Maize (51%)

1Kernels and flour.

1Kernels and flour.

There are two kinds of maize ear rot, roughly differentiated as "red ear rot" or "red fu-sariosis", caused mainly by species of the Discolor section, and "pink ear rot" or "pink fu-sariosis", caused mainly by representatives of the Liseola section (Bottalico, 1998). The distribution and prevalence of the different Fusarium species causing these two kinds of ear rot disease are largely governed by environmental conditions, primarily temperature and humidity (Bottalico, 1998). In general, "red fusariosis" is particularly severe in years and locations characterized by frequent rainfalls and low temperatures during summer and early fall, while "pink fusariosis" prevails in the drier and warmer climates of Southern Europe (Bottalico, 1998). Among the species causing maize "red ear rot" the most common ones are F. graminearum, F. culmorum, and to a lesser extent F. cerealis and F. avenaceum. The species most frequently isolated from maize "pink ear rot" are Fusarium verticillioides (te-leomorph Gibberella moniliformis), Fusarium proliferatum (teleomorph Gibberella intermedia), and F. subglutinans (teleomorph Gibberella subglutinans). All of these species can produce several mycotoxins in naturally infected maize kernels, including trichothecenes, zearalenone, and fumonisins. Other potentially toxic metabolites produced by Fusarium spp., e.g., beauvericin and moniliformin, also have been found on maize although the toxicity of these compounds needs to be better evaluated. For information on the main chemical and toxic features of the mycotoxins produced by Fusarium species commonly occurring on maize, see Logrieco et al. (2002c) or Desjardins (2006).

Geographic distribution of Fusarium species

Central and Northern Europe - Maize "red ear rot". The main pathogen of maize red ear rot, is F. graminearum. Reports from Austria, Slovenia, Yugoslavia, Poland, Czech Republic, and Romania (Logrieco et al., 2002c) clearly indicate that F. graminearum is increa singly common in Central and Northern Europe. Fusarium graminearum occasionally is associated with many other Fusarium species, whose occurrence and prevalence vary by region and year, depending primarily on climatic conditions (temperature and rain) and less importantly on tillage practices (crop rotation, fertilization and planting area). Fusarium graminearum, F. culmorum and F. cerealis co-occur more frequently in Central Europe. Fusarium sporotrichioides also can cause maize red ear rot, but only rarely cause epidemics. This species occurs in the northern and colder regions of Europe where maize cultivation is common, e.g., Poland, and is better adapted to extremely cold environmental conditions than are other Fusarium species. In northern Italy, only in unusually cold seasons does F. graminearum occur at high incidence on maize kernels. A very rare report of F. graminearum from Southern Italy was due to maize grown as a second crop that was harvested at the end of November under cooler and wetter conditions than usual (Logrieco et al., 2003).

Central and Southern Europe - Maize "pink ear rot'. Maize "pink ear rot" is common in Southern and Central European areas. The species most commonly associated with pink ear rot were F. verticillioides, F. subglutinans and to a lesser extent F. proliferatum. Fusarium proliferatum was more common in Southern Europe, and was displaced by F. subglutinans in central areas where the latter predominates as the primary causal agent of pink ear rot and usually is isolated much more frequently than is F. verticillioides. Fusarium prolifera-tum commonly co-occurs with F. verticillioides in Italy (Logrieco et al., 2002c), but in Austria, Croatia, Hungary, and the Slovak Republic, F. proliferatum is only rarely isolated (Logrieco et al., 2002c). The unusually dry and warm summers that occurred in the late 1990s increased the incidence of F. proliferatum in Central Europe and the species was reported from the Slovak Republic in 1996 (Srobarova et al., 2002) and from Austria (Logrieco et al., 2002c). In Yugoslavia (Logrieco et al., 2002c) during a three-year survey (1994-96) of maize ears Fusarium species present at harvest included F. verticillioides, F. subglutinans, and F. proliferatum. In Italy, where environmental conditions often are conducive to a high incidence of maize pink ear rot, F. verticillioides dominates, with F. proli-feratum co-occurring in southern areas in over 60% of the infected kernels and then declining in frequency from the central to the northern parts of the country (Logrieco et al., 2002c). However, F. proliferatum is assumed to be more widespread than reported since it can be misidentified relatively easily as F. verticillioides.


Mycotoxin production depends on temperature, substrate and aw, however, the optimum climatic conditions for mycotoxin production in grain varies by genus, species and isolate. Most studies indicate that high moisture and warm temperatures favor the production of all classes of mycotoxins. However, production of type A trichothecenes by F. sporotri-chioides requires moderate temperatures and low moisture rather than warmer temperatures and higher aws (Mateo et al., 2002). The production of type B trichothecenes is favored when infected grain is stored under warm humid conditions (Martins and Martins, 2002). The conditions for optimal production of zearalenone also are species, isolate and substrate specific, and may differ from those that are optional for trichothecene production. Reports of an optimum temperature for zearalenone production are confusing and vary depending on the isolate and the substrate (Doohan et al., 2003). Fumonisins commonly are produced in maize infected by F. verticillioides and F. proliferatum, species that usually grow better at higher temperatures. The optimal aw for the production of fumonisins seems to be high (aw ~ 0.98), but varies depending on temperature, which may be optimal across a relatively wide range, e.g., 15-30°C (Marin et al., 1999).

Trichothecenes and zearalenone. Epidemics of maize red ear rot, induced by F. graminea-rum, F. culmorum and F. cerealis usually lead to the widespread occurrence of zearalenone, deoxynivalenol, and to a lesser incidence of nivalenol and fusarenon X. The severity of the disease is not always proportional to the amount of toxin produced, and unexpectedly high levels of toxins may occur in the absence of severe disease symptoms. A survey in 1977 found that zearalenone occurred in maize ears infected by F. graminearum when the maize was grown as a second crop in southern Italy and harvested when weather conditions were cooler and wetter than usual. The occurrence of nivalenol and fusarenon X in Europe is most closely related to the presence of F. cerealis rather than the presence of F. graminea-rum as reported in Austria, Finland, Germany, Poland, and Yugoslavia (Logrieco et al., 2002c), since F. graminearum nivalenol-chemotype strains are rare. Finally, accumulation of T-2 toxin in maize ears usually is related to epidemics of F. sporotrichioides as seen in Poland when record low temperatures occurred (Logrieco et al., 2002c).

Fumonisins. Fumonisins usually are formed in plants infected with F. verticillioides or F. proliferatum and are commonly found in maize prior to harvest. The incidence of fumoni-sin B1 in maize and maize-based foods and feed in Europe is increasing and problematic (SCOOP, 2003). In general, fumonisin B1 in maize is most important in Southern Europe, e.g., Portugal, France, Spain, Croatia and Italy (Logrieco et al., 2002c). In Italy, high levels of fumonisins (up to 250 ^g/g) were more often associated with pink ear rot than they were in other European countries (Bottalico, 1998). Moreover, an investigation carried out over a five-year period (1995-1999) by Pietri et al. (2004) found that fumonisin B1 is the most common mycotoxin in northern Italian maize and that contamination with other mycotoxins usually is low, with the exception of 1996, a year in which high levels of deoxynivalenol contamination also occurred.

Fumonisin Bi levels are significantly lower in Central to Northeastern Europe (Bottalico, 1998). In some northern areas, under very favorable conditions, fumonisins can accumulate to significant levels (up to 30 ^g/g), as reported for the Slovak Republic in 1998, and may be accompanied by severe epidemics of F. verticillioides and F. proliferatum (Srobarova et al., 2002). Thus, the risk of fumonisin B1 contamination is highest in Southern Europe, where both the major fungal producers of fumonisin B1, F. verticillioides and F. proliferatum, co-occur.

Moniliformin. In infected maize ears, the main moniliformin-producing Fusarium species are F. subglutinans, and F. proliferatum. Fusarium subglutinans is widespread in Central to Northern Europe, whereas F. proliferatum is increasingly common in South and Central European maize-growing areas (Logrieco et al., 1995). In Italy, high levels of moniliformin were found in maize ears co-infected with F. proliferatum and F. verticillioides (Logrieco et al., 2002c). Moniliformin also was found commonly in maize ears infected with F. sub-glutinans from Central and Northern European countries, including Austria and Poland, with very high amounts of moniliformin found in years with severe epidemics of F. subglu-tinans. The high incidence of moniliformin in maize ear rot from Austria and Poland also may be related to the occurrence of F. avenaceum, although this species rarely occurs at high frequencies on maize kernels (Logrieco et al., 2002c). The co-occurrence of F. avenaceum and F. subglutinans in maize in Central and Northern Europe increases the risk of moniliformin accumulation in infected ears. Thus, moniliformin may be the most commonly expected mycotoxin associated with maize ear rot in Central Europe.

Beauvericin. In maize ears infected with F. verticillioides, F. subglutinans and F. prolife-ratum, beauvericin co-occurred with fumonisin Bi produced by F. verticillioides or F. pro-liferatum, and/or moniliformin produced by F. subglutinans and F. proliferatum. In particular, beauvericin was reported in Italy, Poland and Austria (Logrieco et al., 2002c), and in the Slovak Republic (Srobarova et al., 2002). However, beauvericin is presumed to be more widespread than recorded, since it is produced not only by F. proliferatum and F. subgluti-nans, but also by several other Fusarium species that occur less frequently on maize including F. tricinctum (Logrieco et al., 1998) and F. poae (Chelkowski et al., 2007).

Aspergillus maize infection and aflatoxins: A future problem for Southern Europe?


Aflatoxins are produced by some strains of A. flavus, which synthesize aflatoxin B1 and af-latoxin B2, and by most strains of A. parasiticus, which also synthesize aflatoxin G1 and aflatoxin G2. Of these four main aflatoxins, aflatoxin B1 and aflatoxin G1, occur most frequently and at the highest levels in plant products. Aflatoxin-producing strains of A. flavus and A. parasiticus are distributed worldwide in soil and air. Some strains are plant pathogens and can infect maize in the field and then colonize harvested or stored maize kernels where aflatoxins accumulate. The contamination of maize by aflatoxins is a worldwide problem of particular concern in tropical and sub-tropical areas, although A. flavus and A. parasiticus also may colonize maize before harvest under favorable climatic conditions in the United States and Southern Europe. Hence, crops may be contaminated with aflatoxins, which leads to the contamination of processed maize-based foods and feeds. Such contamination is dangerous because aflatoxins are mutagenic, teratogenic and carcinogenic compounds that are classified by the IARC as Group 1 compounds, i.e., compounds known to be carcinogenic to humans (IARC, 1993).

Occurrence of aflatoxins and aflatoxin producers on maize in Southern Europe

European Union legislation limits maize intended for feed to < 20 ng/g aflatoxin B1 and maize intended for human consumption to < 2 ng/g aflatoxin B1. Although some contamination of maize in the field always occurs (Pietri et al., 2004), the occurrence of aflatoxins in excess of the European Union limits in maize kernels and maize-based products is rare in Italy. During the 2003 cropping season, environmental conditions during maize cultivation enabled high levels of maize contamination by aflatoxins in northern Italy. The weather was very hot and dry for several months, which water-stressed the maize plants and resulted in a very early harvest of very dry kernels. Thus, the levels of the aflatoxin B1 contamination in 2003 were 5-70 times higher then the levels observed from 1995-2000. Over 25% of the flour samples intended for polenta preparation analyzed between November 2003 and

June 2004, were contaminated by aflatoxin Bi at levels > 2 ng/g legal limit. Moreover, since this maize also was used to feed dairy cattle, the milk produced was highly contaminated by aflatoxin Mi leading to the dumping of thousands of tons of contaminated milk (Pinelli et al., 2005). Such incidents confirm the widespread occurrence of aflatoxigenic strains of Aspergillus in Italy and stress the importance of good agricultural practices (GAPs) both in the field and post-harvest. As the global climate changes to become hotter and drier, the possibility that all of Southern Europe may face a constant threat of aflatoxin contamination increases.

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