Wheat

Fusarium head blight and related toxins

Fusarium species

Several Fusarium species are widespread pathogens of soft and durum wheats worldwide, including all European cereal-growing areas where they may cause stem and ear rots and severely reduce crop yields. In addition, several Fusarium strains can produce mycotoxins either in preharvest infected plants in the fields or in stored grain (Bottalico, 1998). The occurrence of mycotoxins in wheat is of great concern worldwide, because their presence in processed feeds and foods seems almost unavoidable. Virtually all of the wheat grown in Northern Europe is at least to some extent contaminated by deoxynivalenol, whereas wheat grown in southern parts of the continent is less contaminated by Fusarium toxins (Bottalico and Perrone, 2002). To the most common and best known mycotoxin contaminants of wheat, i.e., trichothecenes, zearale-none and moniliformin, are now being added new problems, e.g., the cyclic hexadepsipeptides enniatins and beauvericin (Logrieco et al., 2002a; Uhlig et al., 2006).

Fusarium species that cause Fusarium head blight of wheat can affect individual kernels, single spikelets or entire heads. Infected spikelets first appear water-soaked and then lose their chlorophyll and become straw-colored. In warm, humid weather, pinkish-red my-celia and conidia develop abundantly in the infected spikelets, and the infection spreads to adjacent spikelets. Infected kernels become shriveled and discolored with a white, pink, or light brown scaly appearance as a result of mycelia growing from the pericarp.

The species of Fusarium most commonly associated with Fusarium head blight of wheat in Europe are Fusarium graminearum (and its widespread teleomorph Gibberella zeae), Fusarium culmorum, Fusarium avenaceum (teleomorph Gibberella avenacea), and Fusarium poae (Xu et al., 2005). Other, less-frequently isolated species are Fusarium ce-realis (syn. Fusarium crookwellense), Fusarium equiseti (teleomorph Gibberella intricans), Fusarium sporotrichioides and Fusarium tricinctum, with other species of the genus found on an irregular basis (Bottalico, 1998). An important etiological characteristic of Fusarium head blight in Europe is the co-occurrence or the quick succession of several Fusarium species often referred to as a "species complex." Many different Fusarium species can be recovered from grain harvest in a limited geographic area. However, only a small number of species are regarded as pathogenic and these species usually co-exist with other less pathogenic or opportunistic Fusarium species that also can produce considerable amounts of my-cotoxins. Therefore, the mycotoxin content of a contaminated crop is due not only to the common pathogenic Fusarium species, but also to other opportunistic species in the species complex. The distribution and predominance of Fusarium head blight pathogens and related toxins also are influenced by agronomic and genetic factors. Climate, particularly temperature and moisture, are important, so the species composition of the Fusarium head blight species complex may vary significantly across Europe (Xu et al., 2005), with the fungal species present and the climate not necessarily independent variables.

Geographic distribution of Fusarium species

Of the four Fusarium species most commonly associated with Fusarium Head Blight of wheat in Europe, F. graminearum is the most common in continental and moist-warm climates, e.g., Central, Eastern and Southern Europe, although it also occurs frequently in maritime and cooler northwestern areas, where F. culmorum and F. avenaceum are more commonly found. Strains of F. graminearum and F. culmorum have been classified into two toxigenic types based on the trichothecene toxin they produce - either deoxynivalenol or nivalenol. The nivalenol chemotype may be more common amongst F. graminearum strains associated with maize (Miller et al., 1991). The deoxynivalenol and nivalenol che-motypes of F. graminearum are not evenly distributed worldwide, and the ecological differences in chemotype distribution may be important in determining specific regional grain contamination risks. The chemotypes of F. culmorum also differ in aggressiveness in plant pathogenicity assays (Bottalico and Perrone, 2002).

In the coolest areas of Europe, i.e., the Scandinavian regions, F. avenaceum, F. poae and F. langsethiae are the most common species, and all have interesting and important taxonomic problems. Within section Sporotrichiella, Fusarium langsethiae, formerly termed "powdery F. poae," recently was elevated to species status to distinguish it from F. poae sensu stricto. Fusarium langsethiae synthesizes T-2 toxin and its deacetylated derivative, HT-2 toxin, in Norwegian cereals (Torp and Nirenberg, 2004). Although this species is morphologically similar to F. poae, its mycotoxin profile is similar to that of F. sporotri-chioides. In Europe, this species usually occurs in Scandinavia, where the climatic conditions commonly are cooler and wetter. The acceptability of F. avenaceum as a homogeneous species is a matter of debate. Leslie and Summerell (2006) include all strains of both F. avenaceum and F. arthrosporioides in F. avenaceum. Yli-Mattila et al. (2004) distinguished F. avenaceum from F. arthrosporioides, but the morphological and molecular similarities of the two species make it very difficult to correctly distinguish these species. Another argument for the taxonomical distinctness of F. arthrosporioides is that the strains assigned to this species can produce much higher levels of enniatins under both natural and in vitro conditions than do strains assigned to F. avenaceum (Jestoi et al., 2004; Uhlig et al., 2006).

Southern Europe. The species profile of strains causing Fusarium Head Blight in southern regions of Europe varies annually depending on environmental conditions. In general, Fu-sarium Head Blight incidence is low and in the most southern regions of Italy and Spain, the disease is absent. In northern portions of Italy, Spain, Portugal, and in the south of France, F. graminearum and F. poae are the dominant species. There are reports of F. ave-naceum and F. culmorum being present and associated with diseased plants in Southern Europe, but such reports are not common and often are not well-substantiated suggesting that these two species are less common and are problematic only if the weather conditions are right (Bottalico and Perrone, 2002; Xu et al., 2005).

Central-Eastern Europe. Fusarium graminearum is the most common species, but F. avenaceum, occurs at significant frequency in more central regions, e.g., Austria and Switzerland (Bottalico and Perrone, 2002). In eastern countries, e.g., Hungary, F. graminearum usually is the dominant species although F. poae may occur in warmer, dryer seasons (Bottalico and Perrone, 2002; Xu et al, 2005).

Maritime areas of Northern and Western Europe. In the cooler maritime areas of Northwestern Europe, including the Netherlands, Belgium, England, Scotland and northwestern areas of France, the four Fusarium species commonly associated with Fusarium head blight, F. culmorum, F. graminearum, F. avenaceum and F. poae, all occur at significant levels. However, more recent surveys describe an increasing frequency of F. culmorum and a greater importance of F. poae and F. avenaceum, especially in years less conducive to F. graminearum infection (Waalwijk et al., 2003; Xu et al., 2005).

Northern and Eastern Europe. In Poland, surveys of Fusarium head blight conducted in the late 1990s and covering various climatic areas, found that F. poae dominated, with F. spo-rotrichioides reemerging in importance. In Russia, Fusarium head blight of wheat is very widespread and losses can reach 25-50%. In the northwestern and in central regions (Moscow area) of Russia, the most frequently isolated species were F. culmorum, F. avenaceum, F. tricinctum, F. poae, and F. sporotrichioides, with F. graminearum almost completely absent. In the warm, humid areas of the Southeastern European part of Russia, Belorussia and the Ukraine, F. graminearum dominates (Bottalico and Perrone, 2002). Strains of F. poae isolated from the coolest areas of Russia, where the environment is similar to that in Scandinavia, need to be evaluated to see if they are F. langsethiae.

Scandinavia. This geographic area has the coolest conditions in Europe. The Fusarium species most frequently encountered in surveys of wheat in these countries is F. avena-ceum/F. arthrosporioides, together with species from section Sporotrichiella, e.g., F. poae, F. langsethiae, F. tricinctum and F. sporotrichioides. Fusarium culmorum occurs when drier and colder weather that is less conducive to F. avenaceum occurs (Logrieco et al,. 2002a; Jestoi et al., 2004; Uhlig et al., 2006).

Mycotoxins

Deoxynivalenol, other trichothecenes and zearalenone are endemic contaminants of wheat in Europe, while moniliformin and hexadepsipeptides are emerging mycotoxins that can occur at high levels in cereals, particularly in cooler European regions.

Deoxynivalenol. The mycotoxins most frequently encountered in Fusarium head blight of wheat throughout Europe are the trichothecenes, and in particular deoxynivalenol. This toxin occurs across the continent. Its occurrence is correlated with environmental conditions, but this toxin has been found in wheat continent-wide. Schothorst and van Egmond (2004) found numerous samples positive for deoxynivalenol in all monitored European countries except Italy. However, some reports from Italy in 1998-2000 indicated that deoxynivalenol may be a common wheat contaminant there as well. In particular, deoxynivalenol contamination decreased from northern to central Italian regions, with very little, if any, deoxynivalenol detected in southern parts of the country where the disease is almost completely absent. Agronomic (crop rotation) and genetic (resistant genotypes) strategies that prevent the accumulation of this toxin in wheat kernels should be pursued simultaneously and combined with forecasting models to predict Fusarium head blight incidence and the potential for deoxynivalenol production (Xu, 2003).

Other trichothecenes. Nivalenol and fusarenon X, often co-occur with deoxynivalenol and are commonly reported from throughout Europe in ears of cereals affected by Fusarium head blight. Their presence has been attributed to the infection of wheat by strains of F. gra-minearum and F. culmorum with nivalenol chemotypes. Nivalenol and fusarenon X also may be produced by F. poae in Sweden and other northern countries, and by F. cerealis in Central and Northeastern Europe. Nivalenol in wheat samples from Poland usually is associated with F. poae, while in the United Kingdom, the highest levels of nivalenol are associated with F. poae and F. culmorum (Bottalico and Perrone, 2002; Tomczak et al., 2002). Schothorst and van Egmond (2004) reported that ~15% of 2200 samples of wheat from across Europe were positive for nivalenol and that most of these samples were from Scandinavian countries.

Epidemics of F. sporotrichioides and F. langsethiae in cold European locations may lead to contamination with T-2 toxin derivatives, such as T-2, HT-2 and T-2 triol. In Poland, scabby wheat grains contain T-2 and HT-2 toxins if the grain is infected with F. sporotrichioides (Bottalico and Perrone, 2002). Curiously, the highest levels of T-2 toxin have been reported from wheat collected in warmer countries such as Italy, France and Portugal (Schothorst and van Egmond, 2004).

Zearalenone. Zearalenone is produced primary by F. graminearum and F. culmorum and is a common co-contaminant with deoxynivalenol and its derivatives. Zearalenone is one of the most common mycotoxins associated with Fusarium head blight of wheat in Europe. Austrian pre-harvest hard wheat ears are infected primary by F. graminearum, but also with lower numbers of F. culmorum. Wheat from Slovakia with Fusarium head blight symptoms was infected primarily with F. graminearum, and wheat samples from Germany and the Netherlands all were contaminated with zearalenone (Bottalico, 1998).

Moniliformin. Severe infection by F. avenaceum, F. tricinctum, and to a lesser extent Fusarium subglutinans, in Central and Northeastern European countries, could result in the accumulation of moniliformin in scabby grain (Jestoi et al., 2004; Uhlig et al., 2004). In particular, in Poland, significant levels of moniliformin were found in scabby kernels obtained in 1998/1999 from ears of wheat heavily infected with F. avenaceum (Tomczak et al., 2002). Moniliformin also was reported in freshly harvested durum wheat in Austria. In all of these surveys, the moniliformin content of the kernels was correlated with the presence of F. avenaceum (Bottalico and Perrone, 2002).

An emerging problem - hexadepsipeptides. Enniatins and the chemically closely related beauvericins are cyclic hexadepsipeptides and selective cation ionophores. Beauvericin is cy-totoxic to mammalian cell tissues and causes apoptosis in both murine and human cell lines (Logrieco et al., 2002b). Beauvericin co-occurred with enniatins in Finnish samples of wheat kernels heavily contaminated with F. avenaceum, F. poae and F. tricinctum (Logrieco et al., 2002a; Jestoi et al., 2004). In addition, most wheat samples heavily colonized by F. avena-ceum/F. arthrosporioides, collected in two years (2001/2) in Norway also were contaminated with high levels of beauvericin and enniatins (Uhlig et al., 2006). Thus, the contamination of cereals with cyclic hexadepsipeptides is an important emerging toxicological problem.

In the same report (Uhlig et al., 2006) there was a significant correlation between the concentration of enniatins and moniliformin. This correlation is important from a toxicological point of view as it means that several different and potentially hazardous fungal metabolites may be present simultaneously in the same sample. Beauvericin and moniliformin are metabolites with toxic activities, but there are no data on the toxicological effects of enniatins on humans and animals. Thus, it is not possible to determine if the levels of enniatins found in the European surveys, are a safety concern for human and animal health. Further studies are needed to identify the possible toxic effects of enniatins, and, whether their co-occurrence with moniliformin, beauvericin and trichothecenes has a synergistic effect on human and animal toxicity.

Pénicillium and ochratoxin A

Fungal agents

Ochratoxin A is nephrotoxic, immunotoxic, teratogenic and has been classified by the International Agency for Research on Cancer (IARC) as a possible human carcinogen (group 2B) (IARC, 1993). The major fungal species producing ochratoxin A in wheat kernels are Aspergillus ochraceus and Penicillium verrucosum. These toxigenic species are considered to be opportunistic or saprophytic and may colonize cereals before harvest under favorable climatic conditions. Aspergillus ochraceus and P. verrucosum differ with respect to their ecological niches and their geographic distributions. Aspergillus ochraceus grows at warmer temperatures and at water activities (aw) as low as 0.80. It can affect wheat in warmer, subtropical and tropical parts of the world. Penicillium verrucosum grows well below 30°C and at aw > 0.80 and usually is found in wheat in cool temperate regions of Northern Europe and North America, although it may occasionally be found in Mediterranean regions.

Ochratoxin A: Natural occurrence on wheat

Ochratoxin A-producing molds grow and produce toxin when the moisture content of the grain is high at harvest and during subsequent drying and storage. Grain should be dried to < 18% moisture content as quickly as possible, with drying continued until the moisture content is < 14.5%. The only producer of ochratoxin A reliably recorded from cereals in Europe is P. verrucosum (Lund and Frisvad, 2003). The maximum tolerable limits adopted by European Union countries for raw cereal grain contamination with ochratoxin A is 5 ng/g. Ochratoxin A often occurs above this limit in wheat grown in Europe, with the biggest problems usually occurring in Northern European countries (Rizzo et al., 2002). Data from Croatia, Denmark, Germany, Italy, Norway, Poland, Spain, Sweden, Switzerland, the United Kingdom and Yugoslavia, confirm the differential geographic associated risks with ochratoxin A contamination (Puntaric et al., 2001; Rizzo et al., 2002; Lund and Frisvad, 2003).

Table 1. Fusarium mycotoxins occurring in cereals of European Countries (after SCOOP, 2003).

Toxin

Number of

Number of

% Positive

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