Alternaria in food: Ecophysiology, mycotoxin production and toxicology

Mycobiology

Volumn 43, Issue 2, 2015, Pages 93-106

  Lee, Hyang Burm ^a   Patriarca, Andrea ^b   Magan, Naresh ^c  

^a Chonnam National University   (South Korea)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c CRANFIELD UNIVERSITY   (United Kingdom)

Author keywords

Alternaria species; Ecology; Food products; Mycotoxins; Physiology

Indexed keywords

ALTERNARIA; ALTERNARIA TENUISSIMA; FUNGI; LYCOPERSICON ESCULENTUM; MICROPUS; SORGHUM BICOLOR BICOLOR;

EID: 84937031008     PISSN: 12298093     EISSN: 20929323     Source Type: Journal    
DOI: 10.5941/MYCO.2015.43.2.93     Document Type: Review

References (73)

1. Robiglio AL, López SE. Mycotoxin production by Alternaria alternata strains isolated from red delicious apples in Argentina. Int J Food Microbiol 1995;24:413-7.
2. Solfrizzo M, Girolamo AD, Vitti C, Tylkowska K, Grabarkiewicz-Szczesna J, Szopinska D, Dorna H. Toxigenic profile of Alternaria alternata and Alternaria radicina occurring on umbelliferous plants. Food Addit Contam 2005;22:302-8.
3. Culshaw F, Cook, RJ, Magan N, Evans EJ. Blackpoint of wheat. London: Home Grown Cereals Authority; 1988.
4. Magan N, Lacey J. Effect of water activity, temperature and substrate on interactions between field and storage fungi. Trans Br Mycol Soc 1984;82:83-93.
5. Li F, Yoshizawa T. Alternaria mycotoxins in weathered wheat from China. J Agric Food Chem 2000;48:2920-4.
6. Patriarca A, Azcarate MP, Terminiello L, Fernández Pinto V. Mycotoxin production by Alternaria strains isolated from Argentinean wheat. Int J Food Microbiol 2007;119:219-22.
7. Andersen B, Thrane U, Svendsen A, Rasmussen IA. Associated field mycobiota on malt barley. Can J Bot 1996;74:854-8.
8. Kosiak B, Torp M, Skjerve E, Andersen B. Alternaria and Fusarium in Norwegian grains of reduced quality: a matched pair sample study. Int J Food Microbiol 2004;93:51-62.
9. Logrieco A, Moretti A, Solfrizzo M. Alternaria toxins and plant diseases: an overview of origin, occurrence and risks. World Mycotoxin J 2009;2:129-40.
10. Medina Á, Valle-Algarra FM, Mateo R, Gimeno-Adelantado JV, Mateo F, Jiménez M. Survey of the mycobiota of Spanish malting barley and evaluation of the mycotoxin producing potential of species of Alternaria, Aspergillus and Fusarium. Int J Food Microbiol 2006;108:196-203.
11. Webley DJ, Jackson KL, Mullins JD, Hocking AD, Pitt JI. Alternaria toxins in weather-damaged wheat and sorghum in the 1995-1996 Australian harvest. Aust J Agric Res 1997;48: 1249-56.
12. Woudenberg JH, Groenewald JZ, Binder M, Crous PW. Alternaria redefined. Stud Mycol 2013;75:171-212.
13. Azcarate MP, Patriarca A, Terminiello L, Fernández Pinto V. Alternaria toxins in wheat during the 2004 to 2005 Argentinean harvest. J Food Prot 2008;71:1262-5.
14. Liu GT, Qian YZ, Zhang P, Dong ZM, Shi ZY, Zhen YZ, Miao J, Xu YM. Relationships between Alternaria alternata and oesophageal cancer. IARC Sci Publ 1991;(105):258-62.
15. Liu GT, Qian YZ, Zhang P, Dong WH, Qi YM, Guo HT. Etiological role of Alternaria alternata in human oesophageal cancer. Chin Med J (Engl) 1992;105:394-400.
16. EFSA Panel on Contaminants in the Food Chain (CONTAM). Scientific opinion on the risks for animal and public health related to the presence of Alternaria toxins in feed and food. EFSA J 2011;9:2407.
17. Lopez P, Venema DP, de Rijk TC, de Kok A, Scholten J, Mol JG, de Nijs WC. Occurrence of Alternaria mycotoxins in food products in the Netherlands. In: World Mycotoxin Forum; 2014 Nov 10-12; Vienna, Austria.
18. Magan N, Aldred D. Why do fungi produce mycotoxins? In: Dijksterhuis J, Samson RA, editors. Food mycology: a multifaceted approach to fungi and food. Boca Raton: Taylor and Francis; 2007. p. 121-33.
19. Patriarca A, Medina A, Fernández Pinto V, Magan N. Temperature and water stress impacts on growth and production of altertoxin-II by strains of Alternaria tenuissima from Argentinean wheat. World Mycotoxin J 2014;7:329-34.
20. Oviedo MS, Ramirez ML, Barros GG, Chulze SN. Effect of environmental factors on tenuazonic acid production by Alternaria alternata on soybean-based media. J Appl Microbiol 2009;107:1186-92.
21. Pose G, Patriarca A, Kyanko V, Pardo A, Fernández Pinto V. Effect of water activity and temperature on growth of Alternaria alternata on a synthetic tomato medium. Int J Food Microbiol 2009;135:60-3.
22. Vaquera S, Patriarca A, Fernández Pinto V. Water activity and temperature effects on growth of Alternaria arborescens on tomato medium. Int J Food Microbiol 2014;185:136-9.
23. Magan N, Lacey J. The phylloplane microflora of ripening wheat and effect of late fungicide applications. Ann Appl Biol 1986;109:117-28.
24. Wallace HA, Sinha RN. Causal factors operative in distributional patterns and abundance of fungi: a multivariate study. In: Wicklow DT, Carroll GC, editors. The fungal community: its organization and role in the ecosystem. New York: Marcel Dekker; 1981. p. 233-47.
25. Magan N, Aldred D, Hope R, Mitchell D. Environmental factors and interactions with mycobiota of grain and grapes: effects on growth, deoxynivalenol and ochratoxin production by Fusarium culmorum and Aspergillus carbonarius. Toxins 2010;2;353-66.
26. Hope R. Ecology and control of Fusarium species and mycotoxins in wheat grain [dissertation]. Bedford: Cranfield University; 2004.
27. Magan N, Aldred D. Chapter 2. Environmental fluxes and fungal interactions: maintaining a competitive edge. In: Avery SV, Stratford M, Van West P, editors. Stress in yeasts and filamentous fungi. Amsterdam: Elsevier Ltd.; 2007. p. 19-36.
28. Marin S, Sanchis V, Ramos AJ, Vinas I, Magan N. Environmental factors, in vitro interactions, and niche overlap between Fusarium moniliforme, F. proliferatum, and F. graminearum, Aspergillus and Penicillium species from maize grain. Mycol Res 1998;102:831-7.
29. Lee HB, Magan N. Environmental factors and nutritional utilization patterns affect niche overlap indices between Aspergillus ochraceus and other spoilage fungi. Lett Appl Microbiol 1999;28:300-4.
30. Mohale S, Magan N, Medina A. Comparison of growth, nutritional utilisation patterns, and niche overlap indices of toxigenic and atoxigenic Aspergillus flavus strains. Fungal Biol 2013;117:650-9.
31. Müller ME, Urban K, Köppen R, Siegel D, Korn U, Koch M. Mycotoxins as antagonistic or supporting agents in the interaction between phytopathogenic Fusarium and Alternaria fungi. World Mycotoxin J 2015;8:311-21.
32. Magan N, Cayley GR, Lacey J. Effect of water activity and temperature on mycotoxin production by Alternaria alternata in culture and on wheat grain. Appl Environ Microbiol 1984; 47:1113-7.
33. Magan N, Lacey J. The effect of water activity and temperature on mycotoxin production by Alternaria alternata in culture and on wheat grain. In: Lacey J, editor. Trichothecenes and other mycotoxins. Chichester: Wiley & Sons; 1985. p. 243-56.
34. Sanchis V, Magan N. Environmental profiles for growth and mycotoxin production. Chapter 8. In: Magan N, Olsen M, editors. Mycotoxins in food: detection and control. Cambridge: Woodhead Publishing Ltd.; 2004. p. 174-89.
35. Oviedo MS, Ramirez ML, Barros GG, Chulze SN. Impact of water activity and temperature on growth and altenariol and altenariol monomethyl ether production of Alternaria alternata isolated from soybean. J Food Prot 2010;73:336-43.
36. Oviedo MS, Ramirez ML, Barros GG, Chulze SN. Influence of water activity and temperature on growth and mycotoxin production by Alternaria alternata on irradiated soya beans. Int J Food Microbiol 2011;149:127-32.
37. Magan N, Baxter ES. Relationship between environmental factors and tenuazonic acid production by Alternaria isolates from sorghum. In: Scudamore KA, editor. Occurrence and significance of mycotoxins. Slough: Central Science Laboratories; 1994. p. 309-13.
38. Pose G, Patriarca 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 Microbiol 2010;142:348-53.
39. Ostry V. Alternaria mycotoxins: an overview of chemical characterization, producers, toxicity, analysis and occurrence in foodstuffs. World Mycotoxin J 2008;1:175-88.
40. Scott PM. Other mycotoxins. In: Magan N, Olsen M, editors. Mycotoxins in food: detection and control. Cambridge: Woodhead Publishing Ltd.; 2004. p. 406-40.
41. Scussel VM, Scholten JM, Rensen PM, Spanjer MC. Multitoxins in cork stoppers and fermented beverages by liquid chromatography-mass spectrometry including Alternaria toxins. In: XIIth International IUPAC Symposium on Mycotoxins and Phycotoxins; 2007 May 21-25; Istanbul, Turkey; poster 1356.
42. Spanjer MC, Rensen PM, Scholten JM. LC-MS/MS multimethod for mycotoxins after single extraction, with validation data for peanut, pistachio, wheat, maize, cornflakes, raisins and figs. Food Addit Contam 2008;25:472-89.
43. Rasmussen RR, Storm IM, Rasmussen PH, Smedsgaard J, Nielsen KF. Multi-mycotoxin analysis of maize silage by LCMS/ MS. Anal Bioanal Chem 2010;397:765-76.
44. Wang S, Cheng L, Ji S, Wang K. Simultaneous determination of seventeen mycotoxins residues in Puerariae lobatae radix by liquid chromatography-tandem mass spectrometry. J Pharm Biomed Anal 2014;98:201-9.
45. Zur G, Hallerman EM, Sharf R, Kashi Y. Development of a polymerase chain reaction-based assay for the detection of Alternaria fungal contamination in food products. J Food Prot 1999;62:1191-7.
46. Somma S, Pose G, Pardo A, Mulè G, Pinto VF, Moretti A, Logriecoa AF. AFLP variability, toxin production, and pathogenicity of Alternaria species from Argentinean tomato fruits and puree. Int J Food Microbiol 2011;145:414-9.
47. Oviedo MS, Sturm ME, Reynoso MM, Chulze SN, Ramirez ML. Toxigenic profile and AFLP variability of Alternaria alternata and Alternaria infectoria occurring in wheat. Braz J Microbiol 2013;44:447-55.
48. Crespo-Sempere A, Estiarte N, Marín S, Sanchis V, Ramos AJ. Propidium monoazide combined with real-time quantitative PCR to quantify viable Alternaria spp. contamination in tomato products. Int J Food Microbiol 2013;165:214-20.
49. Abdel-Hadi A, Schmidt-Heydt M, Parra R, Geisen R, Magan N. A systems approach to model the relationship between aflatoxin gene cluster expression, environmental factors, growth and toxin production by Aspergillus flavus. J R Soc Interface 2012;9:757-67.
50. Medina A, Schmidt-Heydt M, Cárdenas-Chávez DL, Parra R, Geisen R, Magan N. Integrating toxin gene expression, growth and fumonisin B1 and B2 production by a strain of Fusarium verticillioides under different environmental factors. J R Soc Interface 2013;10:20130320.
51. Rivoire B, Attucci S, Anthonioz P, Carré P, Lemarié E, Hazouard E. Occupational acute lung injury due to Alternaria alternata: early stage of organic dust toxic syndrome requires no corticosteroids. Intensive Care Med 2001;27:1236-7.
52. Pero RW, Posner H, Blois M, Harvan D, Spalding JW. Toxicity of metabolites produced by the "Alternaria". Environ Health Perspect 1973;4:87-94.
53. Haubruge E, Chasseur C, Debouck C, Begaux F, Suetens C, Mathieu F, Michel V, Gaspar C, Rooze M, Hinsenkamp M, et al. The prevalence of mycotoxins in Kashin-Beck disease. Int Orthop 2001;25:159-61.
54. Menzies D, Comtois P, Pasztor J, Nunes F, Hanley JA. Aeroallergens and work-related respiratory symptoms among office workers. J Allergy Clin Immunol 1998;101(1 Pt 1):38-44.
55. Licorish K, Novey HS, Kozak P, Fairshter RD, Wilson AF. Role of Alternaria and Penicillium spores in the pathogenesis of asthma. J Allergy Clin Immunol 1985;76:819-25.
56. Brugger EM, Wagner J, Schumacher DM, Koch K, Podlech J, Metzler M, Lehmann L. Mutagenicity of the mycotoxin alternariol in cultured mammalian cells. Toxicol Lett 2006; 164:221-30.
57. Xu DS, Kong TQ, Ma JQ. The inhibitory effect of extracts from Fructis lycii and Rhiozoma polygonati on in vitro DNA breakage by alternariol. Biomed Environ Sci 1996;9:67-70.
58. Fehr M, Pahlke G, Fritz J, Christensen MO, Boege F, Altemöller M, Podlech J, Marko D. Alternariol acts as a topoisomerase poison, preferentially affecting the IIalpha isoform. Mol Nutr Food Res 2009;53:441-51.
59. Fleck SC, Burkhardt B, Pfeiffer E, Metzler M. Alternaria toxins: Altertoxin II is a much stronger mutagen and DNA strand breaking mycotoxin than alternariol and its methyl ether in cultured mammalian cells. Toxicol Lett 2012;214:27-32.
60. Terminiello L, Patriarca A, Pose G, Fernández Pinto V. Occurrence of alternariol, alternariol monomethyl ether and tenuazonic acid in Argentinean tomato puree. Mycotoxin Res 2006;22:236-40.
61. Gannibal PB, Orina AS, Mironenko NV, Levitin MM. Differentiation of the closely related species, Alternaria solani and A. tomatophila, by molecular and morphological features and aggressiveness. Eur J Plant Pathol 2014;139:609-23.
62. Lee HB, Yu SH. Incidence of Alternaria species in red pepper and sesame from Korea and their ability to produce mycotoxins. Korean J Plant Pathol 1995;11:1-8.
63. Lee HB, Yu SH. Distribution of mycotoxin-producing isolates in the genus Alternaria. Korean J Plant Pathol 1995;11:151-7.
64. Greco M, Patriarca A, Terminiello L, Fernández Pinto V, Pose G. Toxigenic Alternaria species from Argentinean blueberries. Int J Food Microbiol 2012;154:187-91.
65. Benavidez Rozo ME, Patriarca A, Cabrera G, Fernández Pinto VE. Determination of the profiles of secondary metabolites characteristic of Alternaria strains isolated from tomato. Rev Iberoam Micol 2014;31:119-24.
66. Polizzotto R, Andersen B, Martini M, Grisan S, Assante G, Musetti R. A polyphasic approach for the characterization of endophytic Alternaria strains isolated from grapevines. J Microbiol Methods 2012;88:162-71.
67. Jensen B, Knudsen IM, Andersen B, Nielsen KF, Thrane U, Jensen DF, Larsen J. Characterization of microbial communities and fungal metabolites on field grown strawberries from organic and conventional production. Int J Food Microbiol 2013;160:313-22.
68. Lawrence DP, Gannibal PB, Peever TL, Pryor BM. The sections of Alternaria: formalizing species-groups concepts. Mycologia 2013;105:530-46.
69. Mislivec PB, Bruce VR, Stack ME, Bandler R. Molds and tenuazonic acid in fresh tomatoes used for catsup production. J Food Prot 1987;1:38-41.
70. Motta SD, Valente Soares LM. Survey of Brazilian tomato products for alternariol, alternariol monomethyl ether, tenuazonic acid and cyclopiazonic acid. Food Addit Contam 2001;18:630-4.
71. Bottalico A, Logrieco A. Alternaria plant diseases in Mediterranean countries and associated mycotoxins. In: Chelkowski J, Visconti A, editors. Alternaria: biology plant diseases and metabolites. Amsterdam: Elsevier; 1992. p. 209-32.
72. Visconti A, Sibilia A, Sabia C. Alternaria alternata from oilseed rape: mycotoxin production, and toxicity to Artemia salina larvae and rape seedlings. Mycotoxin Res 1992;8:9-16.
73. Andersen B, Nielsen KF, Fernández Pinto V, Patriarca A. Characterization of Alternaria strains from Argentinean blueberry, tomato, walnut and wheat. Int J Food Microbiol 2015;196:1-10.