Alternaria Genusu Üyelerinin Meyve ve Sebzeler Üzerine Etkileri

Öz

Alternaria yağlı tohumlar, tahıllar, meyve ve sebzelerde bozulmaya neden olan mikotoksijenik bir mikrofungus cinsidir. Gıdaları hasat öncesi ve hasat sırasında çeşitli yollarla enfekte ederek yanıklık, siyah çürüklük olarak adlandırılan bozulmalara neden olmaktadır. Ayrıca düşük sıcaklıklarda gelişim göstermesinden dolayı hasat sonrası depolama ve taşıma sırasında da bozulmaya neden olarak gıda endüstrisinde önemli ekonomik kayıplara yol açmaktadır. Günümüzde Alternaria genusuna ait türlerin 70 ’den fazla sekonder metabolit ürettiği bilinmektedir. Ancak bu sekonder metabolitlerin bazıları insan sağlığına olumsuz yönde etki eden mikotoksinlerdir. Yapılan birçok çalışmada rapor edilen alternariol (AOH), alternariol metil eter (AME), tenuazonik asit (TeA), tentoksin (TEN) ve altenuen (ALT), Alternaria cinsine ait türlerinin ürettiği en önemli mikotoksinlerdir. Bu derlemede Alternaria türleri, önemli mikotoksinleri, gelişimi ve toksin oluşumuna etki eden faktörleri ve meyve ve sebzelerdeki önemi hakkında yapılan çalışmalar bir araya getirilmiştir.

Anahtar Kelimeler

• Alternaria
• Metabolit
• Mikotoksin
• Meyve
• Sebze

Effects of Genus Alternaria Members on Fruit and Vegetables

Öz

Alternaria is a mycotoxigenic microfungus genus that causes deterioration in oilseeds, grains, fruits and vegetables. It infects foods before and during harvest in various ways, causing spoilage called blight, black rot. Besides, due to its development at low temperatures, it causes deterioration during post-harvest storage and transportation, leading to significant economic losses in the food industry. Today, it is known that Alternaria species are producing more than 70 secondary metabolites. However, some of these secondary metabolites are mycotoxins that negatively affect human health. Alternariol (AOH), alternariol methyl ether (AME), tenuazonic acid (TeA), tentoxin (TEN), and altenuene (ALT) reported in many studies are the most critical mycotoxins produced by species belong to Genus Alternaria. In this review, the studies on Alternaria species, their mycotoxins, factors affecting their growth and toxin formation are combined with the studies about their importance in fruit and vegetables.

Anahtar Kelimeler

• Alternaria
• Metabolite
• Mycotoxin
• Fruit
• Vegetable

Kaynakça

1. Aiello, D., Guarnaccia, V., Azzaro, A. and Polizzi, G. (2020). Alternaria Brown Spot on New Clones of Sweet Orange and Lemon in Italy. Phytopathol. Mediterr., 59 (1) 131-145.
2. Amirmajdi, M. M., Amirmajdi, N. A. M., Mashhadi, I. E., Azad, F. J., Afshari, J. T. and Shakeri, M. T. (2011). Alternaria in Patients with Allergic Rhinitis. Ann. Allergy Asthma Immunol., 221-226.
3. Andersen, B. and Thrane, U. (2006). Food-borne Fungi in Fruit and Cereals and Their Production of Mycotoxins, Advances in Food Mycology. Boston: Springer.
4. Andersen, B., Krøger, E. and Roberts, R. G. (2001). Chemical and Morphological Segregation of Alternaria alternata, A. gaisen and A. longipes. Mycol. Res., 105 (3) 291-299.
5. Anonymous (2020a). https://ag.umass.edu/vegetable/fact-sheets/solanaceous-alternaria-fruit-rot/, (Erişim tarihi: 25 Ağustos 2020).
6. Anonymous (2020b). https://www.fwi.co.uk/arable/stop-stealth-potato-disease-sneaking-radar/, (Erişim tarihi: 25 Ağustos 2020).
7. Anonymous (2020c). http://www.omafra.gov.on.ca/IPM/english/potatoes/diseases-and-disorders/alternaria.html/. (Erişim tarihi: 25 Ağustos 2020).
8. Anonymous (2020d). https://www.forestryimages.org/browse/detail.cfm?imgnum=5492320/, (Erişim tarihi: 25 Ağustos 2020).

9. Anonymous (2020e). https://www.pestnet.org/fact_sheets/carrot_black_rot_204.htm/, (Erişim tarihi: 25 Ağustos 2020).
10. Anonymous (2020g). http://blogs.cornell.edu/plantpathhvl/blog/page/2/, (Erişim tarihi: 25 Ağustos 2020).
11. Anonymous(2020f).https://www.reddit.com/r/mildlyinteresting/comments/6oq3ur/i_cut_open_an_orange_to_find_this_black_decay/, (Erişim tarihi: 25 Ağustos 2020).
12. Asam, S., Konitzer, K. and Rychlik, M. (2011).Precise Determination of the Alternaria Mycotoxins Alternariol and Alternariol Monomethyl Ether in Cereal, Fruit and Vegetable Products Using Stable Isotope Dilution Assays. Mycotoxin Res., 27 (1) 23-28.
13. Avenot, H. F., Solorio, C., Morgan, D. P. and Michailides, T. J. (2016). Sensitivity and Cross-resistance Patterns to Demethylation-inhibiting Fungicides in California Populations of Alternaria alternata Pathogenic on Pistachio. Crop Prot., 88 72-78.
14. Barkai-Golan, R., 2008. Alternaria Mycotoxins, Mycotoxins in Fruits and Vegetables. San Diego: Academic Press.
15. Broggi, L., Reynoso, C., Resnik, S., Martinez, F., Drunday, V. and Bernal, Á. R. (2013). Occurrence of Alternariol and Alternariol Monomethyl Ether in Beverages from the Entre Rios Province Market, Argentina. Mycotoxin Res., 29 (1) 17-22.
16. Chaerani, R. and Voorrips, R. E. (2006). Tomato Early Blight (Alternaria solani): the Pathogen, Genetics, and Breeding for Resistance. J. Gen. Plant Pathol., 72 (6) 335-347.
17. Chou, H.H. and Wu, W.S. (2002). Phylogenetic Analysis of Internal Transcribed Spacer Regions of the Genus Alternaria, and the Significance of Filament-beaked Conidia. Mycol. Res., 106 164-169.
18. Çalış, Ö. ve Yazar, Ç. (2011). Fare Kulağı Teresi, Arabidopsis thaliana’da Konukçu Dışı Dayanıklılığın Erken Yanıklık Hastalık Etmeni Alternaria solani 'nin Kontrolü için Araştırılması. Gaziosmanpaşa Üniv. Ziraat Fak. Derg., 2011 (2) 179-186.
19. Da Cruz Cabral, L., Terminiello, L., Pinto, V. F., Nielsen, K. F. and Patriarca, A. (2016). Natural Occurrence of Mycotoxins and Toxigenic Capacity of Alternaria Strains from Mouldy Peppers. Int. J. Food Microbiol., 236 155-160.
20. Dall’Asta, C., Cirlini, M. and Falavigna, C. (2014). Mycotoxins from Alternaria: Toxicological Implications, Advances in Molecular Toxicology (pp. 107-121). Elsevier.
21. De Hoog, G. S. and Horre, R. (2002). Molecular Taxonomy of the Alternaria and Ulocladium Species from Humans and their Identification in the Routine Laboratory. Mycoses, 45 (7‐8) 259-276.
22. Escrivá, L., Oueslati, S., Font, G. and Manyes, L. (2017). Alternaria Mycotoxins in Food and Feed: an Overview. J. Food Qual., 1569748.
23. Escuredo, O., Seijo, M. C., Fernández-González, M. and Iglesias, I. (2011). Effects of Meteorological Factors on the Levels of Alternaria Spores on a Potato Crop. Int. J. Biometeorol., 55 (2) 243-252.
24. Estiarte, N., Lawrence, C. B., Sanchis, V., Ramos, A. J. and Crespo-Sempere, A. (2016). LaeA and VeA are Involved in Growth Morphology, Asexual Development, and Mycotoxin Production in Alternaria alternata. Int. J. Food Microbiol., 238 153-164.
25. Fraeyman, S., Croubels, S., Devreese, M. and Antonissen, G. (2017). Emerging Fusarium and Alternaria Mycotoxins: Occurrence, Toxicity and Toxicokinetics. Toxins, 9 (7) 228.
26. Gambacorta, L., Magistà, D., Perrone, G., Murgolo, S., Logrieco, A. F. and Solfrizzo, M. (2018). Co-occurrence of Toxigenic Moulds, Aflatoxins, Ochratoxin A, Fusarium and Alternaria Mycotoxins in Fresh Sweet Peppers (Capsicum annuum) and their Processed Products. World Mycotoxin J., 11 (1) 159-174.
27. Garibaldi, A., Gilardi, G., Matic, S. and Gullino, M. L. (2019). First Report of Alternaria alternata on Chili Pepper (Capsicum frutescens) in Italy. Plant Dis., 103 (5) 1024.
28. Graf, E., Schmidt-Heydt, M. and Geisen, R. (2012). HOG MAP Kinase Regulation of Alternariol Biosynthesis in Alternaria alternata is Important for Substrate Colonization. Int. J. Food Microbiol., 157 (3) 353-359.
29. Gravesen, S., Frisvad, J. C. and Samson, R. A. (1994). Microfungi, Copenghang: High Tech PrePres A/S.
30. Greco, M., Patriarca, A., Terminiello, L., Pinto, V. F. and Pose, G. (2012). Toxigenic Alternaria Species from Argentinean Blueberries. Int. J. Food Microbiol., 154 (3) 187-191.
31. Hajnal, E. J., Čolović, R., Pezo, L., Orčić, D., Vukmirović and Đ., Mastilović, J. (2016). Possibility of Alternaria Toxins Reduction by Extrusion Processing of whole Wheat Flour. Food Chem., 213 784-790.
32. Hong, S.G., Cramer, R.A., Lawrence, C.B. and Pryor, B.M. (2005). Alt a1 allergen Homologs from Alternaria and Related Taxa: Analysis of Phylogenetic Content and Secondary Structure. Fungal Genet. Biol., 42 119-129.
33. Hyang B. L., Patriarca A. and Magan N. (2015). Alternaria in Food: Ecophysiology, Mycotoxin Production and Toxicology. Kor. J. Mycol., 43 (2) 93-106.
34. Inderbitzin, P., Shoemaker, R. A., O'Neill, N. R., Turgeon, B. G. and Berbee, M. L. (2006). Systematics and Mating Systems of two Fungal Pathogens of Opium Poppy: the Heterothallic Crivellia papaveracea with a Brachycladium Penicillatum Asexual State and a Homothallic Species with a Brachycladium papaveris Asexual State. Botany, 84 (8) 1304-1326.
35. Jackson, L. S. and Al-Taher, F. (2008). Factors Affecting Mycotoxin Production in Fruits. In: Barkai-Golan, R. And Paster, N. (Ed.), Mycotoxins in fruits and vegetables (pp. 75-104). San Diego: USA.
36. Kathe, L., Nothnagel, T., Krämer, R., Budahn, H., Rabenstein, F. and Pillen, K. (2017). Characterisation of Alternaria radicina Isolates and Assessment of Resistance in Carrot (Daucus carota L.). J. Kulturpflanzen, 69 277-290
37. Landschoot S., Vandecasteele M., De Baets B., Höfte M., Audenaert K. and Haesaert G. (2017). Identification of A. arborescens, A. grandis, and A. protenta as New Members of the European Alternaria Population on Potato. Fungal Biol. 121 (2) 172-188.
38. Lawrence, D. P., Gannibal, P. B., Peever, T. L. and Pryor, B. M. (2013). The Sections of Alternaria: Formalizing Species-Group Concepts. Mycologia, 105 (3) 530-546.
39. Lawrence, D. P., Park, M. S. and Pryor, B. M. (2012). Nimbya and Embellisia revisited, with nov. comb for Alternaria celosiae and A. perpunctulata. Mycol. Prog., 11 (3) 799-815.
40. Li, Y., Ma, Y., Zhang, T., Bi, Y., Wang, Y. and Prusky, D. (2019). Exogenous Polyamines Enhance Resistance to Alternaria alternata by Modulating Redox Homeostasis in Apricot Fruit. Food Chem., 301 125303.
41. Lopez, P., Venema, D., Mol, H., Spanjer, M., de Stoppelaar, J., Pfeiffer, E. and de Nijs, M. (2016). Alternaria Toxins and Conjugates in Selected Foods in the Netherlands. Food Control, 69 153-159.
42. Lopez, S. E. and Cabral, D. (1999). Alternaria, Encyclopedia of Food Microbiology. London: Academic Press.
43. Mikula, H., Skrinjar, P., Sohr, B., Ellmer, D., Hametner, C. and Fröhlich, J. (2013). Total Synthesis of Masked Alternaria Mycotoxins-sulfates and Glucosides of Alternariol (AOH) and Alternariol-9-methyl ether (AME). Tetrahedron, 69 (48), 10322-10330.
44. Mohsin, S. M., Islam, M. R., Ahmmed, A. N. F., Nisha, H. A. C. and Hasanuzzaman, M. (2016). Cultural, Morphological and Pathogenic Characterization of Alternaria porri Causing Purple Blotch of Onion. Not. Bot. Horti. Agrobot Cluj Napoca, 44 (1) 222-227.
45. Nishikawa, J. and Nakashima, C. (2019). Morphological and Molecular Characterization of the Strawberry Black Leaf Spot Pathogen Referred to as the Strawberry Pathotype of Alternaria alternata. Mycoscience, 60 (1) 1-9.
46. Noser, J., Schneider, P., Rother, M. and Schmutz, H. (2011). Determination of six Alternaria toxins with UPLC-MS/MS and their Occurrence in Tomatoes and Tomato Products from the Swiss Market. Mycotoxin Res., 27 (4) 265-271.
47. Ntasiou, P., Myresiotis, C., Konstantinou, S., Papadopoulou-Mourkidou, E. and Karaoglanidis, G. S. (2015). Identification, Characterization and Mycotoxigenic Ability of Alternaria spp. Causing Core Rot of Apple Fruit in Greece. Int. J. Food Microbiol., 197 22-29.
48. Ostry, V. (2008). Alternaria Mycotoxins: an Overview of Chemical Characterization, Producers, Toxicity, Analysis and Occurrence in foodstuffs. World Mycotoxin J., 1 (2) 175-188.
49. Ostry, V., Skarkova, J., Prochazkova, I., Kubatova, A. and Ruprich, J. (2007). Mycobiota of Czech Wine Grapes and Occurrence of Ochratoxin A and Alternaria Mycotoxins in Fresh Grape Juice, Must and Wine. Czech Mycol., 59 (2) 241.
50. Oviedo, M. S., Ramirez, M. L., Barros, G. G. and Chulze, S. N. (2011). Influence of Water Activity and Temperature on Growth and Mycotoxin Production by Alternaria alternata on Irradiated Soya Beans. Int. J. Food Microbiol., 149 (2) 127-132.
51. Oviedo, M. S., Sturm, M. E., Reynoso, M. M., Chulze, S. N. and Ramirez, M. L. (2013). Toxigenic Profile and AFLP Variability of Alternaria alternata and Alternaria infectoria Occurring on Wheat. Braz. J. Microbiol., 44 (2) 447-455.
52. Pane, C. and Zaccardelli, M. (2015). Evaluation of Bacillus Strains Isolated from Solanaceous Phylloplane for Biocontrol of Alternaria Early Blight of Tomato. Biol. Control, 84 11-18.
53. Patriarca, A., Azcarate, M. P., Terminiello, L. and Pinto, V. F. (2007). Mycotoxin Production by Alternaria Strains Isolated from Argentinean Wheat. Int. J. Food Microbiol.,119 (3) 219-222.
54. Phuwapraisirisan, P., Rangsan, J., Siripong, P. and Tip-pyang, S. (2009). New Antitumour Fungal Metabolites from Alternaria porri. Nat. Prod. Res., 23 (12) 1063-1071.
55. Pose, G., Patriarca, A., Kyanko, V., Pardo, A. and Pinto, V. F. (2010). Water Activity and Temperature Effects on Mycotoxin Production by Alternaria alternata on a Synthetic Tomato Medium. Int. J. Food Microbiol., 142 (3) 348-353.
56. Prajapati, M. K., Simon, S. and Faisal, M. (2019a). Efficacy of Organic Amendments Against the Purple Blotch of Garlic (Alternaria porri). Int. J. Pharmacogn. Phytochem., 8 (1) 1896-1898.
57. Prajapati, M. K., Simon, S. and Khan, K. Z. (2019b). Efficacy of Organic Amendments Against the Purple Blotch of Garlic Caused by Alternaria porri (Ellis) Cif. Int. J. Pharmacogn. Phytochem., 8 (1) 08-10.
58. Pryor B. M. and Bigelow D. M. (2003) Molecular Characterization of Embellisia and Nimbya Species and their Relationship to Alternaria, Ulocladium and Stemphylium. Mycologia, 95 1141-1154.
59. Pryor B. M., Creamer R., Shoemaker R. A., McLain-Romero J. and Hambleton S. (2009). Undifilum, A New Genus for Endophytic Embellisia oxytropis and Parasitic Helminthosporium bornmuelleri on Legumes. Botany, 87 (2) 178-194.
60. Pryor, B. M. and Gilbertson, R. L. (2000). Molecular Phylogenetic Relationships Amongst Alternaria Species and Related Fungi Based Upon Analysis of Nuclear ITS and mt SSU rDNA Sequences. Mycol. Res., 104 1312-1321.
61. Rahimloo, T. and Ghosta, Y. (2015). The Occurrence of Alternaria Species on Cabbage in Iran. Zemdirbyste, 102 (3).
62. Ravikumar, M. C., Singh, H. and Garampalli, R. H. (2016). Comparative Evaluation of Long-term Storage Techniques on Viability and Virulence of Alternaria solani. J. Taibah Univ. Sci., 10 (4) 607-613.
63. Reddy, M. B., Angers, P., Castaigne, F. and Arul, J. (2000). Chitosan Effects on Blackmold Rot and Pathogenic Factors Produced by Alternaria alternata in Postharvest Tomatoes. J. Am. Soc. Hortic. Sci., 125 (6) 742-747.
64. Roberts, R. G., Bischoff, J. F. and Reymond, S. T. (2012). Differential Gene Expression in Alternaria gaisen Exposed to Dark and Light. Mycol. Prog., 11 (2) 373-382.
65. Runa, F., Park, M. S. and Pryor, B. M. (2009). Ulocladium Systematics Revisited: Phylogeny and Taxonomic Status. Mycol. Prog., 8 (1) 35.
66. Samson, R. A., Houbraken, J., Thrane, U., Frisvad, J. C. and Andersen, B. (2010). Food and Indoor Fungi. Utrecht: Centraalbureay voor Schimmelcultures.
67. Sanchis, V. and Magan, N. (2004). Environmental Conditions Affecting Mycotoxins. Mycotoxins in food: Detection and Control, Boca Raton: CRC Press.
68. Sanzani, S. M., Gallone, T., Garganese, F., Caruso, A. G., Amenduni, M. and Ippolito, A. (2019). Contamination of Fresh and Dried Tomato by Alternaria Toxins in Southern Italy. Food Addit. Contam., 36 (5) 789-799.
69. Sanzani, S. M., Reverberi, M. and Geisen, R. (2016). Mycotoxins in Harvested Fruits and Vegetables: Insights in Producing Fungi, Biological Role, Conducive Conditions, and Tools to Manage Postharvest Contamination. Postharvest Biol. Technol., 122 95-105.
70. Scott, P. M., Zhao, W., Feng, S. and Lau, B. P. Y. (2012). Alternaria Toxins Alternariol and Alternariol Monomethyl ether in Grain Foods in Canada. Mycotoxin Res., 28 (4) 261-266.
71. Simmons, E.G., (2007). Alternaria: an Identification Manual. Utrecht: CBS Fungal Diversity Centre.
72. Solfrizzo, M. (2017). Recent Advances on Alternaria Mycotoxins. Curr. Opin. Food Sci., 17 57-61.
73. Solfrizzo, M., Girolamo, A. D., Vitti, C., Tylkowska, K., Grabarkiewicz-Szczęsna, J., Szopińska, D. and Dorna, H. (2005). Toxigenic profile of Alternaria alternata and Alternaria radicina Occurring on Umbelliferous Plants. Food Addit. Contam., 22 (4) 302-308.
74. Somma, S., Pose, G., Pardo, A., Mulè, G., Pinto, V. F., Moretti, A. and Logrieco, A. F. (2011). AFLP Variability, Toxin Production and Pathogenicity of Alternaria Species from Argentinean Tomato Fruits and Puree. Int. J. Food Microbiol., 145 (2-3) 414-419.
75. Tančinová, D., Felšöciová, S., Rybárik, Ľ., Mašková, Z. and Císarová, M. (2015). Colonization of Grapes Berries and Cider by Potential Producers of Patulin. Potr. S. J. F. Sci., 9 (1) 138-142.
76. Tournas, V. H., Stack, M. E. (2001). Production of Alternariol and Alternariol Methyl Ether by Alternaria alternata Grown on Fruits at Various Temperatures. J. Food Prot., 64 (4) 528-532.
77. Van de Perre, E., Jacxsens, L., Liu, C., Devlieghere, F. and De Meulenaer, B. (2015). Climate Impact on Alternaria Moulds and their Mycotoxins in Fresh Produce: The Case of the Tomato Chain. Food Res. Int., 68 41-46.
78. Vaquera, S., Patriarca, A. and Pinto, V. F. (2014). Water Activity and Temperature Effects on Growth of Alternaria arborescens on Tomato Medium. Int. J. Food Microbiol.,185 136-139.
79. Wang Y., Geng Y., Ma J., Wang Q. and Zhang X. (2011). Sinomyces: A New Genus of Anamorphic Pleosporacea. Fungal Biol., 115 188–195.
80. Wolters, P. J., Faino, L., Van Den Bosch, T. B., Evenhuis, B., Visser, R. G., Seidl, M. F. and Vleeshouwers, V. G. (2018). Gapless Genome Assembly of the Potato and Tomato Early Blight Pathogen Alternaria solani. Mol. Plant Microbe Interact., 31 (7) 692-694.
81. Woudenberg, J. H. C., Groenewald, J. Z., Binder, M. and Crous, P. W. (2013). Alternaria Redefined. Stud. Mycol., 75 171-212.
82. Woudenberg, J. H. C., Seidl, M. F., Groenewald, J. Z., De Vries, M., Stielow, J. B., Thomma, B. P. H. J. and Crous, P. W. (2015). Alternaria Section Alternaria: Species, Formae Speciales or Pathotypes. Stud. Mycol., 82 1-21.
83. Yuan, S., Yan, J., Wang, M., Ding, X., Zhang, Y., Li, W., Jiang, W. (2019). Transcriptomic and Metabolic Profiling Reveals ‘Green Ring’and ‘Red Ring’on Jujube Fruit Upon Postharvest Alternaria alternata Infection. Plant Cell Physiol., 60 (4) 844-861.
84. Zhang, S., Wang, Q., Guo, Y., Kang, L. and Yu, Y. (2020). Carbon Monoxide Enhances the Resistance of Jujube Fruit Against Postharvest Alternaria Rot. Postharvest Biol. Technol., 168 111268.
85. Zheng, H. H. and Wu, X. H. (2013). First Report of Alternaria Blight of Potato Caused by Alternaria tenuissima in China. Plant Dis., 97 (9) 1246-1246.