.; Fouillaud, M. Fungal pigments: Deep into the rainbow of colorful fungi. J. Fungi 2017, 3, 45. [CrossRef] [PubMed]
28. Frandsen, R.J.N.; Rasmussen, S.A.; Knudsen, P.B.; Uhlig, S.; Petersen, D.; Lysøe, E.; Gotfredsen, C.H.; Giese, H.; Larsen, T.O. Black perithecial pigmentation in fusarium species is due to the accumulation of 5-deoxybostrycoidin-based melanin. Sci. Rep. 2016, 6, 26206. [CrossRef] [PubMed]
29. Gerber, N.N.; Ammar, M.S. New antibiotic pigments related to fusarubin from fusarium solani (Mart.) Sacc. II. Structure elucidations. J. Antibiot. (Tokyo) 1979, 32, 685–688. [CrossRef] [PubMed]
30. Ammar, M.S.; Gerber, N.N.; McDaniel, L.E. New antibiotic pigments related to fusarubin from fusarium solani (Mart.) Sacc. I. Fermentation, isolation, and antimicrobial activities. J. Antibiot. (Tokyo) 1979, 32, 679–684. [CrossRef] [PubMed]
31. Jarolim, K.; Wolters, K.; Woelflingseder, L.; Pahlke, G.; Beisl, J.; Puntscher, H.; Braun, D.; Sulyok, M.; Warth, B.; Marko, D. The secondary fusarium metabolite aurofusarin induces oxidative stress, cytotoxicity and genotoxicity in human colon cells. Toxicol. Lett. 2018, 284, 170–183. [CrossRef] [PubMed]
32. Medentsev, A.G.; Kotik, A.N.; Trufanova, V.A.; Akimenko, V.K. Identification of aurofusarin in fusarium graminearum isolates, causing a syndrome of worsening of egg quality in chickens. Appl. Biochem. Microbiol. 1993, 29, 542–546.
33. Glentham Life Sciences. Ga7883-aurofusarin. In Product Datasheet; Glentham Life Sciences, Ed.; Glentham Life Sciences: Wiltshire, United Kingdom, 2018.
34. Beccari, G.; Colasante, V.; Tini, F.; Senatore, M.T.; Prodi, A.; Sulyok, M.; Covarelli, L. Causal agents of Fusarium head blight of durum wheat (Triticum durum Desf.) in central Italy and their in vitro biosynthesis of secondary metabolites. Food Microbiol. 2018, 70, 17–27. [CrossRef] [PubMed]
35. Birchall, G.R.; Bowden, K.; Weiss, U.; Whalley, W.B. The chemistry of fungi. Part LVI. Aurofusarin. J. Chem. Soc. C: Org. 1966, 2237–2239. [CrossRef]
36. Frandsen, R.J.; Schutt, C.; Lund, B.W.; Staerk, D.; Nielsen, J.; Olsson, S.; Giese, H. Two novel classes of enzymes are required for the biosynthesis of aurofusarin in fusarium graminearum. J. Biol. Chem. 2011, 286, 10419–10428. [CrossRef] [PubMed]
37. Gaffoor, I.; Brown, D.W.; Plattner, R.; Proctor, R.H.; Qi, W.; Trail, F. Functional analysis of the polyketide synthase genes in the filamentous fungus gibberella zeae (anamorph Fusarium graminearum). Eukaryot. Cell 2005, 4, 1926–1933. [CrossRef] [PubMed]
38. Kim, J.-E.; Kim, J.-C.; Jin, J.-M.; Yun, S.-H.; Lee, Y.-W. Functional characterization of genes located at the aurofusarin biosynthesis gene cluster in gibberella zeae. Plant Pathol. J. 2008, 24, 8–16. [CrossRef]
39. Hoffmeister, D.; Keller, N.P. Natural products of filamentous fungi: Enzymes, genes, and their regulation. Nat. Prod. Rep. 2007, 24, 393–416. [CrossRef] [PubMed]
40. Kim, J.-E.; Han, K.-H.; Jin, J.; Kim, H.; Kim, J.-C.; Yun, S.-H.; Lee, Y.-W. Putative polyketide synthase and laccase genes for biosynthesis of aurofusarin in Gibberella zeae. Appl. Environ. Microbiol. 2005, 71, 1701–1708. [CrossRef] [PubMed]
41. Dvorska, J.E.; Surai, P.F.; Speake, B.K.; Sparks, N.H. Effect of the mycotoxin aurofusarin on the antioxidant composition and fatty acid profile of quail eggs. Br. Poult. Sci. 2001, 42, 643–649. [CrossRef] [PubMed]
42. Ezekiel, C.N.; Bandyopadhyay, R.; Sulyok, M.; Warth, B.; Krska, R. Fungal and bacterial metabolites in commercial poultry feed from nigeria. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 2012, 29, 1288–1299. [CrossRef] [PubMed]
43. Nichea, M.J.; Palacios, S.A.; Chiacchiera, S.M.; Sulyok, M.; Krska, R.; Chulze, S.N.; Torres, A.M.; Ramirez, M.L. Presence of multiple mycotoxins and other fungal metabolites in native grasses from a wetland ecosystem in argentina intended for grazing cattle. Toxins 2015, 7, 3309–3329. [CrossRef] [PubMed]
44. Streit, E.; Schwab, C.; Sulyok, M.; Naehrer, K.; Krska, R.; Schatzmayr, G. Multi-mycotoxin screening reveals the occurrence of 139 different secondary metabolites in feed and feed ingredients. Toxins 2013, 5, 504–523. [CrossRef] [PubMed]
45. Tola, S.; Bureau, D.; Hooft, J.; Beamish, F.; Sulyok, M.; Krska, R.; Encarnação, P.; Petkam, R. Effects of wheat naturally contaminated with fusarium mycotoxins on growth performance and selected health indices of red tilapia (Oreochromis niloticus × O. mossambicus). Toxins 2015, 7, 1929–1944. [CrossRef] [PubMed]
46. Springler, A.; Vrubel, G.J.; Mayer, E.; Schatzmayr, G.; Novak, B. Effect of fusarium-derived metabolites on the barrier integrity of differentiated intestinal porcine epithelial cells (IPEC-J2). Toxins 2016, 8, 345. [CrossRef] [PubMed]
47. Dvorska, J.E.; Surai, P.F. Yeast glucomannans prevent deterioration of quail egg quality during aurofusarinotoxicosis. In Proceedings of the XVI European Symposium on the Quality of Poultry Meat and the X European Symposium on the Quality of Eggs and Egg Products, Sint-Brieuc-Ploufragan, France, 23–26 September 2003; pp. 93–101.
48. Dvorska, J.E.; Surai, P.F.; Speake, B.K.; Sparks, N.H. Antioxidant systems of the developing quail embryo are compromised by mycotoxin aurofusarin. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2002, 131, 197–205. [CrossRef]
49. Dvorska, J.E.; Surai, P.F.; Speake, B.K.; Sparks, N.H. Protective effect of modified glucomannans against aurofusarin-induced changes in quail egg and embryo. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2003, 135C, 337–343. [CrossRef]
50. BioViotica. Rubrofusarin. Available online: https://adipogen.com/productmanagement/resource/ download/type/sheet/id/8299 (acessed on 10 August 2018).
51. Marazzi, B.; Endress, P.K.; De Queiroz, L.P.; Conti, E. Phylogenetic relationships within Senna (Leguminosae, Cassiinae) based on three chloroplast DNA regions: Patterns in the evolution of floral symmetry and extrafloral nectaries. Am. J. Bot. 2006, 93, 288–303. [CrossRef] [PubMed]
52. Tanaka, H.; Tamura, T. The chemical constitution of rubrofusarin, a pigment from fusarium graminearum. Agric. Biol. Chem. 1962, 26, 767–770. [CrossRef]
53. Demicheli, C.; Bcraldo, H.; Tosi, L. Cu (II) and Ni (II) complexes of rubrofusarin and 6-galactosyl rubrofusarin. J. Braz. Chem. Soc. 1992, 52–54. [CrossRef]
54. Pereira, E.; Demicheli, C.; Peixoto, L. A spectrometric study of the chelating properties of 6-galactosyl-rubrofusarin: Mg (II), Al (III), Fe (III), Ni (II) and Cu(II). J. Braz. Chem. Soc. 1995, 6, 381–386. [CrossRef]
55. Moreira, L.M.; Lyon, J.P.; Lima, A.; Codognoto, L.; da Hora Machado, A.E.; de S. Tiago, F.; Araújo, D.M.S.; Silva, E.L.; Hioka, N.; Rodrigues, M.R.; et al. Quinquangulin and rubrofusarin: A. spectroscopy study. Orbital: Electron. J. Chem. 2017, 9. [CrossRef]
56. Branco, A.; Pinto, A.C.; Braz-Filho, R.; Silva, E.F.; Grynberg, N.F.; Echevarria, A. Rubrofusarin, a natural polyketide as new human topoisomerase II-α inhibitor. Rev. Bras. Farmacogn 2008, 18, 703–708. [CrossRef]
57. Mata, R.; Gamboa, A.; Macias, M.; Santillan, S.; Ulloa, M.; Gonzalez Mdel, C. Effect of selected phytotoxins from guanomyces polythrix on the calmodulin-dependent activity of the enzymes camp phosphodiesterase and NAD-kinase. J. Agric. Food Chem. 2003, 51, 4559–4562. [CrossRef] [PubMed]
58. European Molecular Biology Laboratory. Rubrofusarin B (CHEBI:133805). Available online: https://www. ebi.ac.uk/chebi/searchId.do?chebiId=CHEBI:133805 (accessed on 4 September 2018).
59. Song, Y.C.; Li, H.; Ye, Y.H.; Shan, C.Y.; Yang, Y.M.; Tan, R.X. Endophytic naphthopyrone metabolites are co-inhibitors of xanthine oxidase, SW1116 cell and some microbial growths. FEMS Microbiol. Lett. 2004, 241, 67–72. [CrossRef] [PubMed]
60. Rangaswami, S. Crystalline chemical components of the seeds of Cassia Tora Linn. Identity of Tora Substance C with rubrofusarin and Tora Substance B with nor-rubrofusarin. Proc. Indian Acad. Sci. Sect. A 1963, 57, 88–93.
61. Oliveira, A.; Fernandes, M.; Shaat, V.; Vasconcelos, L.; Gottlieb, O. Constituents of cassia species. Rev. Latinoamer. Quim. 1977, 8, 82–85.
62. Jing, Y.; Yang, J.; Wu, L.; Zhang, Z.; Fang, L. Rubrofusarin glucosides of Berchemia Polyphylla var. Leioclada and their scavenging activities for DPPH radical. Zhongguo Zhong Yao Za Zhi 2011, 36, 2084–2087. [PubMed]
63. Coelho, R.G.; Vilegas, W.; Devienne, K.F.; Raddi, M.S.G. A new cytotoxic naphthopyrone dimer from paepalanthus bromelioides. Fitoterapia 2000, 71, 497–500. [CrossRef]
64. Ernst-Russell, M.A.; Chai, C.L.L.; Wardlaw, J.H.; Elix, J.A. Euplectin and coneuplectin, new naphthopyrones from the lichen flavoparmelia euplecta. J. Nat. Prod. 2000, 63, 129–131. [CrossRef] [PubMed]
65. Mock, B.H.; Robbers, J.E. Biosynthesis of rubrofusarin by Fusarium graminearum. J. Pharm. Sci. 1969, 58, 1560–1562. [CrossRef] [PubMed]
66. Hallen, H.E.; Trail, F. The L-type calcium ion channel cch1 affects ascospore discharge and mycelial growth in the filamentous fungus gibberella zeae (anamorph Fusarium graminearum). Eukaryot. Cell 2008, 7, 415–424. [CrossRef] [PubMed]
67. Rugbjerg, P.; Naesby, M.; Mortensen, U.H.; Frandsen, R.J. Reconstruction of the biosynthetic pathway for the core fungal polyketide scaffold rubrofusarin in Saccharomyces cerevisiae. Microb. Cell Fact. 2013, 12, 31. [CrossRef] [PubMed]
68. Alqahtani, S.D.; Assiri, H.A.; Al-Abbasi, F.A.; El-Halawany, A.M.; Al-Abd, A.M. Abstract 1205: Rubrofusarin and toralactone sensitize resistant mcf-7adr cell line to paclitaxel via inhibiting p-glycoprotein efflux activity. Cancer Res. 2017, 77, 1205. [CrossRef]
69. El-Halawany, A.M.; Chung, M.H.; Nakamura, N.; Ma, C.M.; Nishihara, T.; Hattori, M. Estrogenic and anti-estrogenic activities of cassia tora phenolic constituents. Chem. Pharm. Bull. (Tokyo) 2007, 55, 1476–1482. [CrossRef] [PubMed]
70. Ghebremeskel, M.; Langseth, W. The occurrence of culmorin and hydroxy-culmorins in cereals. Mycopathologia 2001, 152, 103–108. [CrossRef] [PubMed]
71. Young, J.C.; Games, D.E. Supercritical fluid chromatography of fusarium mycotoxins. J. Chromatogr. 1992, 627, 247–254. [CrossRef]
72. Weber, J.; Vaclavikova, M.; Wiesenberger, G.; Haider, M.; Hametner, C.; Frohlich, J.; Berthiller, F.; Adam, G.; Mikula, H.; Fruhmann, P. Chemical synthesis of culmorin metabolites and their biologic role in culmorin and acetyl-culmorin treated wheat cells. Org. Biomol. Chem. 2018, 16, 2043–2048. [CrossRef] [PubMed]
73. National Center for Biotechnology Information. Culmorin. Available online: https://pubchem.ncbi.nlm.nih. gov/compound/Culmorin#section=Top (accessed on 5 September 2018).
74. Miller, J.D.; MacKenzie, S. Secondary Metabolites of Fusarium venenatum Strains with Deletions in The Tri5 Gene Encoding Trichodiene Synthetase. Mycologia 2000, 92, 764–771. [CrossRef]
75. Kasitu, G.C.; ApSimon, J.W.; Blackwell, B.A.; Fielder, D.A.; Greenhalgh, R.; Miller, J.D. Isolation and characterization of culmorin derivatives produced by Fusariumculmorum CMI 14764. Can. J. Chem. 1992, 70, 1308–1316. [CrossRef]
76. Langseth, W.; Ghebremeskel, M.; Kosiak, B.; Kolsaker, P.; Miller, D. Production of culmorin compounds and other secondary metabolites by Fusarium culmorum and F. Graminearum strains isolated from Norwegian cereals. Mycopathologia 2001, 152, 23–34. [CrossRef] [PubMed]
77. iChemLabs. 2D Sketcher. Chemdoodle Web Components. Available online: https://web.chemdoodle.com/ demos/sketcher/ (accessed on 9 September 2018).
78. Nara Institute of Science and Technology. Knapsack metabolite information—culmorin. Available online: http://kanaya.naist.jp/knapsack_jsp/information.jsp?word=C00021971 (accessed on 2 September 2018).
79. Pedersen, P.B.; Miller, J.D. The fungal metabolite culmorin and related compounds. Nat. Toxins 1999, 7, 305–309. [CrossRef]
80. Grafenhan, T.; Johnston, P.R.; Vaughan, M.M.; McCormick, S.P.; Proctor, R.H.; Busman, M.; Ward, T.J.; O’Donnell, K. Fusarium praegraminearum sp. Nov., a novel nivalenol mycotoxin-producing pathogen from New Zealand can induce head blight on wheat. Mycologia 2016, 108, 1229–1239. [PubMed]
81. Strongman, D.; Miller, J.; Calhoun, L.; Findlay, J.; Whitney, N. The biochemical basis for interference competition among some lignicolous marine fungi. Botanica Marina 1987, 30, 21–26. [CrossRef]
82. McCormick, S.P.; Alexander, N.J.; Harris, L.J. CLM1 of Fusarium graminearum encodes a longiborneol synthase required for culmorin production. Appl. Environ. Microbiol. 2010, 76, 136–141. [CrossRef] [PubMed]
83. National Center for Biotechnology, I. Gibberella zeae strain GZ3639 longiborneol synthase (CLM1) gene, complete cds. Available online: https://www.ncbi.nlm.nih.gov/nuccore/GU123140 (accessed on 7 September 2018).
84. Humer, E.; Lucke, A.; Harder, H.; Metzler-Zebeli, B.U.; Bohm, J.; Zebeli, Q. Effects of citric and lactic acid on the reduction of deoxynivalenol and its derivatives in feeds. Toxins 2016, 8, 285. [CrossRef] [PubMed]
85. Uhlig, S.; Eriksen, G.S.; Hofgaard, I.S.; Krska, R.; Beltran, E.; Sulyok, M. Faces of a changing climate: Semi-quantitative multi-mycotoxin analysis of grain grown in exceptional climatic conditions in Norway. Toxins 2013, 5, 1682–1697. [CrossRef] [PubMed]
86. Abia, W.A.; Warth, B.; Sulyok, M.; Krska, R.; Tchana, A.N.; Njobeh, P.B.; Dutton, M.F.; Moundipa, P.F. Determination of multi-mycotoxin occurrence in cereals, nuts and their products in cameroon by liquid chromatography tandem mass spectrometry (LC-MS/MS). Food Control 2013, 31, 438–453. [CrossRef]
87. Generotti, S.; Cirlini, M.; Sarkanj, B.; Sulyok, M.; Berthiller, F.; Dall’Asta, C.; Suman, M. Formulation and processing factors affecting trichothecene mycotoxins within industrial biscuit-making. Food Chem. 2017, 229, 597–603. [CrossRef] [PubMed]
88. Mastanjevic, K.; Sarkanj, B.; Krska, R.; Sulyok, M.; Warth, B.; Mastanjevic, K.; Santek, B.; Krstanovic, V. From malt to wheat beer: A comprehensive multi-toxin screening, transfer assessment and its influence on basic fermentation parameters. Food Chem. 2018, 254, 115–121. [CrossRef] [PubMed]
89. Delgado, R.M.; Sulyok, M.; Jirsa, O.; Spitzer, T.; Krska, R.; Polisenska, I. Relationship between lutein and mycotoxin content in durum wheat. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 2014, 31, 1274–1283. [CrossRef] [PubMed]
90. Dowd, P.F.; Miller, J.D.; Greenhalgh, R. Toxicity and interactions of some Fusarium graminearum metabolites to caterpillars. Mycologia 1989, 81, 646–650. [CrossRef]
91. Rotter, R.; Trenholm, H.; Prelusky, D.; Hartin, K.; Thompson, B.; Miller, J. A preliminary examination of potential interactions between deoxynivalenol (DON) and other selected Fusarium metabolites in growing pigs. Can. J. Anim. Sci. 1992, 72, 107–116. [CrossRef]
92. Trail, F.; Common, R. Perithecial development by gibberella zeae: A light microscopy study. Mycologia 2000, 130–138. [CrossRef]
93. Lawler, K.; Hammond-Kosack, K.; Brazma, A.; Coulson, R.M. Genomic clustering and co-regulation of transcriptional networks in the pathogenic fungus Fusarium graminearum. BMC Syst. Biol. 2013, 7, 52. [CrossRef] [PubMed]
94. Studt, L.; Wiemann, P.; Kleigrewe, K.; Humpf, H.-U.; Tudzynski, B. Biosynthesis of fusarubins accounts for pigmentation of Fusarium fujikuroi perithecia. Appl. Environ. Microbiol. 2012, 78, 4468–4480. [CrossRef] [PubMed]
95. Parisot, D.; Devys, M.; Barbier, M. Notizen: 5-Deoxybostrycoidin, a New Metabolite Produced by the Fungus Nectria haematococca (Berk. and Br.) Wr. Zeitschrift für Naturforschung B 1989, 44, 1473–1474. [CrossRef]
96. Ma, L.J.; Geiser, D.M.; Proctor, R.H.; Rooney, A.P.; O’Donnell, K.; Trail, F.; Gardiner, D.M.; Manners, J.M.; Kazan, K. Fusarium pathogenomics. Annu. Rev. Microbiol. 2013, 67, 399–416. [CrossRef] [PubMed]
97. O’Donnell, K.; Rooney, A.P.; Proctor, R.H.; Brown, D.W.; McCormick, S.P.; Ward, T.J.; Frandsen, R.J.; Lysoe, E.; Rehner, S.A.; Aoki, T.; et al. Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. Fungal Genet. Biol. 2013, 52, 20–31. [CrossRef] [PubMed]
98. Dadachova, E.; Bryan, R.A.; Howell, R.C.; Schweitzer, A.D.; Aisen, P.; Nosanchuk, J.D.; Casadevall, A. The radioprotective properties of fungal melanin are a function of its chemical composition, stable radical presence and spatial arrangement. Pigm. Cell Melanoma Res. 2008, 21, 192–199. [CrossRef] [PubMed]
99. Avalos, J.; Estrada, A.F. Regulation by light in fusarium. Fungal Genet. Biol. 2010, 47, 930–938. [CrossRef] [PubMed]
100. Prado-Cabrero, A.; Schaub, P.; Diaz-Sanchez, V.; Estrada, A.F.; Al-Babili, S.; Avalos, J. Deviation of the neurosporaxanthin pathway towards beta-carotene biosynthesis in fusarium fujikuroi by a point mutation in the phytoene desaturase gene. FEBS J. 2009, 276, 4582–4597. [CrossRef] [PubMed]
101. Avalos, J.; Cerdà-Olmedo, E. Carotenoid mutants of gibberella fujikuroi. Curr. Genet. 1987, 11, 505–511. [CrossRef]
102. Diaz-Sanchez, V.; Estrada, A.F.; Trautmann, D.; Al-Babili, S.; Avalos, J. The gene card encodes the aldehyde dehydrogenase responsible for neurosporaxanthin biosynthesis in fusarium fujikuroi. FEBS J. 2011, 278, 3164–3176. [CrossRef] [PubMed]
103. Kot, A.M.; Błazejak, S.; Gientka, I.; Kieliszek, M.; Bry´s, J. Torulene and torularhodin: “New” fungal ˙ carotenoids for industry? Microb. Cell Fact. 2018, 17, 49. [CrossRef] [PubMed]
104. Li, C.; Zhang, N.; Li, B.; Xu, Q.; Song, J.; Wei, N.; Wang, W.; Zou, H. Increased torulene accumulation in red yeast sporidiobolus pararoseus ngr as stress response to high salt conditions. Food Chem. 2017, 237, 1041–1047. [CrossRef] [PubMed]
105. National Center for Biotechnology, I. Torulene. Available online: https://pubchem.ncbi.nlm.nih.gov/ compound/5281253 (accessed on 12 September 2018).
106. Royal Society of Chemistry. Torulene. Available online: http://www.chemspider.com/Chemical-Structure. 4444665.html?rid=28fe93b0-090b-48cf-ba81-28141d575d21 (accessed on 2 September 2018).
107. Saelices, L.; Youssar, L.; Holdermann, I.; Al-Babili, S.; Avalos, J. Identification of the gene responsible for torulene cleavage in the neurospora carotenoid pathway. Mol. Genet. Genomics 2007, 278, 527–537. [CrossRef] [PubMed]
108. Shi, Q.; Wang, H.; Du, C.; Zhang, W.; Qian, H. Tentative identification of torulene cis/trans geometrical isomers isolated from sporidiobolus pararoseus by high-performance liquid chromatography-diode array detection-mass spectrometry and preparation by column chromatography. Anal. Sci. 2013, 29, 997–1002. [CrossRef] [PubMed]
109. Zoz, L.; Carvalho, J.C.; Soccol, V.T.; Casagrande, T.C.; Cardoso, L. Torularhodin and torulene: Bioproduction, properties and prospective applications in food and cosmetics—A review. Braz. Arch. Biol. Technol. 2015, 58, 278–288. [CrossRef]
110. Maldonade, I.R.; Rodriguez-Amaya, D.B.; Scamparini, A.R.P. Carotenoids of yeasts isolated from the brazilian ecosystem. Food Chem. 2008, 107, 145–150. [CrossRef]
111. Martín, J.-F.; García-Estrada, C.; Zeilinger, S. Biosynthesis and Molecular Genetics of Fungal Secondary Metabolites, 1st ed.; Springer-Verlag New York: New York, NY, USA, 2014.
112. National Center for Biotechnology, I. Neurosporaxanthin. Available online: https://pubchem.ncbi.nlm.nih. gov/compound/637039 (accessed on 11 September 2018).
113. Royal Society of Chemistry. Neurosporaxanthin. Available online: http://www.chemspider.com/ChemicalStructure.552701.html (accessed on 2 September 2018).
114. Prado-Cabrero, A.; Scherzinger, D.; Avalos, J.; Al-Babili, S. Retinal biosynthesis in fungi: Characterization of the carotenoid oxygenase Carx from Fusarium fujikuroi. Eukaryot. Cell 2007, 6, 650–657. [CrossRef] [PubMed]