Microorganisms 2013, 1(1), 188-198; doi:10.3390/microorganisms1010188

Review
Temporal Variation of Mycotoxin Producing Fungi in Norwegian Cereals
Leif Sundheim 1,2,*, Guro Brodal 1, Inger S. Hofgaard 1 and Trond Rafoss 1,2
1
Norwegian Institute for Agricultural and Environmental Research, Fr. A. Dahlsvei 20, Ås 1430, Norway; E-Mails: guro.brodal@bioforsk.no (G.B.); ingerd.hofgaard@bioforsk.no (I.S.H.); trond.rafoss@bioforsk.no (T.R.)
2
Norwegian Scientific Committee for Food Safety, P.O. Box 4404, Nydalen, Oslo 0403, Norway
*
Author to whom correspondence should be addressed; E-Mail: leif.sundheim@bioforsk.no; Tel.: +47-9260-7476; Fax: +47-6494-6110.
Received: 1 October 2013; in revised form: 19 November 2013 / Accepted: 10 December 2013 /
Published: 17 December 2013

Abstract

: Spring barley is grown on about half of the Norwegian cereal area. The rest of the area is equally divided between wheat and oats. Most years the domestic production provides 70%–80% of the domestic market for bread wheat. Barley and oats are mainly grown for animal feed. During the years 2008–2012, severe epidemics of Fusarium head blight have led to increased mycotoxin contamination of cereals. During that period, precipitation was above normal during anthesis and grain maturation. The most important mycotoxin producers have been F. avenaceum, F. culmorum, F. graminearum and F. langsethiae. Increased deoxynivalenol contamination of Norwegian cereals during recent years is due to severe F. graminearum epidemics.
Keywords:
Fusarium; deoxynivalenol; nivalenol; precipitation

1. Introduction

In Norway and Finland, cereals are grown further north than anywhere else. About 85% of the cereal production is concentrated in the south-eastern counties, while the majority of the remainder is located in the Trøndelag counties in central Norway [1]. Most cereal growers practice monoculture on farms without domestic animals. Spring barley is grown on about half of the 300,000 ha of cereals, and the rest of the area is equally divided between growth of wheat and oats. During most of the last ten years, domestic production has provided 70%–80% of the domestic bread wheat consumption. Barley and oats are mainly used for animal feed with less than 5% of the production for human consumption. A risk assessment of mycotoxins in Norwegian cereals was published in 2013 [2]. We summarize data on mycotoxin producing fungi in Norway during the last century.

2. The Most Prevalent Fusarium spp. in Norwegian Cereals

An increased occurrence of mycotoxin-producing Fusarium spp. has been reported in Norway over the last decade. The cereal harvests during the years 2008–2012 gave particular reason for concern, as precipitation was higher than normal during the period from anthesis to harvest, which is favorable for epidemic development of Fusarium spp. [2].

Most reports list Fusarium avenaceum (Fr.) Sacc. as the most common Fusarium species in Norwegian cereals [3,4,5] (Table 1, Table 2, Table 3, Table 4 and Table 5). It is widely distributed in temperate regions and is most commonly soil-borne [6]. Fusarium avenaceum can be isolated from cereal seeds, cereal foot rot, and causes head blight. The teleomorph stage, Gibberella avenacea Cooke, has not been found in Norway. Langseth et al. [7] reported that Norwegian strains of F. avenaceum produce moniliformin and enniatin.

Table 1. Occurrence (%) of Fusarium spp. isolated from symptomatic cereal plants in Norway from 1980 to 1983, as determined by Haave [3].

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Table 1. Occurrence (%) of Fusarium spp. isolated from symptomatic cereal plants in Norway from 1980 to 1983, as determined by Haave [3].
Isolated SpeciesWheatBarleyOatsMean
F. avenaceum21.620.525.225.0
F. culmorum25.325.638.229.6
F. graminearum7.44.311.57.8
F. poae2.50.9-1.2
F. equiseti1.90.9-1.0
F. tricinctum0.60.8-0.5
Table 2. Occurrence (%) of Fusarium spp. isolated from seed samples at five experimental fields in Norway from 1994 to 1997, as determined by Henriksen [4].

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Table 2. Occurrence (%) of Fusarium spp. isolated from seed samples at five experimental fields in Norway from 1994 to 1997, as determined by Henriksen [4].
FieldKvithamarApelsvollBrandvalNorderåsHauerMean
CountyN-TrøndelagOpplandHedmarkAkershusAkershus
Isolated Species
F. avenaceum32.34.045.55.912.420.0
F. culmorum1.40.27.51.52.22.5
F. graminearum2.10.52.4001.0
F. poae5.46.34.013.010.77.9
F. tricinctum3.310.21.22.532.39.9
F. crookwellense3.00.055.50.60.21.9
Table 3. Occurrence (%) of Fusarium spp. isolated from wheat samples from four regions in Norway from 1994 to 1996, as determined by Kosiak et al. [5].

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Table 3. Occurrence (%) of Fusarium spp. isolated from wheat samples from four regions in Norway from 1994 to 1996, as determined by Kosiak et al. [5].
Isolated speciesSouth-EastUpper-EastMid-NorwaySouth-West
F. avenaceum97.6100.0100.0100.0
F. culmorum65.978.028.668.8
F. graminearum9.836.642.912.5
F. poae87.895.142.985.4
F. equiseti4.929.37.131.3
F. tricinctum70.765.950.077.1
F. sporotrichoides4.94.90.08.3
F. langsethiae76.570.656.670.0
Table 4. Occurrence (%) of Fusarium spp. isolated from barley samples from four regions in Norway from 1994 to 1996, as determined by Kosiak et al. [5].

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Table 4. Occurrence (%) of Fusarium spp. isolated from barley samples from four regions in Norway from 1994 to 1996, as determined by Kosiak et al. [5].
Isolated speciesSouth-EastUpper-EastMid-NorwaySouth-West
F. avenaceum100.0100.0100.097.4
F. culmorum77.869.254.982.1
F. graminearum20.426.931.014.1
F. poae94.483.343.791.0
F. equiseti14.934.64.234.6
F. tricinctum90.793.662.0100.0
F. sporotrichoides3.77.71.49.0
F. langsethiae71.484.062.573.3
Table 5. Occurrence (%) of Fusarium spp. isolated from oat samples from four regions in Norway from 1994 to 1996, as determined by Kosiak et al. [5].

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Table 5. Occurrence (%) of Fusarium spp. isolated from oat samples from four regions in Norway from 1994 to 1996, as determined by Kosiak et al. [5].
Isolated speciesSouth-EastUpper-EastMid-NorwaySouth-West
F. avenaceum98.198.8100.098.8
F. culmorum72.277.545.581.5
F. graminearum13.031.372.728.4
F. poae96.390.049.196.3
F. equiseti20.430.01.824.7
F. tricinctum83.390.065.588.9
F. sporotrichoides7.41.30.04.9
F. langsethiae95.596.330.088.5

The frequency of Fusarium crookwellense L.W. Burgess, P.E. Nelson and Toussoun is low in Norway [4] (Table 2). Fusarium crookwellense strains produce fusarin C [8], zearalenone (ZON) and nivalenol (NIV). In a review, Schollenberger et al. [9] list Fusarium crookwellense among the fungi producing type A trichothecenes in the diacetoxyscirpenol (DAS) group.

One of the most commonly isolated fungi from Norwegian cereals has been Fusarium culmorum (W.G. Sm.) Sacc. [3,4,5] (Table 1, Table 2, Table 3, Table 4 and Table 5). However, during the last ten years the frequency of this species has decreased [5]. In temperate regions, F. culmorum causes seedling blight, foot rot and head blight of cereals, and the fungus is common on cereal plant debris. Fusarium culmorum contains the tri5 and tri6 genes for trichothecene biosynthesis [10]. Schollenberger et al. [9] include F. culmorum among those fungi producing DAS. Langseth et al. [7] reported that Norwegian strains of F. culmorum produced nivalenol (NIV), deoxynivalenol (DON), the acetylated DON-derivative 3-acetyldeoxynivalenol (3-ADON) and ZON. Bakan et al. [11] divided F. culmorum into two chemotypes, the NIV chemotype and the DON chemotype; and the authors reported that these chemotypes are distributed independently of wheat variety and geographical origin. ZON production was significantly higher in the DON-producing strains of F. culmorum than in the NIV-producing strains. DON appears to play a role in the pathogenicity of F. culmorum [12]. In Denmark, Hestbjerg et al. [13] found correlation between DON content and aggressiveness. The frequency of Fusarium equiseti (Corda) Sacc. with the teleomorph stage Gibberella intricans Wollenw. is low to medium in Norwegian cereals [3,5] (Table 1, Table 2, Table 3, Table 4 and Table 5). Schollenberger et al. [9] included F. equiseti among fungi that produce DAS. Langseth et al. [7] reported that Norwegian strains of F. equiseti produced DAS, NIV, and ZON.

Fusarium graminearum Schwabe has a long history as a pathogen of cereals in Norway and it is common in barley, oats and wheat [3,4,5] (Table 1, Table 2, Table 3, Table 4 and Table 5). During the last ten years the prevalence of F. graminearum has increased in Norway [5]. However, Roll-Hansen [14] reported that the fungus has been a cereal pathogen in Norway for more than 70 years. In Germany, Oerke et al. [15] concluded that F. graminearum is the only Fusarium species in which airborne sexual spores contribute significantly to dissemination and development of epidemics in cereals. Schollenberger et al. [9] reported that F. graminearum produces type A trichothecenes in the DAS group. Norwegian strains of F. graminearum produce 3-ADON and ZON [7,16]. Fusarin C is also produced by F. graminearum isolates [8]. Ward et al. [17] described three chemotypes of F. graminearum: (i) NIV chemotype that produces NIV and its acetylated derivatives; (ii) 3-ADON chemotype that produces 3-ADON; and (iii) 15-ADON chemotype that produces 15-ADON. In Northern Europe, the 3-ADON genotype has been dominant, while in Southern and Central Europe the 15-ADON genotype is the most prevalent [18]. DON is a pathogenicity factor for F. graminearum causing necrosis in wheat leaves, which allows the fungus to spread into the rachis from florets [19]. Waalwijk et al. [20] employed multiplex PCR and found F. graminearum to be the most abundant species in Dutch wheat fields during the years 2000–2001. This contrasts with results from earlier studies in 1980s and 1990s, when F. culmorum was more common than F. graminearum in the Netherlands. The authors suggested that increased cultivation of maize in the Netherlands and warmer summers were the factors behind the change. Increases in the prevalence of F. graminearum have been reported from several European countries [21].

Torp and Nirenberg in 2004 described Fusarium strains, previously known as “powdery” F. poae, as F. langsethiae [22]. In recent studies the frequency of F. langsethiae in Norway has been found to be medium to high [5] (Table 3, Table 4 and Table 5). This species is a common Fusarium sp. in oats in Norway [5]. Phylogenetic analyses have confirmed that F. langsethiae is a distinct, new species, and that F. langsethiae is more closely related to F. sporotrichioides than to F. poae [23]. Imathiu et al. [24] reported that F. langsethiae could be isolated from symptomless oat and wheat grain, but the authors were unable to demonstrate any evidence of pathogenicity in inoculation experiments on wheat leaves. When different inoculation methods for F. langsethiae in oats were compared, Divon et al. [25] found that the fungus has a strong preference for panicle infection. Thrane et al. [26] concluded that F. langsethiae produced enniatin and the type A trichothecenes T-2, HT-2 and DAS. Aamot et al. [27] confirmed the production of T-2 and HT-2 in oats and detected up to 2040 μg/kg in Norwegian oats sampled during the years 2004-2009.

The frequency of Fusarium poae (Peck) Wollenw. is low to medium in cereal grains in Norway [3,4,5] (Table 1, Table 2, Table 3, Table 4 and Table 5). However, isolates of the morphologically similar species F. langsethiae were probably included in F. poae until F. langsethiae was described as a separate species [22]. Fusarium poae is most common in temperate regions, and cereal seeds and heads are commonly contaminated by this fungus. Liu and Sundheim [28] identified 13 vegetative compatibility groups (VCG) in 22 Norwegian and two Polish isolates of F. poae. The relatively large number of VCG groups indicates that sexual recombination occurs infrequently in this species. Liu et al. [29] found that 20 of the 24 F. poae isolates from Norway and Poland produced DAS, and half of the isolates produced NIV. None of the isolates produced T-2 or HT-2 toxins. Langseth et al. [7] reported that of five Norwegian F. poae strains, one produced NIV and DAS and four strains produced ZON.

In Norway the frequency of Fusarium sporotrichioides Sherb. is low [3,4,5] (Table 3, Table 4 and Table 5). Fusarium sporotrichioides is widely distributed on cereals, grasses and alfalfa in temperate regions [30]. Phylogenetic analyses have confirmed that F. sporotrichioides and F. langsethiae are sister taxa [23]. Strains of F. sporotrichioides produce HT-2, T-2, DAS, fusarin C and enniatin [8,26]. Three Norwegian strains of F. sporotrichioides all produced T2, HT-2, DAS and ZON [7].

The frequency of Fusarium tricinctum (Corda) Sacc. is low to medium in Norway [3,4,5] (Table 1, Table 2, Table 3, Table 4 and Table 5) . Golinski et al. [31] concluded that the fungus is most common in temperate regions, and that F. tricinctum usually occurs as a saprophyte or a weak parasite. Langseth et al. [7] found that two of three Norwegian strains of F. tricinctum produced moniliformin, and all three produced traces of enniatin. Fusarium tricinctum is also known to produce fusarin C [6].

3. Temporal Variation of Fusarium Species

Over the years the importance of Fusarium species in Norwegian cereal crops has increased [2]. Drivers for these changes may have been the development of specialized cereal production regions and changes in weather conditions. During the last fifty years there have been dramatic changes in the cropping practices in the cereal producing areas of Norway [1]. Until 1960, most farms had domestic animals and produced cereals in rotation with pasture, potato or vegetables. Since then the Government Agricultural Policy (Oslo, Norway) has led to specialized cereal production in south-east and Central Norway. Severe epidemics caused by virulent, mycotoxigenic F. graminearum strains have occurred in both North America and Europe during the last 20 years [32,33,34]. Following the recent description of F. langsethiae, several authors have reported high levels of its mycotoxins T-2 and HT-2, especially in oats [24,26].

Fusarium species were recognized as cereal pathogens for many years before their production of mycotoxins was discovered. In Norway, research on diseases caused by members of this genus started more than seventy years ago [35]. During the last twenty years, greater awareness of the potential health problems caused by mycotoxins in humans and domestic animals has led to an almost exponential growth in research on mycotoxins and mycotoxin-producing fungi [2]. Roll-Hansen [14] in 1939, identified F. graminearum as the causal agent of a serious foot rot and head blight epidemic of oats in south-east Norway. In a report on diseases of field crops, Jørstad in 1945 [35] referred to F. avenaceum as the most common Fusarium spp. on cereals, and he diagnosed foot rot and head blight caused by F. graminearum in herbarium material of oats collected in 1911. The teleomorph stage, Gibberella zeae (Schwein.) Petch, was identified on barley and wheat obtained from Ullensaker, Akershus county (Norway) in 1941, and on wheat from Øyestad, Aust-Agder county (Norway) in 1939 [35]. Jørstad concluded that F. avenaceum, F. culmorum, F. graminearum, and F. sporotrichioides were the most common Fusarium species on Norwegian cereals [35].

Haave isolated Fusarium spp. from 416 plant samples of barley, oats and wheat during the years 1980–1983 [3] (Table 1). Symptoms of the plants included discoloration of the lower straw internodes, mycelium growth within the straw, whitehead or shriveled grain and occasionally pink spore layers in the culm. The most common Fusarium spp. were F. culmorum, followed by F. avenaceum and F. graminearum. During the dry summer of 1983, F. culmorum was isolated from 41% of the plant samples, while F. avenaceum was obtained from 22% of the samples. F. culmorum and F. avenaceum were more common on oats than on barley and wheat. Isolations from kernels during 1982–1983 yielded 19.2% F. poae, 5.8% F. avenaceum, 5.3% F. culmorum, and 2.3% F. graminearum.

Abbas et al. [36] isolated Fusarium spp. from soil samples collected in Finnmark county, Troms county and the cereal growing counties in central and south eastern Norway during 1985–1986. Fusarium acuminatum Ellis and Evereh. was most common in the north, while F. avenaceum was more uniformly distributed. Abbas et al. [37] determined mycotoxin production in the isolates and found that most of them did not produce trichothecenes. One F. culmorum isolate produced zearalenone. All but one of the F. avenaceum isolates produced fusarin C. Moniliformin was produced by most of the F. acuminatum isolates and half of the F. avenaceum isolates.

In a comparison of different tillage systems, Henriksen [4] isolated Fusarium spp. from cereal kernels harvested in field trials at five locations during the years 1994–1997 (Table 2). At Kvithamar Research Centre in Nord-Trøndelag county (Norway), F. avenaceum was found to be the dominant species in all four years. F. poae was the second most common species during 1997, while F. graminearum and F. crookwellense were the second most common species during 1995. At Apelsvoll Research Centre in Oppland county (Norway), F. tricinctum, F. avenaceum and F. poae were identified as the most common species. F. avenaceum was found to be the dominant Fusarium species at Brandval, Hedmark county (Norway). At Norderås, Akershus county (Norway), the Research Farm of the Norwegian University of Life Sciences F. poae and F. avenaceum were determined to be the most prevalent Fusarium species in the field during two of the four experimental years. At the Hauer farm, Frogn, Akershus county (Norway), F. tricinctum was identified as the dominant Fusarium spp. during two of the four years of field experiments [4].

Langseth and Rundberget [38] considered F. avenaceum, F. culmorum, F. equiseti, F. graminearum, F. poae, F. sporotrichioides, F. torulosum (Berk. and M.A. Curtis) Nirenberg and F. tricinctum to be the most common Fusarium species in Norwegian cereals, and mycotoxin production and cytotoxicity were determined in 34 isolates of these eight species.

In a post-harvest survey of wheat, barley and oat kernels from the major cereal-growing regions of Norway during 1994–1996, Kosiak et al. [5] identified F. avenaceum, F. poae, F. tricinctum and F. culmorum as the most common field fungi in all four regions where samples were taken (Table 3, Table 4 and Table 5). F. graminearum, F. equiseti, F. sporotrichioides and “powdery F. poae”, which was later described as F. langsethiae, were also common in all regions. Table 5 shows the occurrence of Fusarium spp. in oat samples from four regions. Kosiak et al. [5] provided data on the prevalence of Fusarium in barley and wheat (Table 3 and Table 4). The relatively high occurrence of F. graminearum in Central Norway was unexpected, since the temperature during most of the growing season is lower than in the cereal districts of south-east Norway. Samples from south-east Norway had a significantly lower total Fusarium prevalence than samples from the other regions. Wheat had lower Fusarium levels than barley and oats.

Henriksen and Elen [39] reported on Fusarium infections in wheat, barley and oat grain from field trials during 1996–1998. Fusarium avenaceum and F. tricinctum were the most common of the Fusarium spp. isolated. In oats, F. tricinctum was the dominant species during both the experimental years. In barley and wheat field experiments, F. avenaceum was the dominant species, while F. culmorum, F. graminearum and F. tricinctum were less frequently isolated from the harvested grain.

Halstensen et al. [40] used a PCR assay to identify Fusarium spp. in settled grain dust. The dominant species was F. avenaceum, which was identified in 94% of the grain dust samples from wheat, oats and barley harvested in 11 of the most important cereal-producing municipalities in Norway during 1999 and 2000. Fusarium poae, F. langsethiae and F. culmorum were also frequently detected in the grain dust samples. Less than 10% of the samples contained F. graminearum or F. sporotrichioides.

Based on the microbiological and chemical analyses of cereals grown in Norway, Uhlig et al. [41] identified F. avenaceum as the dominant species. They determined concentrations of up to 5.8 ppm enniatins in Norwegian grain harvested during the years 2000, 2001 and 2002, and concluded that conditions in Norway do not favor the production of moniliformin by F. avenaceum. Uhlig et al. [41] detected only low levels of moniliformin in Norwegian grain.

In parallel samples collected at organic and conventional farms during the years 2002–2004, Bernhoft et al. [42] identified Fusarium spp. from cereal grains. The mean percentages of kernels infected with the most common species, F. avenaceum, were 58% in organically grown barley and 56% in conventionally grown barley; in oats, the corresponding figures were 44% and 43%, and in wheat the percentages were 50% and 54%, respectively. The mean percentages of infected kernels of F. graminearum were 8% in organically grown barley and 10% in conventionally grown barley; in oats, the corresponding figures were 11% and 19%, and in wheat the percentages were 7% and 10%, respectively. Fusarium poae in oats was at mean proportions of 18% and 13%, respectively, while in barley and wheat this species was less common. The mean percentages of F. culmorum, F. equiseti, F. langsethiae, F. sporotrichioides and F. tricinctum were less than 10% in samples of barley, oats and wheat from the nine counties sampled.

Increased prevalence of F. graminearum and F. langsethiae has been reported from several north European countries. In Denmark, Nielsen et al. [34] used quantitative real-time PCR to identify Fusarium spp. During 2003–2007 DON was the dominant mycotoxin in wheat and F. avenaceum, F. graminearum and F. culmorum were the most prevalent species. In barley F. poae, F. culmorum, F. langsethiae and F. graminearum were most common. Fusarium avenaceum, F. poae, F. langsethiae and F. graminearum were the dominant species in oats. When Nielsen et al. [34] analyzed wheat and barley samples from 1957 to 1996 they found only low levels of F. graminearum, while F. culmorum was the dominant species. Yli-Mattila et al. [43] determined Fusarium DNA levels and mycotoxins in grain samples from Finland and Estonia. The correlation between F. graminearum DNA and DON levels was highly significant in both countries, while there was no correlation between F. culmorum DNA and DON levels. Yli-Mattila et al. [43] found no correlation between combined T-2 and HT-2 and combined F. langsethiae/F. sporotrichoides DNA levels. In the United Kingdom Opuko et al. [44] determined DNA of F. langsethiae and its mycotoxins in commercial cereal production. In oats F. langsethiae was the dominant Fusarium species, and high levels of its mycotoxins HT-2 and T-2 were detected in the harvested grains. DNA of F. langsethiae was not detected in roots or seedlings. Symptomless heads of oats, barley and wheat had high levels of HT-2 and T-2.

4. Conclusions

Mycotoxin producing fungi is a major problem in Norwegian cereal production. Fusarium species infect the cereal heads from anthesis to harvest. During the last decade this period has been wetter than normal, and severe Fusarium epidemics have developed in the cereal growing regions of the country. Fusarium avenaceum is still the most prevalent species, but the mycotoxins produced by F. avenaceum have low toxicity for humans and domestic animals. Fusarium graminearum has become the dominant DON producing species in Norwegian cereals, while F. culmorum has decreased in importance.

Conflicts of Interest

The authors declare no conflict of interest.

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