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Alternaria Species and Mycotoxins Associated to Black Point of Cereals

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Alternaria Species and Mycotoxins Associated to Black Point of Cereals Mycotoxins 63 (1), 39-46 (2013) 39 Proceedings Paper www.jstage.jst.go.jp/browse/myco Alternaria species and mycotoxins associated to black point of cereals ＊ Maria T. AMATULLI, Francesca FANELLI, Antonio MORETTI, Giuseppina MULÈ, Antonio F. LOGRIECO Research National Council, Institute of Sciences of Food Production, Via Amendola 122/0 70126 Bari, Italy Key words : Alternaria; mycotoxins; wheat (Received January 25, 2013) Abstract Mycotoxins are secondary metabolites produced by several fungal species and represent a great concern for the economical and healthy implications on food and feed chain. Cereals are the primary source of human diet, wheat being the third most produced grain worldwide. Although Fusarium still represents the main source of mycotoxin contamination of wheat, in recent years, due also to evident climate changes that influence agricultural environment, other mycotoxingenic fungi have been pointed out as important wheat contaminants. Among these a disease called “Black Point”, caused by Alternaria spp., is increasing it importance as re-emerging risk. Diseases and mycotoxins (alternariol, altenuene, alternariol methyl-ether and tenuazolic acid) associated with Alternaria infection have been reported in several countries suggesting to deepen the knowledge about this genus. This paper summarizes the recent findings on wheat contamination by Alternaria spp and their related toxins. Introduction Alternaria spp. are worldwide distributed mainly as saprophyte in soil or in rot plant materials. They are also reported as contaminants of food commodities as well as fungal pathogens of several important crops, including cereals, oil crops, ornamentals, vegetable and fruits1, 2). Economic losses on fruits and vegetable trade are strongly dependent on the nature of the disease; they are usually lower compared to other fungal diseases but in some case they can lead to consistent losses3). In cereals, particularly wheat, barley and oat, Alternaria infection is generally not associated with yield losses but with a reduction in grains quality due to a discoloration of kernels and loss in nutritive values4, 5). Alternaria spp. are known for the production of a great number of secondary metabolites including mycotoxins and host specific toxins6, 7, 2). Among the Alter- naria mycotoxins, alternariol (AOH), alternariol monomethyl ether (AME), altenuene (ALT), and tenuazonic acid (TA), occur with higher frequency on plants8). Toxicity, mutagenicity and genotoxicity of these metabo- lites have been proved both in vitro and in vivo assays9-11). Alternaria spp. produce also host specific toxins that are required for fungal pathogenicity2). Moreover, Alternaria spores are one of the most common airborne allergens associated with respiratory diseases and skin infection in human12, 13). Corresponding Author ＊ Research National Council, Institute of Sciences of Food Production, Via Amendola 122/0 70126 Bari, Italy. E-mail: Antonio. [email protected] A full color PDF reprint of this article is available at the journal WEB site. 40 AMATULLI et al. Mycotoxins The ubiquitous presence of Alternaria spores is due to its flexibility in surviving under different weather conditions. Although sporulation and host infection generally occur at high temperature ( 25 - 32 °C), Alter- naria is able to survive in cold, hot, and dry weather and to overseasoning in debris and seeds3). The aim of this paper is to overview the recent data on Alternaria contamination on wheat reviewing the ecology and toxigenicity of this fungal genus. Ecology and epidemiology of Alternaria black point on wheat Alternaria spp. are the main causal agents of black point disease in cereals, particularly wheat and barley. Contamination of wheat kernel by Alternaria has been reported in different countries including Italy, China, Russia, Argentina, Tunisia and Slovakia4, 15-19). Although this disease does not affects harvest yield, it can compromise grain quality and its commercial value especially if kernels are address to milling and processing pathway. Symptoms on wheat are usually visible after harvesting and are promoted by frequent and persistent rainfall and exceeds of irrigation during kernel development and maturation. The disease consists of the dark discoloration of the embryo-end of the kernel even if embryo vitality is generally not affected. Different Alternaria species have been associated to this disease but A. alternata has been isolated with the higher frequency worldwide. Moreover, A. tricitina one of the most important causal agent of wheat leaf blight in Argentina, India and China20, 21) is also considered one of the main species involved in black point. Some of the species that generally contaminate wheat seeds, produce mycotoxins including ALT, AOH, AME, TeA and Altertoxins I, II and III (ATX-I, -II, -III). Alternaria mycotoxin contamination of wheat and grain based products have been reported in several countries: Italy, China, Canada, Argentina, Slovakia and Tunisia15, 22, 17-19), in some cases, contamination reached very high levels as in the case of 63 ppm of AOH, detected in soft wheat bran in Canada22). A molecular studies of the Italian population of Alternaria in wheat showed a great biodiversity inside the genus. Isolates were grouped in two main clades: the small-spored Alternaria species complex, including A. alternata, A. tenuissima and A. arborescens, and the A. infectoria species complex, that includes A. infectoria and A. triticina. In addition other 2 clades, grouping a smaller number of isolates, were identified. The comparison between the Italian strains and strains sampled worldwide, did not showed a correlation between phylogenesis and geographic origin of the strains. Indeed, isolates were grouped based only on their phylogenetic relationship23). Effect of climate changes on Alternaria spp. Occurrence During the 21 st century we are incurring in a dramatic warming trend that will influence natural and managed ecosystems. The climate changes that will occur in next years will affect natural ecosystem and biodiversity, shifting the composition of the organism in the environment in respect to their ability in the adaptation to climate change24). Temperature increases are predicted to be in a range of 6°C, having remarkable consequences for lifestyles, ecosystems, agriculture, and other livelihoods. In general, the projec- tions indicate that dry areas, especially in the latitude band just outside the tropics will tend to get drier on average25, 26). Areas that are already wet, especially in the tropics and closer to the poles, will tend to get wetter on average. Increased climate variability and increased evaporation in a warmer world will results in an increase in the occurrence and in the intensity of future droughts. Vol. 63, No. 1, 39-46 (2013) 41 Alternaria spp. have been isolated worldwide in a wide range of environmental conditions. Its flexibility to different climate is responsible for the apparent contradiction related to Alternaria diseases, which may develop either at high and low temperature, differences in moisture content, and under multiple combination of environmental factors. In a scenario of a rapid climate changes, the tolerance demonstrated by this fungal genus3), which is able to survive in prolonged stressing conditions of high and low temperature and dryness, increase the concern about Alternaria spp., which spreading could be potentially extended globally at higher levels of occurrence27). Alternaria toxins Alternaria spp produce more than 70 phytotoxins, but a small proportion of them have been chemically characterized and reported to act as mycotoxins to humans and animals. The most important Alternaria mycotoxins are AOH, AME, ALT, ATX-I, -II, -IIIand TeA, which belong to three structural classes28) : diben- zopyrone derivatives (AOH, AME, ALT), perylene derivatives (ATX-I, -II, -III) and tetramic acid derivatives (TeA). Several studies have demonstrated the in vitro toxicity of these mycotoxins including genotoxicity, inhibition of topoisomerase I and II, oestrogenicity and clastogenicity of AOH and AME29-31), high mutagen- icity of altertoxin II32)and tetratogenicity and foetotoxicity of different Alternaria cultures and extracts33-35). A recent study by Bensassi et al36).reported the AOH-induced cytotoxicity in human colon carcinoma cells, proponing a mechanism mediated by activation of the mitochondrial pathway of apoptosis. Moreover, AOH and AME contamination of grains in China has been related with oesophageal cancer in China by different studies37-39). Recently, the attention on Alternaria toxins is increasing both in research programs and risk assessment studies9), even though data published so far about Alternaria toxins are not enough to define a regulation about contamination limits in foodstuffs. Opinions of different European scientific committees40-42) assess the need to collect more information about the toxicity of these molecules to better understand the real risk for public health. The dietary exposure to Alternaria toxins is mainly related to grain and grain-based products, vegetables and vegetable products (in particular tomato products), fruits and fruit products, alcoholic beverages (wine and beer), oilseeds and vegetable oils (mainly sunflower seeds and sunflower oil). So far the only data reported on these toxins toxicity are related to acute exposure, and hence they cannot be used for any risk assessment. Environmental factors affecting Alternaria toxins Mycotoxins can be produced
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