ARTICLE IN PRESS Microbiological Research 160 (2005) 353—359
Contamination of malt barley and wheat by Fusarium graminearum and Fusarium culmorum from the crop years 2001–2003 in eastern Croatia ´a, Tomislav Klapeca,, Natalija Velic ´a, Zlata Milakovic ´b Vinko Krstanovic a
Faculty of Food Technology, pp 709, HR-31107 Osijek, Croatia Faculty of Agriculture, pp 719, HR-31107 Osijek, Croatia
Accepted 28 February 2005
KEYWORDS Malt barley; Wheat; Fusarium graminearum; Fusarium culmorum; Eastern Croatia
Summary This study investigated infection levels with Fusarium graminearum and Fusarium culmorum in malt barley and wheat in eastern Croatia. The contamination was surveyed over three consecutive crop years (2001–2003) on five locations for barley and three wheat cultivating locations. F. graminearum loads reached levels of potentially serious threat for the commercial production of malting raw materials in both cereals (up to 29.1%). On the other hand, the mean percentage of kernels infected with F. culmorum was low to medium (up to 6.1%). The fungal invasions for years and locations were affected by meteorologic and other environmental factors and the pattern seemed to be consistent with species-specific optimal conditions reported by other authors. & 2005 Elsevier GmbH. All rights reserved.
Introduction Fusarium head blight or scab is a disease causing considerable yield and quality losses in cereals. More intense Fusarium infections of barley can render it technologically nonuseable for malt production (Schwarz et al., 1997). The major negative effect of contamination of malt barley with these molds is reduced test weight of infected grains, which implies less endosperm, i.e. a
decreased starch:protein ratio, resulting in reduced malting yields (Sloey and Prentice, 1962; Duijnhouwer et al., 1993). Infection has also been reported to cause an increased enzymatic degradation of cell matter (primarily proteolysis and amylolysis) caused by fungal enzymes, in addition to a very probable increased endogenous enzymatic activity induced by fungal gibberellins (Schwarz et al., 2001). Germinative capacity of Fusariuminfected barley can be seriously compromised as
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(T. Klapec). 0944-5013/$ - see front matter & 2005 Elsevier GmbH. All rights reserved. doi:10.1016/j.micres.2005.02.009
ARTICLE IN PRESS 354
Materials and methods Wheat and barley samples Samples of barley from variety trials (15 different varieties) at five representative locations in eastern Croatia: Nova Gradisˇka (NG), Pozˇega (PZ), ˇupanja (ZU), were Osijek (OS), Baranja (BA), and Z taken over three consecutive seasons (2001–2003). Accordingly, samples of 10 wheat cultivars were collected at three of the locations listed above: NG, PZ, and OS. Sampling (5 kg per sample) was performed on cleaned and processed wheat and barley grains and the samples were kept refrigerated in sterile dry containers till analysis. Environmental conditions Meteorological data (temperature and precipitation) for locations were obtained from weather stations and due to minimum differences the mean values are given in Fig. 1. Soil types at locations were: alluvial soil (NG), acidic pseudogley (PZ), pseudogley (ZU), and eutric cambisol (OS, BA). Fusarium contamination Following homogenization, 2 100 grains were taken from each sample. Superficial disinfection of grains was carried out by a bath for 10 min in a 1% NaOCl solution followed by rinsing twice with sterile water. Determination of contamination with F. graminearum and F. culmorum was performed according to Mitteleuropa ¨ische brautechnische Analysenkommission (MEBAK) (1997). Grains were plated on Petri dishes (4 25). The composition of the culture medium for F. graminearum was: 2 g/l D()-mannitol, 20 g/l technical agar in distilled water. Following sterilization at 120 1C for 15 min
120 rainfall (mm)
well (Haikara, 1983), which besides being a serious problem for seed producers, is also a drawback in malt production since it further decreases total quantity of malt extract and can effect poor runoffs. Malting provides favorable conditions (high humidity, low temperature, germinating seed) for fungal growth and the main adverse impacts of Fusarium head blight on malt and wort quality include: a significantly higher content of nitrogen species resulting from protein degradation, discoloration, changes in wort viscosity, etc. (Sloey and Prentice, 1962; Schwarz et al., 2001). Fusarium molds also synthesize unidentified compounds called hydrophobins which cause beer gushing (Kleemola et al., 2001). Moreover, detrimental effects of Fusarium infection on brewing performance and beer flavor have also been noted (Sloey and Prentice, 1962; Anderson et al., 1967; Haikara, 1983). Fusarium growth often implies production of mycotoxins (e.g. trichothecenes, zearalenone, fumonisins, moniliformin, etc.) which pose a threat to human or animal health (Hussein and Brasel, 2001; Logrieco et al., 2003), and have also been found to affect enzymatic processes in infected grains (Nummi et al., 1975; Schapira et al., 1989). Trichothecenes (primarily deoxynivalenol i.e. DON) seem to be especially problematic in beer production (Schwarz et al., 1995; Scott, 1996). Fusarium epidemics can also result in significant economic losses to producers due to yield losses, lower prices and mycotoxin contamination (Schaafsma, 2002; Mesterha ´zy et al., 2003). Very similar negative effects of Fusarium infection in barley are also highly likely in wheat used for malting. Infected wheat has a significantly worsened gluten quality and if intended for baking industry, it would have a pronounced negative impact on viscoelastic and processing properties of dough (Nightingale et al., 1999). This paper investigated initial infection levels with Fusarium graminearum and Fusarium culmorum in malt barley and wheat grown in eastern Croatia. These two species were chosen based on two factors: the frequency of isolated species from the grains in the area and the fact of these Fusarium species being the most damaging to the malt production (Mesterha ´zy, 1984; Jurkovic ´ and ´ osic´, 1997; Miedaner et al., 1997; Sacher, 1997; C Jurkovic ´ et al., 1998; Logrieco et al., 2003). The area is the greatest producer of the raw materials in the country, and the reasearch will provide insight into anticipated levels of Fusarium infection in the raw materials used for malt (primarily used in beer manufacture), as well as for wheat flour production.
V. Krstanovic´ et al.
rainfall 2001 rainfall 2002
Figure 1. Mean temperature and rainfall during crop years 2001–2003 in eastern Croatia.
ARTICLE IN PRESS Contamination of malt barley and wheat by Fusarium graminearum and cooling to 55 1C, chlortetracycline hydrochloride (0.030 g/l), streptomycin sulfate (0.030 g/l), and 99% pentachloronitrobenzene (1 g/l) were added. The preparation of the culture medium for F. culmorum was identical except that pentachloronitrobenzene was replaced by 0.0156 g/l malachite green. The determination of F. graminearum was performed as follows: After inoculation on Petri dishes the grains were left at room temperature for 24–36 h, and then kept at 18 1C for 6 h to prevent germination (Neergaard, 1977). Contamination levels were estimated on the basis of number of grains developing a cherry-colored pigment. Estimation of F. culmorum contamination was based on the number of grains covered with a characteristic white cotton-like mycelium during the first 48 h of cultivation. Additional confirmation of species and photodocumentation was performed by observation of shape and size of macroconidia using a digital camera microscope (Olympus COVER 018, C4040 Zoom), after suspicious colonies were transferred to sporulation medium (CLA agar for F. graminearum and water agar for F. culmorum) as suggested by Nelson et al. (1983) and Burgess et al. (1988). Sample means (% infected grains) were calculated from two replicas.
Table 1. Mean contamination level (% of infected grains) with Fusarium graminearum of malt barley (n ¼ 15) from eastern Croatia in three consecutive crop years Year
2001 2002 2003 Mean
12.9b 26.5b,d 17.7b 19.0b
4.4 6.6c 7.0c 6.0c
4.9 2.2 2.1 3.0
2.2 2.1 2.0 2.1
2.2 2.3 1.3 1.9
5.3 7.9 6.0 6.4
NG—Nova Gradisˇka, PZ—Pozˇega, OS—Osijek, BA—Baranja, ZU— ˇupanja. Z b Significantly higher (po0:05) than other locations. c Significantly higher (po0:05) than OS, BA and ZU locations. d Significantly higher (po0:05) than other seasons.
Table 2. Mean contamination level (% of infected grains) with Fusarium graminearum of wheat (n ¼ 10) from eastern Croatia in three consecutive crop years Locationa
2001 2002 2003 Mean
15.3 29.1b,d 21.4b 21.9b
6.7 3.8 4.8c 5.1
8.9 12.6 9.0 10.2
4.9 4.9e 0.8 3.5
NG—Nova Gradisˇka, PZ—Pozˇega, OS—Osijek. Significantly higher (po0:05) than other locations. c Significantly higher (po0:05) than OS location. d Significantly higher (po0:05) than season 2001. e Significantly higher (po0:05) than season 2003. b
Normal distribution of data was improved by arcsine transformation prior to ANOVA and LSD test of means, as well as Spearman rank correlations of data. All calculations were performed with the computer programs Excel 2000 (Microsoft Corp.) and Statistica 6.0 (StatSoft Inc.).
Results and discussion The results for mean contamination levels of malt barley and wheat with F. graminearum and F. culmorum are given in Tables 1–4. A higher prevalence of F. graminearum infection over the three seasons is obvious on all but one (OS) of the surveyed locations. These findings are in agreement with observations of F. culmorum occurrence being more characteristic for NorthEuropean countries (Bottalico, 1998; Kosiak et al., 2003). The mean F. graminearum infection levels of 6.4% for barley and 10.2% for wheat were within the range previously determined in Croatia and surrounding countries (Mesterha ´zy, 1984; Tomasovic ´ and Koric´, 1991; ´ osic´, 1997; Bottalico, 1998; Jurkovic´ Jurkovic ´ and C et al., 1998). Similar values have been determined
Table 3. Mean contamination level (% of infected grains) with Fusarium culmorum of malt barley (n ¼ 15) from eastern Croatia in three consecutive crop years Year
2001 2002 2003 Mean
6.1b,c 2.2b,d 1.0 3.1
5.6b,c 2.4b,d 0.7 2.9
6.0b,c 3.1b,d 0.2 3.1
2.1c 1.2d 0.2 1.2
2.2c 1.2d 0.4 1.3
4.4c 2.0d 0.5 2.3
NG—Nova Gradisˇka, PZ—Pozˇega, OS—Osijek, BA—Baranja, ZU— ˇupanja. Z b Significantly higher (po0:05) than BA and ZU locations. c Significantly higher (po0:05) than other seasons. d Significantly higher (po0:05) than season 2003.
in Norway (Kosiak et al., 2003), much lower in the Rhineland, Germany on wheat (Birzele et al., 2002), while there are reports of both, similar and much lower prevalence of F. graminearum in
ARTICLE IN PRESS 356
V. Krstanovic´ et al.
Table 4. Mean contamination level (% of infected grains) with Fusarium culmorum of wheat (n ¼ 10) from eastern Croatia in three consecutive crop years Year
2001 2002 2003 Mean
2.4b 2.3 1.7c 2.1b
1.4 1.7d 0.6 1.2
0.7d 1.5d 0.1 0.8
1.5 1.8 0.8 1.4
NG—Nova Gradisˇka, PZ—Pozˇega, OS—Osijek. Significantly higher (po0:05) than OS location. c Significantly higher (po0:05) than other locations. d Significantly higher (po0:05) than season 2003. b
Finland (Hietaniemi and Kumpulainen, 1991; Eskola et al., 2001). Percentages above 10% are considered high infection levels (Lori et al., 2003). On the other hand, the mean F. culmorum invasion was low, i.e. below 1.5%, in wheat (Table 4), and medium, 1.5–10%, in malt barley (Table 3). On average, results on F. culmorum contamination of cereals from Finland, Norway, Denmark and The Netherlands reveal higher infection levels, although considerable deviations between locations and growing years have also been noted (Hietaniemi and Kumpulainen, 1991; Andersen et al., 1996; DeNijs et al., 1996; Eskola et al., 2001; Kosiak et al., 2003). These probably reflect differences in methodology, unless they were reported in the same paper, and growing conditions. Results from Germany depend on localities; both comparable and higher F. culmorum infection rates were found (Nirenberg et al., 1994; Birzele et al., 2002). Due to the harmful impact of Fusarium infection and disease of barley and wheat (yield loss, mycotoxin contamination of raw materials used in the production of malt and feed, etc.), the Canadian province of Alberta developed a management plan aimed at reducing the risk of F. graminearum spread in Alberta (Alberta Agriculture, Food and Rural Development, 2002). The current advisory level for DON in the US is 1 ppm for grain products (Doyle, 1997). Malting companies reject lots suspected of containing detectable levels of DON. On the basis of estimates of relationship between scabby grain and concentration of DON (one grain ¼ 4 ppb) (Sacher, 1997), the mean infection levels by both investigated species, and especially F. graminearum, reported here, represent a potential threat to commercial production of malt and beer in Croatia. Fungal invasion of wheat on
surveyed locations (NG, PZ, OS) showed a pattern similar to barley (F. graminearum), or the location means were higher for barley (F. culmorum) (Tables 1–4). The results are somewhat surprising considering the claims of greater vulnerability of wheat to Fusarium infection (Narziß, 1999). At least partial explanation is offered by the fact that wheat was dehusked prior to analysis as opposed to malt barley, reflecting the usual practices in the production of malt (from either barley or wheat) and wheat flour (Clear et al., 1997). In addition to that, as opposed to wheat, infected barley kernels are not so easily removed in the combining process. Although statistically significant (po0:05), the association between invasion levels of F. graminearum and F. culmorum was not strong in either barley (r ¼ 0:15) nor wheat (r ¼ 0:38). Although the correlation is usually negative, it has also been reported that F. graminearum levels above 10% are needed to suppress the growth of less pathogenic species like F. culmorum (Kosiak et al., 2003). The impact of location, crop year and cultivar properties on F. graminearum and F. culmorum contamination was also examined. The NG and PZ locations showed consistently higher mean F. graminearum infection in both cereals compared to the other locations (Tables 1 and 2). None of the mean F. graminearum contamination values for the other locations were below the marginal 1.5% level which denotes low fungal invasion. The mean F. graminearum infection levels for the three crop years do not reveal statistically significant differences, but there is a tendency of a higher mean for the year 2002 in both cereals (Tables 1 and 2). Only the mean F. culmorum infection levels in wheat on the NG location reached statistical significance, while the other location means were below the 1.5% margin (Table 4). There were no significant differences between F. culmorum contamination means for locations in barley, while only BA and ZU locations had infection levels below 1.5% (Table 3). The mean incidence of F. culmorum infection was highest in the crop year 2001 in barley, and the mean fungal infection in 2003 is the only one which can be considered low (Table 3). There were no significant differences between years in F. culmorum infection of wheat, and the highest mean for crop year 2002 barely exceeded the 1.5% level (Table 4). The results should be viewed in the light of factors which have a synergistic effect on Fusarium infection. Corn was a previous field crop at all locations and is known for leaving behind large amounts of cellulose and protein which support Fusarium growth (Teich, 1989; Beck et al., 1993). Fusarium infection is also appreciably influenced by
ARTICLE IN PRESS Contamination of malt barley and wheat by Fusarium graminearum environmental conditions, especially if temperature, rainfall and relative humidity are high during heading and flowering periods (Doohan et al., 2003; Xu, 2003). The crop year 2002 seemed to have provided the most favorable conditions for Fusarium invasion over the usual heading and flowering period in both barley (May 5–10) and wheat (May 5–15) (Fig. 1). Exposure to optimal temperature and moisture continued until harvest during the crop year 2002, which may have exacerbated infection (Hart et al., 1984). All F. graminearum infection levels in both cereals, grown at the NG location, are above the margin of 10% and can thus be considered high (Tables 1 and 2). The highest infection levels at this location were determined for the crop year 2002, which is in agreement with the observations drawn from comparing meteorological conditions. PZ is another location with significantly higher F. graminearum infection levels in barley (Table 1). However, all F. graminearum infection levels were in the medium range. Other locations had lower F. graminearum invasions, mostly around 2%, and the variations between crop years were not consistent with the pattern for the NG location. The crop year 2001 affected growth of F. culmorum in barley in a favorable manner (Table 3). The mean levels are the highest across years for all locations, but still in the medium range. This may be explained by somewhat lower temperatures during critical heading periods in the crop year, which have been reported to selectively stimulate growth of F. culmorum (Mills, 1989; Bottalico, 1998). The NG, PZ and OS locations had similarly high F. culmorum invasions in the year 2001, the levels were medium in 2002 and dropped below 1.5% in 2003. The last crop year was unusually dry and warm during the whole growing period of wheat and barley (Fig. 1), which coincides with significant reductions of F. culmorum infection in both cereals (Tables 3 and 4), as opposed to F. graminearum. Dry spring generally weakens plants making them more susceptible to infection (Sacher, 1997). The relatively high F. graminearum contamination levels in 2003, during which the meteorological conditions were not favorable for scab development, could be a combined effect of increased infection in the preceding year and the plant-weakening dry spring. Wheat grown at the NG location again had greatest invasions of F. culmorum at the lower part of the medium range, while the other two locations had low contamination levels of the fungi. Only two out of 15 barley varieties had mean F. graminearum infection levels significantly higher than the others. All varieties had higher F.
graminearum invasions on barley at the NG location, with minimal differences between crop years. Wheat varieties did not differ in resistance to F. graminearum infection independent of year or location, although the varieties always had higher infection levels when grown at the NG location compared to the other locations. All investigated barley varieties were more affected by F. culmorum invasion in crop year 2001, with three out of 15 having significantly higher F. culmorum loads. Wheat varieties did not differ in resistance to F. culmorum infection independent of year or location. There were no differences in tillage systems among locations, which, in instances of no tillage, have been shown to increase Fusarium infection rate (Teich, 1989). Therefore, it seems like soil type, fertility, pH-value, etc., could have been primary factors affecting the resistance of wheat and barley at different locations. Perhaps the more abundant water retention of alluvial soil at the NG location may have effected greater production of fungal conidia and ascospores, ultimately resulting in higher infection levels (Xu, 2003). Previous unpublished observations indicated dispensable differences in scab resistance among investigated varieties. There is also a possibility of drawing wrong conclusions about resistance of varieties due to heavily affected grains and heads being separated during harvest and cleaning of grain. Similarly to the present results, Sacher (1997) reported huge effect of ecological, including meteorological, factors on Fusarium infection of wheat. Although there are ambivalent reports on the connection between Fusarium infection and mycotoxin levels (Birzele et al., 2002), most authors found a positive correlation between these variables (Hart et al., 1984; Sacher, 1997; Lamper et al., 2000; Schwarz et al., 2001; Lori et al., 2003). Theoretical consideration of the determined grain contaminations (especially with F. graminearum) at some locations and favorable meteorological conditions (Fig. 1; Doohan et al., 2003), suggests the possibility of substantial levels of technologically and nutritionally relevant mycotoxins and hydrophobins. However, many known and hitherto unknown factors are capable of modifying this, and unexpected findings have been reported before (Eskola et al., 2001). This study surveyed the occurrence of two prominent Fusarium species in barley and wheat grown in eastern Croatia. The results indicate the possibility for a considerable proportion of wheat and barley essentially unsuitable for malt production. Routine controls of the raw materials for
ARTICLE IN PRESS 358 Fusarium infection levels as well as the levels of related metabolites in Croatia are necessary.
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