El editor solo permite decargar el artículo en su versión post-print desde el repositorio. Por favor, si usted posee dicha versión, enviela a
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor


The group of the small-spored Alternaria species is particularly relevant in foods due to its high frequency and wide distribution in different crops. These species are responsible for the accumulation of mycotoxins and bioactive secondary metabolites in food. The taxonomy of the genus has been recently revised with particular attention on them; several morphospecies within this group cannot be segregated by phylogenetic methods, and the most recent classifications proposed to elevate several phylogenetic species-groups to the taxonomic status of section. The purpose of the present study was to compare the new taxonomic revisions in Alternaria with secondary metabolite profiles with special focus on sections Alternaria and Infectoriae and food safety. A total of 360 small-spored Alternaria isolates from Argentinean food crops (tomato fruit, pepper fruit, blueberry, apple, wheat grain, walnut, pear, and plum) was morphologically identified to species-group according to Simmons (2007), and their secondary metabolite profile was determined. The isolates belonged to A. infectoria sp.-grp. (19), A. tenuissima sp.-grp. (262), A. arborescens sp.-grp. (40), and A. alternata sp.-grp. (7); 32 isolates, presenting characteristics overlapping between the last three groups, were classified as Alternaria sp. A high chemical diversity was observed; 78 different metabolites were detected, 31 of them of known chemical structure. The isolates from A. infectoria sp.-grp. (=Alternaria section Infectoriae) presented a specific secondary metabolite profile, different from the other species-groups. Infectopyrones, novae-zelandins and phomapyrones were the most frequent metabolites produced by section Infectoriae. Altertoxin-I and alterperylenol were the only compounds that these isolates produced in common with members of section Alternaria. None of the well-known Alternaria toxins, considered relevant in foods, namely alternariol (AOH), alternariol monomethyl ether (AME), tenuazonic acid (TeA), tentoxin (TEN) or altenuene (ALT), were produced by isolates of this section. On the other hand, strains from section Alternaria (A. tenuissima, A. arborescens, and A. alternata sp.-grps.) shared a common metabolite profile, indistinguishable from each other. AOH, AME, ALT, TEN, and TeA were the most frequently mycotoxins produced, together with pyrenochaetic acid A and altechromone A. Alternaria section Alternaria represents a substantial risk in food, since their members in all types of crops are able to produce the toxic metabolites. © 2018 Elsevier B.V.


Documento: Artículo
Título:Secondary metabolite profiles of small-spored Alternaria support the new phylogenetic organization of the genus
Autor:Patriarca, A.; da Cruz Cabral, L.; Pavicich, M.A.; Nielsen, K.F.; Andersen, B.
Filiación:Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Departamento de Química Orgánica, Laboratorio de Microbiología de Alimentos. CONICET, Instituto de Micología y Botánica (INMIBO), Buenos Aires, Argentina
Department of Biotechnology and Biomedicine, Technical University of Denmark, Kgs. Lyngby, DK-2800, Denmark
Palabras clave:Alternaria; Food safety; Secondary metabolite profiles; Section Alternaria; Section Infectoriae; altenuene; alternariol; alternariol monomethyl ether; alterperylenol; altertoxin i; infectopyrone derivative; mycotoxin; natural product; novae zelandin derivative; phomapyrone derivative; tentoxin; tenuazonic acid; unclassified drug; cyclopeptide; lactone; mycotoxin; tenuazonic acid; Alternaria; Alternaria alternata; Alternaria arborescens; Alternaria infectoria; Alternaria tenuissima; apple; Article; blueberry; food crop; food safety; fungal strain; fungus isolation; genus; grain; metabolite; morphospecies; nonhuman; pear; pepper; phylogeny; plum; tea; tomato; walnut; wheat; Alternaria; analysis; Argentina; black pepper; classification; crop; food contamination; food control; fruit; Malus; metabolism; microbiology; Pyrus; secondary metabolism; Alternaria; Argentina; Blueberry Plants; Crops, Agricultural; Food Contamination; Food Microbiology; Fruit; Juglans; Lactones; Lycopersicon esculentum; Malus; Mycotoxins; Peptides, Cyclic; Phylogeny; Piper nigrum; Prunus domestica; Pyrus; Secondary Metabolism; Tenuazonic Acid; Triticum
Página de inicio:135
Página de fin:143
Título revista:International Journal of Food Microbiology
Título revista abreviado:Int. J. Food Microbiol.
CAS:alternariol, 641-38-3; tenuazonic acid, 610-88-8, 75652-74-3; lactone, 1338-03-0; altenuene; alternariol; alternariol monomethyl ether; Lactones; Mycotoxins; Peptides, Cyclic; tentoxin; Tenuazonic Acid


  • Andersen, B., Thrane, U., Differentiation of Alternaria infectoria and Alternaria alternata based on morphology, metabolite profiles, and cultural characteristics (1996) Can. J. Microbiol., 42, pp. 685-689
  • Andersen, B., Krøger, E., Roberts, R.G., Chemical and morphological segregation of Alternaria alternata, A. gaisen and A. longipes (2001) Mycol. Res., 105, pp. 291-299
  • Andersen, B., Krøger, E., Roberts, R.G., Chemical and morphological segregation of Alternaria arborescens, A. infectoria and A. tenuissima species groups (2002) Mycol. Res., 106, pp. 170-182
  • Andersen, B., Hansen, M.E., Smedsgaard, J., Automated and unbiased image analyses as tools in phenotypic classification of small-spored Alternaria spp (2005) Phytopathology, 95, pp. 1021-1029
  • Andersen, B., Dongo, A., Pryor, B.M., Secondary metabolite profiling of Alternaria dauci, A. porri, A. solani and A. tomatophila (2008) Mycol. Res., 112, pp. 241-250
  • Andersen, B., Sørensen, J.L., Nielsen, K.F., van den Ende, B.G., de Hoog, S., A polyphasic approach to the taxonomy of the Alternaria infectoria species–group (2009) Fungal Genet. Biol., 46, pp. 642-656
  • Andersen, B., Nielsen, K.F., Fernández Pinto, V., Patriarca, A., Characterization of Alternaria strains from Argentinean blueberry, tomato, walnut and wheat (2015) Int. J. Food Microbiol., 196, pp. 1-10
  • Azcarate, M.P., Patriarca, A., Terminiello, L., Fernández Pinto, V., Alternaria toxins in wheat during the 2004 to 2005 Argentinean harvest (2008) J. Food Prot., 71 (6), pp. 1262-1265
  • Blandino, M., Scarpino, V., Sulyok, M., Krska, R., Reyneri, A., Effect of agronomic programmes with different susceptibility to deoxynivalenol risk on emerging contamination in winter wheat (2017) Eur. J. Agron., 85, pp. 12-24
  • Broggi, L.E., González, H.H.L., Resnik, S.L., Pacin, A., Alternaria alternata prevalence in cereal grains and soybean seeds from Entre Ríos, Argentina (2007) Rev. Iberoam. Micol., 24, pp. 47-51
  • Broggi, L., Reynoso, C., Resnik, S., Martinez, F., Drunday, V., Bernal, Á.R., Occurrence of alternariol and alternariol monomethyl ether in beverages from the Entre Rios Province market, Argentina (2013) Mycotoxin Res., 29, pp. 17-22
  • Christensen, K.B., Van Klink, J.W., Weavers, R.T., Larsen, T.O., Andersen, B., Phipps, R.K., Novel chemotaxonomic markers of the Alternaria infectoria species-group (2005) J. Agric. Food Chem., 53, pp. 9431-9435
  • Chulze, S.N., Torres, A.M., Dalcero, A.M., Etcheverry, M.G., Ramirez, M.L., Farnochi, M.C., Alternaria mycotoxins in sunflower seeds: incidence and distribution of the toxins in oil and meal (1995) J. Food Prot., 58, pp. 1133-1134
  • da Cruz Cabral, L., Terminiello, L., Fernández Pinto, V., Nielsen, K.F., Patriarca, A., Natural occurrence of mycotoxins and toxigenic capacity of Alternaria strains from mouldy peppers (2016) Int. J. Food Microbiol., 236, pp. 155-160
  • da Cruz Cabral, L., Rodriguero, M., Stenglein, S., Nielsen, K.F., Patriarca, A., Characterization of small-spored Alternaria from Argentinean crops through a polyphasic approach (2017) Int. J. Food Microbiol., 257, pp. 206-215
  • Dugan, F.M., Peever, T.L., Morphological and cultural differentiation of described species of Alternaria from Poaceae (2002) Mycotaxon, 83, pp. 229-264
  • EFSA, Alexander, J., Benford, D., Boobis, A., Ceccatelli, S., Cottrill, B., Cravedi, J., Di Domenico, A., Doerge, D., Dogliotti, E., Edler, L. Scientific opinion on the risks for animal and public health related to the presence of Alternaria toxins in feed and food (2011) EFSA J., 9, pp. 2407-2504
  • EFSA, Arcella, D., Eskola, M., Gómez Ruiz, J.A. Dietary exposure assessment to Alternaria toxins in the European population (2016) EFSA J., 14 (12), p. 4654
  • Frisvad, J.C., Andersen, B., Thrane, U., The use of secondary metabolite profiling in chemotaxonomy of filamentous fungi (2008) Mycol. Res., 112, pp. 231-240
  • Gannibal, P.B., Lawrence, D.P., Distribution of Alternaria species among sections. 3. Sections Infectoriae and Pseudoalternaria (2016) Mycotaxon, 131, pp. 781-790
  • Geiseler, O., Podlech, J., Total synthesis of infectopyrone, aplysiopsenes A–C, ent-aplysiopsene D, phomapyrones A and D, 8, 9‑dehydroxylarone, and nectriapyrone (2012) Tetrahedron, 68, pp. 7280-7287
  • Greco, M., Patriarca, A., Terminiello, L., Pinto, V.F., Pose, G., Toxigenic Alternaria species from Argentinean blueberries (2012) Int. J. Food Microbiol., 154, pp. 187-191
  • Gu, W., Bioactive metabolites from Alternaria brassicicola ML-P08, an endophytic fungus residing in Malus halliana (2009) World J. Microbiol. Biotechnol., 25, p. 1677
  • Hertz, M., Jensen, I.R., Jensen, L.Ø., Thomsen, S.N., Winde, J., Dueholm, M.S., Sørensen, L.H., Sørensen, J.L., The fungal community changes over time in developing wheat heads (2016) Int. J. Food Microbiol., 222, pp. 30-39
  • Hickert, S., Bergmann, M., Ersen, S., Cramer, B., Humpf, H.U., Survey of Alternaria toxin contamination in food from the German market, using a rapid HPLC–MS/MS approach (2016) Mycotoxin Res., 32, pp. 7-18
  • Ivanova, L., Petersen, D., Uhlig, S., Phomenins and fatty acids from Alternaria infectoria (2010) Toxicon, 55, pp. 1107-1114
  • Kildgaard, S., Mansson, M., Dosen, I., Klitgaard, A., Frisvad, J.C., Larsen, T.O., Nielsen, K.F., Accurate dereplication of bioactive secondary metabolites from marine-derived fungi by UHPLC-DAD-QTOFMS and a MS/HRMS Library (2014) Mar. Drugs, 12, pp. 3681-3705
  • Königs, P., Rinker, B., Maus, L., Nieger, M., Rheinheimer, J., Waldvogel, S., Structural revision and synthesis of altechromone A (2010) J. Nat. Prod., 73, pp. 2064-2066
  • Larsen, T.O., Perry, N.B., Andersen, B., Infectopyrone, a potential mycotoxin from Alternaria infectoria (2003) Tetrahedron Lett., 44, pp. 4511-4513
  • Lawrence, D.P., Gannibal, P.B., Peever, T.L., Pryor, B., The sections of Alternaria: formalizing species-group concepts (2013) Mycologia, 105 (3), pp. 530-546
  • Lawrence, D.P., Gannibal, P.B., Dugan, F.M., Pryor, B.M., Characterization of Alternaria isolates from the infectoria species-group and a new taxon from Arrhenatherum, Pseudoalternaria arrhenatheria sp. nov (2014) Mycol. Prog., 13, pp. 257-276
  • Lawrence, D.P., Rotondo, F., Gannibal, P.B., Biodiversity and taxonomy of the pleomorphic genus Alternaria (2016) Mycol. Prog., 15 (3), pp. 1-22
  • López, P., Venema, D., de Rijk, T., de Kok, A., Scholten, J.M., Mol, H.G.J., de Nijs, M., Occurrence of Alternaria toxins in food products in the Netherlands (2016) Food Control, 60, pp. 196-204
  • Nemecek, G., Cudaj, J., Podlech, J., Revision of the structure and total synthesis of altenuisol (2012) Eur. J. Org. Chem., 2012, pp. 3863-3870
  • Nielsen, K.F., Larsen, T.O., The importance of mass spectrometric dereplication in fungal secondary metabolite analysis (2015) Front. Microbiol., 6 (71), pp. 1-15
  • Oviedo, M., Barros, G., Chulze, S., Ramirez, M., Natural occurrence of alternariol and alternariol monomethyl ether in soya beans (2012) Mycotoxin Res., 28, pp. 169-174
  • Patriarca, A., Alternaria in food products (2016) Curr. Opin. Food Sci., 11, pp. 1-9
  • Patriarca, A., Azcarate, M., Terminiello, L., Pinto, V.F., Mycotoxin production by Alternaria strains isolated from Argentinean wheat (2007) Int. J. Food Microbiol., 119, pp. 219-222
  • Pedras, M.S.C., Chumala, P.B., Phomapyrones from blackleg causing phytopathogenic fungi: isolation, structure determination, biosyntheses and biological activity (2005) Phytochemistry, 66, pp. 81-87
  • Pedras, M.S.C., Park, M.R., Metabolite diversity in the plant pathogen Alternaria brassicicola: factors affecting production of brassicicolin A, depudecin, phomapyrone A and other metabolites (2015) Mycologia, 107, pp. 1138-1150
  • Peres, N.A.R., Agostini, J.P., Timmer, L.W., Outbreaks of Alternaria brown spot of citrus in Brazil and Argentina (2003) Plant Dis., 87, p. 750
  • Pero, R.W., Posner, H., Blois, M., Harvan, D., Spalding, J.W., Toxicity of metabolites produced by the “Alternaria” (1973) Environ. Health Perspect., 4, pp. 87-94
  • Pitt, J.I., Hocking, A.D., Fungi and Food Spoilage (2009), Springer Boston, MA; Pose, G., Ludemann, V., Segura, J., Fernández Pinto, V., Mycotoxin production by Alternaria strains isolated from tomatoes affected by Blackmold in Argentina (2004) Mycotoxin Res., 20, p. 80
  • Pose, G.N., Ludemann, V., Fernandez, D., Segura, J.A., Pinto, V.F., Alternaria species associated with ‘moldy heart’ on peaches in Argentina (2010) Trop. Plant Pathol., 35, pp. 174-177
  • Robiglio, A.L., Lopez, S.E., Mycotoxin production by Alternaria alternata strains isolated from red delicious apples in Argentina (1995) Int. J. Food Microbiol., 24, pp. 413-417
  • Rychlik, M., Lepper, H., Weidner, C., Asam, S., Risk evaluation of the Alternaria mycotoxin tenuazonic acid in foods for adults and infants and subsequent risk management (2016) Food Control, 68, pp. 181-185
  • Samson, R.A., Houbraken, J., Thrane, U., Frisvad, J.C., Andersen, B., Food and Indoor Fungi (2010) CBS Laboratory Manual Series 2, , CBS-Fungal Biodiversity Centre Utrecht
  • Sato, H., Konoma, K., Sakamura, S., Three new phytotoxins produced by Pyrenochaeta terrestris: pyrenochaetic acids A, B and C (1981) Agric. Biol. Chem., 45, pp. 1675-1679
  • Serdani, M., Ji-Chuan, K.A.N.G., Andersen, B., Crous, P.W., Characterisation of Alternaria species-groups associated with core rot of apples in South Africa (2002) Mycol. Res., 106, pp. 561-569
  • Simmons, E.G., Alternaria taxonomy: Current status, viewpoint, challenge (1992) Alternaria: Biology, Plant Diseases, and Metabolites, pp. 1-35. , J. Chelkowski A. Visconti Elsevier New York
  • Simmons, E.G., Alternaria: an identification manual (2007), 6. , CBS Biodiversity Utrecht; Simmons, E.G., Roberts, R., Alternaria themes and variations (73) (1993) Mycotaxon, 48, pp. 109-140
  • Solfrizzo, M., Recent advances on Alternaria mycotoxins (2017) Curr. Opin. Food Sci., 17, pp. 57-61
  • Terminiello, L., Patriarca, A., Pose, G., Fernández Pinto, V., Occurrence of alternariol, alternariol monomethyl ether and tenuazonic acid in Argentinean tomato puree (2006) Mycotoxin Res., 22, pp. 236-240
  • Vargas Trinidad, A., Ganoza, F.Q., Fernández Pinto, V., Patriarca, A., Determination of mycotoxin profiles characteristic of Alternaria strains isolated from Malbec grapes (2015) BIO Web of Conferences, p. 02004. , EDP Sciences
  • Walravens, J., Mikula, H., Rychlik, M., Asam, S., Ediage, E.N., Di Mavungu, J.D., Van Landschoot, A., De Saeger, S., Development and validation of an ultra-high-performance liquid chromatography tandem mass spectrometric method for the simultaneous determination of free and conjugated Alternaria toxins in cereal-based foodstuffs (2014) J. Chromatogr. A, 1372, pp. 91-101
  • Webley, D.J., Jackson, K.L., Mullins, J.D., Hocking, A.D., Pitt, J.I., Alternaria toxins in weather-damaged wheat and sorghum in the 1995–1996 Australian harvest (1997) Aust. J. Agric. Res., 48, pp. 1249-1256
  • Woudenberg, J.H.C., Groenewald, J.Z., Binder, M., Crous, P.W., Alternaria redefined (2013) Stud. Mycol., 75, pp. 171-212
  • Woudenberg, J.H.C., Seidl, M.F., Groenewald, J.Z., de Vries, M., Stielow, J.B., Thomma, B.P.H.J., Crous, P.W., Alternaria section Alternaria: species, formae speciales or pathotypes? (2015) Stud. Mycol., 82, pp. 1-21
  • Zwickel, T., Klaffke, H., Richards, K., Rychlik, M., Development of a high performance liquid chromatography tandem mass spectrometry based analysis for the simultaneous quantification of various Alternaria toxins in wine, vegetable juices and fruit juices (2016) J. Chromatogr. A, 1455, pp. 74-85
  • Zwickel, T., Kahl, S.M., Rychlik, M., Müller, M.E.H., Chemotaxonomy of mycotoxigenic small-spored Alternaria fungi – do multitoxin mixtures act as an indicator for species differentiation? (2018) Front. Microbiol., 9, p. 1368


---------- APA ----------
Patriarca, A., da Cruz Cabral, L., Pavicich, M.A., Nielsen, K.F. & Andersen, B. (2019) . Secondary metabolite profiles of small-spored Alternaria support the new phylogenetic organization of the genus. International Journal of Food Microbiology, 291, 135-143.
---------- CHICAGO ----------
Patriarca, A., da Cruz Cabral, L., Pavicich, M.A., Nielsen, K.F., Andersen, B. "Secondary metabolite profiles of small-spored Alternaria support the new phylogenetic organization of the genus" . International Journal of Food Microbiology 291 (2019) : 135-143.
---------- MLA ----------
Patriarca, A., da Cruz Cabral, L., Pavicich, M.A., Nielsen, K.F., Andersen, B. "Secondary metabolite profiles of small-spored Alternaria support the new phylogenetic organization of the genus" . International Journal of Food Microbiology, vol. 291, 2019, pp. 135-143.
---------- VANCOUVER ----------
Patriarca, A., da Cruz Cabral, L., Pavicich, M.A., Nielsen, K.F., Andersen, B. Secondary metabolite profiles of small-spored Alternaria support the new phylogenetic organization of the genus. Int. J. Food Microbiol. 2019;291:135-143.