COBISS Code 1.02
DOI: 10.2478/acas-2013-0012
Agrovoc descriptors: fusarium, mycotoxins, cereals, cereal crops, damage, biological contamination, zea mays, triticum, hordeum, climatic factors, precipitation, temperature, humidity
Agris category code: H20
The impact of environmental factors on the infection of cereals with Fusarium species and mycotoxin production - a review
Sasho POPOVSKI1, Franci Aco CELAR2
Received Avgust 28, 2012; accepted November 13, 2012. Delo je prispelo 28. avgusta 2012, sprejeto 13. novembra 2012.
ABSTRACT
Several phytopathogenic Fusarium species occurring worldwide on cereals as causal agents of 'head blight' (scab) of small grain cereals and 'ear rot' of maize, are capable of accumulating, in infected kernels, several mycotoxins some of which of notable impact to human and animal health. Fusarium graminearum, F. culmorum, F. poae, F. avenaceum and Microdochium nivale predominantly cause Fusarium diseases of small-grain cereals. Maize is predominantly attacked by F. graminearum, F. moniliforme, F. proliferatum and F. subglutinans. The review is focused on the influence of climatic variables, particularly temperature, humidity and rainfall on growth, reproduction, survival, competitive ability, mycotoxicity and pathogenicity of Fusarium fungi commonly isolated from wheat, barley and maize.
Key words: Fusarium spp., mycotoxins, smal grain cereals, maize, climatic factors
IZVLEČEK
VPLIV OKOLJSKIH DEJAVNIKOV NA OKUŽBO ŽIT Z GLIVAMI FUSARIUM SPP. IN TVORBO MIKOTOKSINOV - PREGLEDNI ČLANEK
Številne fitopatogene glive rodu Fusarium, ki povzročajo plesnivost klasov žit in koruznih storžev, je sposobnih v okuženih zrnih akumulirati številne mikotoksine, med katerimi so nekateri škodljivi za zdravje ljudi in živali. Žita prvenstveno okužujejo vrste Fusarium graminearum, F. culmorum, F. poae, F. avenaceum in Microdochium nivale, medtem ko koruzo F. graminearum, F. moniliforme, F. proliferatum in F. subglutinans. V pregledu je poudarek na vplivu vremenskih dejavnikov (temperatura, vlaga in padavine) na rast, razmnoževanje, preživetje, tekmovalno sposobnost, mikotoksičnost in patogenost Fusarium vrst, običajno izoliranih iz pšenice, ječmena in koruze.
Ključne besede: Fusarium spp., mikotoksini, strna žita, koruza, klimatski dejavniki
1 INTRODUCTION
Fusarium is a common mould in cereal fields. The infestation (superficial contamination) and infection of Fusarium in cereals are of great concern worldwide - as plant pathogens and producers of mycotoxins.
The genus Fusarium comprises a diverse array of fungi, members of which are phytopathogenic to a wide range of plants under diverse environmental conditions. Phytopathogenic Fusarium fungi cause
several diseases of small-grain cereals, including seedling blight and foot rot, fusarium head blight (FHB) (also known as 'scab' or ear blight) and ear rot of maize (Parry et al., 1995). The Fusarium species Fusarium graminearum (teleomorph Gibberella zeae), F. culmorum, F. poae, F. avenaceum (teleomorph G. avenacea) and Microdochium nivale (formerly known as Fusarium nivale, teleomorph Monographella nivalis) are common pathogens of wheat and
1	PhD Student, Biotechnical Faculty, Department of Agronomy, Jamnikarjeva 101, SI-1111 Ljubljana, e-mail: sasopopovski87@hotmail.com
2	Ass. Prof. Dr., e-mail: franc.celar@bf.uni-lj.si, ibid., corresponding author
barley (Sutton, 1982; Parry et al., 1995; Miedaner, 1997; Tekauz et al., 2000; Brennan et al., 2003). Three Fusarium species are frequently isolated from infected maize: F. graminearum, F. moniliforme (syn. F. verticillioides, teleomorph G. fujikuroi mating population A) and F. subglutinans (teleomorph G. fujikuroi mating population E). Other species responsible for ear rot of maize include F. culmorum, F. proliferatum (teleomorph G. fujikuroi mating population D) and F. equiseti (Sutton, 1982; Leslie et al., 1986; Pomeranz et al., 1990; Odiemah and Manninger, 1994; Vigier et al., 1997; Velluti et al., 2000; Torres et al., 2001).
Fusarium diseases of wheat, barley and maize cause significant yield losses world-wide and are therefore of great economic importance (Sutton, 1982; Parry et al., 1995; Miedaner, 1997; Mesterhazy et al., 1999). In addition, many of these Fusarium species have the potential to produce a range of toxic secondary metabolites known as mycotoxins that cause a potential health risk when contaminated grain is consumed in human and animal food products (D'Mello and Macdonald, 1997; D'Mello et al., 1999; Placinta et al., 1999).
2 CLIMATIC DISTRIBU
Host and climatic factors influence the growth, survival, dissemination and hence the incidence of Fusarium fungi and the disease severity. The influence of host cultivars on the pathogenicity and toxicity of Fusarium fungi has been extensively reviewed (Miedaner, 1997; Miedaner et al., 2001; Mesterhazy et al., 1999; Magg et al., 2002).
The influence of climatic factors on Fusarium diseases is complicated by the fact that Fusarium fungi can cause disease individually or in complex infections (Doohan et al., 1998), and there are numerous reports on how species differentially respond to different environmental variations, particularly temperature and humidity.
Also, host susceptibility to fungal disease is directly influenced by temperature and osmotic stress. This review is focused on the influence of climatic variables, particularly temperature, humidity and rainfall, on grain infection, growth, reproduction, survival, competitive ability, mycotoxicity and pathogenicity of Fusarium fungi commonly isolated from wheat, barley and maize.
OF FUSARIUM SPP.
Several factors influence the occurrence of Fusarium in the soil and the infestation and infection it generates in cereal plants. Geographical factors including climate are of superior importance for the occurrence of Fusarium and for the pattern of infestation by various Fusarium species.
The incidence of the causal organisms of FHB of wheat, barley and ear rot of maize is often correlated to different climatic conditions (temperature and rainfall) in different geographic locations. F. culmorum, F. poae, F. avenaceum and M. nivale are common pathogens of wheat and barley in the cooler temperate regions of the world, while F. graminearum tends to be the predominant Fusarium species pathogenic to these cereals in hotter regions of the world (Parry et al., 1995; Brennan et al., 2003).
F. graminearum, F. moniliforme and F. subglutinans are the Fusarium species most
frequently isolated from infected maize, but depending on geographical location, other causal species of ear rot include F. culmorum, F. proliferatum and F. equiseti (Leslie et al., 1986; Vigier et al., 1997; Pomeranz et al., 1990; Odiemah and Manninger., 1994; Velluti et al., 2000; Torres et al., 2001).
Varying the temperature in a simple model ecosystem produces changes in the community structure of Fusarium species that mimic those found along climatic temperature and rainfall gradients (Saremi et al., 1999). The influence of climatic conditions on the incidence of Fusarium species is probably both direct (e.g. an effect on mode of reproduction) and indirect (e.g. an effect of soil and vegetation type).
More research is required to determine the indirect effect of climate on the incidence of Fusarium fungi and how this affects species-specific factors.
3 GERMINATION, GROWTH AND COMPETITION BETWEEN Fusarium spp.
Germination, growth and competition between Fusarium spp. are dependent upon the availability of nutrients and environmental factors such as temperature, pH, humidity, aeration and light. The influence of nutritional availability is outside the scope of this review. It is generally not a limiting factor during infection and colonisation of host tissue, but may be limiting or growth-inhibiting during saprophytic survival (e.g. humic acids in soil) (Moliszewska and Pisarek, 1996).
3.1	Germination
Germination is influenced by water availability (aw) and temperature: warm humid conditions favour this developmental stage. Marín et al. (1996) found that the aw minima for the microconidial germination of Spanish isolates of F. moniliforme and F. proliferatum were 0.88 on maize meal extract medium.
Microconidia of F. moniliforme germinated optimally at 25-37 oC and 0.96-0.98 aw, but at 30 oC when the aw was 0.90-0.94, with intraisolate variation. The germination of microconidia of F. proliferatum was optimal at 30 oC, regardless of aw, and with significant intra-isolate variation. However, Etcheverry et al. (2002) found that Argentinean isolates of F. moniliforme and F. proliferatum grew very slowly, if at all, at aw 0.93 and 25 oC. At marginal temperatures and aw levels, the germination lag time increases (Marín et al., 1996; Etcheverry et al., 2002). Earlier, Francis and Burgess (1977) found that the percentage germination of conidia, ascospores and chlamydospores of F. graminearum Group II isolates was reduced as water potential was lowered from -1 to -20 bars.
3.2	Growth
Temperature and aw differentially affect the growth of Fusarium species (Table 1, Figure 1). Fusarium species differed in their temperature requirements for optimal growth on potato
dextrose agar (Cook and Christen, 1976; Pettitt et al., 1996; Brennan et al., 2003). Irrespective of the European origin of isolates, in vitro culture experiments showed that optimal growth occurred at 25 oC for F. graminearum, at 20-25 oC for F. culmorum and F. poae and at 20 oC for F. avenaceum and M. nivale.
In general, F. culmorum had the fastest growth rate of all five species over the range 10-30 oC. Species accounted for 51-63% and country of origin accounted for 23-52% of growth rate variation. At the low temperature of 5 oC, Pettitt et al. (1996) found that of F. culmorum, F. avenaceum and M. nivale, the latter species was significantly the fastest growing. At the higher temperature of 35 oC, Cook and Christen (1976) found that F. graminearum did not grow, even after 30 days. Marin et al. (1998a) found that the maize pathogens F. moniliforme and F. proliferatum had a faster growth rate than Eurotium and Penicillium species and on sterile layers of maize grew best at 30 oC (Table 1).
The temperature optima for growth of Fusarium spp. appears to be dependent on aw. Cook and Christen (1976) found that the optimal growth temperature for European isolates of F. graminearum (24-28 oC) increased slightly when lower water potentials prevailed. Fusarium graminearum grew optimally at -10 to -20 bars and F. culmorum at -8 to -14 bars. Increasing aw (>0.925) favoured growth of F. moniliforme and F. proliferatum on sterile layers of maize at 30 oC (Marin et al., 1995). More research is required to better understand the influence of aw on the growth of F. culmorum, F. poae and M. nivale. It must be noted that drawing comparisons between growth rate studies is difficult, as the rates are very dependent on the growth substrates used. For example, on maize culture media F. subglutinans grew optimally at 20-25 oC, but faster on rice culture media at 15 oC (Castella et al., 1999).
Table 1: Optimum temperature and water potential/availability for the in vitro growth of Fusarium species. Preglednica 1: Optimalne temperature in vodni potencial/dostopnost za in vitro rast Fusarium vrst.
Species	Substrate3	Optimum growth conditions	References
Water
Temperature (C) potential/availabilityb
F. graminearumBM, PDA	24-	-28	-10 to -20 bars	Cook and Christen (1976),
				Brennan et al. (2003)
F. culmorum BM, CMA, PDA	20	25	-8 to -14 bars	Cook and Christen (1976),
				Parry et al. (1994), Brennan
				et al. (2003)
F. avenaceum PDA	20	25	ND	Parry et al. (1994), Brennan
				et al. (2003)
F. poae PDA	20	25	ND	Brennan et al. (2003)
M. nivale PDA	15	20	ND	Parry et al. (1994), Brennan
				et al. (2003)
F. moniliforme Sterile maize layers	30		aw > 0.925	Marin et al. (1995)
F. proliferatum Sterile maize layers	30		aw > 0.925	Marin et al. (1995)
F. subglutinans MCM, RCM	15	25	ND	Castella et al. (1999)
a BM = basal medium, PDA = potato dextrose agar, CMA = corn meal agar, MCM = maize culture media, RCM =
rice culture media. b ND = no data.
Figure 1: In vitro growth rate of F. poae (strain CC359B) at 10 (A), 15 (B), 20 (C), 25 (D) and 30 oC (E) (Brennan et al., 2003).
Slika 1: In vitro priraščanje glive F. poae (izolat CC359) pri 10 (A), 15 (B), 20 (C), 25 (D) in 30 oC (E) (Brennan et al., 2003).
3.3 Competition: Temperature and water
availability (aw)
Fusarium fungi do not exist in isolation, either in the soil, on debris, or on the host, but are continually competing with other organisms, particularly microorganisms. Microbial interactions and the balance between microbial communities are influenced by the prevailing environmental conditions. It has previously been shown that temperature and aw significantly influence the growth and interaction between F. moniliforme and F. proliferatum, and between F. graminearum, F. subglutinans, F. proliferatum, Aspergillus, Penicillium, Eurotium and Trichoderma species (Marín et al., 1998a,b).
In a study of the competing abilities of Fusarium, Aspergillus, Penicillium, Eurotium and
Trichoderma species, Marin et al.(1998a) found that Fusarium species were only dominant at high aw (0.995). Magan and Lacey (1984) found that of a range of field fungi, F. culmorum was the only one able to compete with and dominate other fungi, particularly at aw > 0.95. Within the Fusarium genus, F. graminearum appears to have a competitive advantage over other species under cooler conditions (Marin et al., 1998b; Velluti et al., 2000). Marin et al. (1998b) suggested that F. graminearum has a competitive advantage over F. moniliforme and F. proliferatum at 15 oC, while at 25-30 oC, these species coexisted in the same niche. Similar results were found by Velluti et al. (2000), regardless of aw (0.93, 0.95 and 0.98). Later in this seminar, the occurrence of Fusarium complexes and their impact on mycotoxin production will be discussed.
4 FUSARIUM SPECIES INVOLVED AND MYCOTOXIN PRODUCED
4.1 Fusarium species involved
The species of Fusarium (teleomorph Gibberella) causing fusariosis of cereals are worldwide in distribution and can cause several diseases generally recognized, according to the host, as Gibberella seedling blight, foot rot, and head blight (scab) of small grain cereals (wheat, oats, barley, rye, triticale); and Gibberella stalk and ear rot, and seedling blight of maize. From the mycotoxicological point of view, the phases of disease of greatest concern are certainly scab of small cereals and ear rot of maize, for the potential accumulation of mycotoxins in grains. The etiological characteristic of both these phases, is the co-occurrence or the quick succession of several species of Fusarium usually referred to as a 'complex'. In fact, it is quite common to isolate up to nine different Fusarium species, from a single fragment of infected tissues or up to seventeen different species from freshly harvested wheat samples collected in a limited area. However only a restricted number of species have been regarded as pathogenic and generally only very few of them predominate in a particular host-agroclimatic system (Burgess et al., 1997).
But, like the strains of the pathogenic and predominant Fusarium species, also several strains of the other less pathogenic or opportunistic
Fusarium species are capable of producing considerable amounts of toxins. Therefore, the toxigenic profile of a contaminated crop is determined not only by the predominant pathogenic species, but also by the opportunistic species included in the "complex" (Burgess et al., 1997).
The species predominantly found associated with head blight of wheat and other small cereals are F. graminearum Schwabe and its widespread teleomorph G. zeae (Schw.) Petch, F. culmorum (Wm.G. Sm.) Sacc. and F. avenaceum (Fr.) Sacc. (G. avenacea R.J. Cooke). Among the other less frequently isolated species there are F. poae (Peck) Wollenw., F. crookwellense L.W. Burgess, P.E. Nelson & T.A. Toussoun (syn. F. cerealis Cooke), F. equiseti (Corda) Sacc. (syn. F. scirpi) (G. intricans Wollenw.), F. sporotrichioides Sherb., and F. tricinctum (Corda) Sacc. Several other species may be sporadically encountered, including F. acuminatum Ellis & Everh. (G. acuminata Wollenw.), F. subglutinans (Wollenw. & Reink.) P.E. Nelson, T.A. Toussoun & Marasas (syn. F. sacchari), F. solani (Mart.) Sacc. (Nectria haematococca Berk. & Broome), F. oxysporum Schlecht., and F. semitectum Berk. & Rav. (syn. F. pallidoroseum, F. incarnatum) (Burgess et al., 1997).
Fusarium species may be responsible for at least two kinds of maize ear rot, commonly called as 'red ear rot' mainly caused by species of the Discolor section, and 'pink ear rot', mainly caused by representatives of the Liseola section. The predominant species causing maize 'red ear rot' are F. gramine arum, F. culmorum and F. crookwellense. Among the other less frequently isolated species there are F. subglutinans, F. avenaceum, F. moniliforme J. Sheld. [syn. F. verticillioides (Sacc.) Nirenberg]. The species more frequently isolated from maize 'pink ear rot' and related 'random kernel rot', are essentially the widespread anamorphs of the rather rare G. fujikuroi (Sawada) Ito in Ito & K. Kimura, namely, F. moniliforme, F. proliferatum (T. Matsushima) Nirenberg and F. subglutinans (Wollenw. & Reinking) P.E. Nelson. Among the other toxigenic Fusarium species less frequently isolated from molded maizeears, there are: F. equiseti, F. poae, F. sporotrichioides, F. acuminatum, F. semitectum, F. solani and F. oxysporum (Burgess et al., 1997).
Finally, there are many other species only sporadically isolated from cereals, but in some occasion reported as emerging problem, such as F. anthophilum (A. Braun) Wollenw., F. chlamydosporum Wollenw. & Reink. (syn. F. fusarioides), F. compactum (Wollenw.) Gordon, F. flocciferum Corda, F. heterosporum Nees (syn. F. reticulatum, F. graminum), F. lateritium Nees, F. sambucinum Fuckel, F. torulosum (Berk. & Curt.) Nirenberg, and F. venenatum Nirenberg (Burgess et al., 1997).
Within F. graminearum (G. zeae) were characterized two populations designated as Group 1 and Group 2, with almost the same toxigenic potentiality. The Group 1 very rarely forms perithecia in nature and mainly causes crown rot of cereals and grasses; Group 2 readily forms abundant perithecia in nature and mainly causes head blight of grain cereals and stalk and ear rot of maize. Studies on genetic diversity indicated that F. graminearum Group 2 have greater affinity to F. culmorum and F. crookwellense than to F. graminearum Group 1 (Burgess et al., 1997).
In addition, the toxigenic strains of F. graminearum were classified in two chemotypes: DON and NIV producers, according to the main type B trichothecenes synthesized. Furthermore,
DON-chemotype strains of F. graminearum were subclassified into two types: 3-AcDON and 15-AcDON producers (Miller et al, 1991; Logrieco et al., 1992; Szecsi and Bartok, 1995; Yoshizawa, 1997).
Ecological differences in chemotype distribution may contribute to characterizing a regional grain contamination. Toxigenic strains of F. culmorum can be divided into two types: DON and NIV chemotypes, according to the main type B trichothecenes produced. DON-type strains produced also AcDON (3-AcDON) (Gang et al., 1998; D'Mello et al., 1997).
The species G. fujikuroi has been subdivided into seven distinct mating populations (biological species), indicated as A to G, and covering several Fusarium anamorphs (Leslie, 1995). From these, the most frequently found on maize were F. moniliforme (A), F. proliferatum (D), and F. subglutinans (E), which were also differentiated by their toxigenic capability (Moretti et al., 1997). F. nivale Ces. ex Berl. & Voglino is a well known pathogen of cereals, very frequently found among the major fungi included in the species complex causing 'foot rot' and 'head blight (scab)' of small cereals. F. nivale is no longer considered a Fusarium, first it was placed in the genus Gerlachia [G. nivalis (Ces. ex Berl. & Voglino) W. Gams & E. Müller], and then transferred to Microdochium as M. nivalis (Fr.) Samuels & I.C. Hallett [teleomorph Monographella nivalis (Schaff.) E. Müller]. Therefore M. nivalis is not included in this paper dedicated to cereal fusarioses, also because it has a very low toxicity, and proved to be incapable of producing the typical Fusarium mycotoxins (Logrieco et al, 1991).
4.2 Mycotoxin production
One of the most serious consequences of FHB and ear rot of cereals is the contamination of grain with mycotoxins (D'Mello and Macdonald, 1997; D'Mello et al., 1999; Placinta et al., 1999). The most important classes of Fusarium mycotoxins, based on their harmful effects on human and animal health, are the trichothecenes, fumonisins, moniliformin and zearalenone (ZEA) (D'Mello et al., 1999).
Trichothecene mycotoxins are tricyclic sesquiterpenes and two classes; types A and B, are commonly found in cereals along with the oestrogenic mycotoxin ZEA (D'Mello and MacDonald, 1997; D'Mello et al., 1999). The fumonisin class of mycotoxins comprises a group of structurally related metabolites of which fumonisin B1 (FB1) and B2 (FB2) are commonly found in maize grain with moniliformin (D'Mello and Macdonald, 1997; D'Mello et al., 1999). Mycotoxin production in grain can begin in the field and continue throughout storage. Mycotoxin production is dependent mainly on both well-defined ranges of temperature and aw. But in turn, the optimum climatic conditions for mycotoxin production in infected grains depends on the substrate, Fusarium species and isolate. The influence of temperature and aw on mycotoxin production by Fusarium fungi is probably not entirely direct but rather a function of the influence of these parameters on fungal growth.
- Trichothecenes and zearalenone (ZEA)
Many Fusarium species, including F. graminearum, F. culmorum, F. poae, F. oxysporum and F. sporotrichioides are producers of trichothecene s and ZEA (D'Mello and Macdonald, 1997; D'Mello et al., 1999) (Table 2). F. sporotrichioides and perhaps F. poae predominately produce type A trichothecenes, which includes T-2 toxin, HT-2 toxin, neosolaniol
and diacetooxyscirpenol (DAS). F. culmorum and F. graminearum predominately produce type B trichothecenes, including deoxynivalenol (DON, also known as vomitoxin), its 3-acetyl and 15-acetyl derivatives (3-ACDON and 15-ACDON, respectively) and nivalenol (NIV). Most studies indicate that high moisture favours the production of both classes of mycotoxins, but the optimum temperatures for trichothecene and ZEA production in Fusarium-infected grain appears to be specific to the substrate, species and individual metabolites (Table 2). Moderate rather than warm temperatures favour the production of type A trichothecenes by F. sporotrichioides (Miller, 1994; Mateo et al., 2002) (Table 2). While the optimum production conditions varied depending on the substrate and toxic metabolite, in general F. sporotrichioides-infected maize, wheat and rice grains contained more type A trichothecenes when moistened with 35% water (aw = 0.990) and incubated at 20 oC for 3 weeks than when incubated at higher temperatures or aw. However, Rabie et al. (1986) detected relatively large amounts of T-2 toxin in F. acuminatum-infected oats stored at 25 oC, although a comparison was not drawn between different incubation conditions. In the case of type B trichothecenes, warm humid conditions favour their production during storage of F. culmorum and F. graminearum-infected grain (Greenhlagh et al., 1983; Lori et al., 1990; Beattie et al., 1998; Homdork et al., 2000; Martins and Martins, 2002) (Table 2).
Table 2: The major classes of Fusarium mycotoxin, their principal producers and optimal production conditions on cereal grains
Preglednica 2: Glavni razredi fuzarijskih mikotoksinov, vrste gliv, ki jih tvorijo in optimalni pogoji za njihovo tvorbo na žitnem zrnju
Toxin	Species	Substrates	Optimum production References
conditions3
Type A trichothecenes [T-2 toxin, HT-2 toxin, neosolaniol and diacetoxyscirpenol (DAS)]
Type B trichothecenes [deoxynivalenol (DON), 3-acetyl DON, 15-acetyl DON, nivalenol (NIV)] ZEA
Fumonisins
Moniliformin
F. sporotrichioides F. poae
F. graminearum F.culmorum
Barley, oats, rice, wheat, maize
F. graminearum F. culmorum
F. moniliforme F. proliferatum F. subglutinans F. subglutinans F. moniliforme F. avenaceum
Moderately warm and humid Mateo et al. (2002), (20-25 °C, aw = 0.990) Miller (1994),
Rabie et al. (1986)
Barley, wheat, rice, Warm and humid maize	(25-28 °C, aw = 0.97)
Wheat, rice, maize Warm (17-28 C), or
temperature cycles (e.g. 25-28 C for 14-15 days; 12-15 C for 20-28 days) and humid (aw = 0.97 or 90% RH)
Maize
Wheat, rye, barley, oats, maize
Cool to warm conditions and humid (15-30 C, flw = 0.98) Warm temperatures (25-30 °C)
Greenhalgh et al. (1983),
Lori et al. (1990), Beattie et al. (1998), Homdork et al. (2000) Jiménez et al. (1996), Lori et al. (1990), Ryu and Bullerman
(1999),	Homdork et al.
(2000),	Martins and Martins (2002) Cahagnier et al.
(1995),
Marín et al. (1999a,b)
Kostecki et al. (1999), Schütt (2001)
a Optimum temperature and humidity vary depending on substrate, species and isolate; typical conditions are given in parentheses. Time of production varies from 3 to 8 weeks.
Martins and Martins (2002) found that on F. graminearum-infected cracked corn (aw = 0.97), more of the type B trichothecene DON was produced following incubation at 28 oC for 35 days, rather than at 22 or 28 oC for 15 days followed by 12 oC for 20 days; their results agreed with those of Greenhlagh et al. (1983). Also, maximal DON was produced by F. graminearum on infected wheat and polished rice following incubation in the dark at 27 oC, but in hulled rice, DON production was maximised when incubated at 27 oC in the light (Lori et al., 1990).
The effect of initial infection level may outweigh the effect of environmental conditions on mycotoxin contamination of grain, depending on the toxic metabolite in question. Following 7
months storage of barley grain with high initial Fusarium infection levels (85%), DON contents did not change significantly, irrespective of conditions (-4, 20 or 24 oC, quiescent or forced aeration), although it was lowest in malt produced from the grain stored at 24 oC (Beattie et al., 1998). Initial infection levels would not normally be so high. In wheat stored for 6-8 weeks under warm humid conditions (25 oC, 90% RH), Homdork et al. (2000) found that, while the DON content significantly increased in grain with a low to moderate (4-15%) initial F. culmorum infection level, it did not increase in samples with high (>50%) initial infection levels.
However, the influence of initial infection levels on mycotoxin production may be toxin specific, as
while these conditions were optimal for the production of NIV, unlike DON, it was not present at harvest and levels increased irrespective of initial infection level. As for trichothecenes, the conditions for optimal ZEA production appear to be species, isolate and substrate specific, and may vary from those for DON production. Several studies have found that maximum ZEA was produced in F. graminearum and F. oxysporum-infected maize at aw 0.97 and by cycling the incubation temperatures from 25 to 28 oC for 1415 days, followed by 12-15 oC for 20-28 days (Jiménez et al., 1996; Ryu and Bullerman, 1999; Martins and Martins, 2002) (Table 2).
However, the optimum temperature for ZEA production may vary with isolate and substrate. Jiménez et al. (1996) found that, while the aforementioned conditions were optimal for ZEA production in maize grain infected by two isolates each of F. graminearum and F. oxysporum, another F. graminearum and two F. culmorum isolates produced maximal ZEA after 30 days incubation at room temperature (16-25 oC) rather than at 28 or 37 oC (aw = 0.97). In wheat grain with moderate to high levels (4-15%) of F. culmorum infection, ZEA production was favoured by warm and humid (25 oC, 90% RH) rather than cool and dry storage conditions.
Most ZEA was produced towards the end of the storage period (6-8 weeks) (Homdork et al., 2000). Lori et al. (1990) reported a lower optimal substrate-dependent temperature for ZEA production by a F. graminearum isolate. ZEA production was maximised by incubation of F. graminearum-infected wheat and polished rice in the dark at 17 and 21 oC, respectively, while production was maximised in hulled rice incubated at 27 oC in the light (Lori et al., 1990).
- Fumonisins and moniliformin
Fumonisins and moniliformin are commonly produced in maize infected by F. moniliforme and F. proliferatum, species which tend to grow better at higher temperatures (Keller et al., 1997;
Kostechi et al., 1999; Miller, 2001; Marín et al., 1999a,b). Moniliformin has also been detected in cereals infected with F. avenaceum and F. subglutinans (Kostechi et al., 1999; Torres et al., 2001; Kiecana et al., 2002). While the temperature optima for the production of fumonisins by these pathogens vary, they all prefer aw~ 0.98 and fumonisin production generally decreases with temperature and higher aw (Cahagnier et al., 1995; Marín et al., 1999a,b). Marín et al. (1999a,b) found that aw had a more significant effect than temperature on total fumonisin production in maize grain and ground maize by F. moniliforme and F. proliferatum. In general, fumonisin production and fungal biomass decreased with temperature and aw and was optimal at 15-30 oC and 0.98 aw, depending on the isolate. At marginal temperatures (especially 15 oC), there was an increase in fumonisin production at lower aw levels (0.92 and 0.95) when compared to the concentrations produced at higher temperatures and higher aw levels. But even at 37 oC, Marín et al. (1999b) found that an isolate of F. moniliforme could produce significant amounts of fumonisin.
Ono et al. (1999) attributed the higher fumonisin content of maize in the Northern region of the State of Párana, Brazil compared to the Central-South to higher rainfall in the former during the month preceding harvest (202 and 92.8 mm, respectively). Oxygen limitation retards the growth of F. moniliforme and F. proliferatum and under such conditions it was found that no FB1 was produced (Keller et al., 1997).
Higher temperatures favour moniliformin production in cereal grains infected by F. avenaceum or F. subglutinans (Kostecki et al., 1999; Schütt, 2001). Moniliformin production by a F. subglutinans isolate from maize was higher at 30 than 20 or 25 oC and on rice rather than on wheat, rye, barley, oat or maize grains (Kostecki et al., 1999). Temperature greatly influenced moniliformin production by F. avenaceum on wheat, with more being produced under mediterranean rather than temperate conditions (Schütt, 2001).
5 CONCLUSIONS
Temperature and humidity/wetness are the main climatic factors influencing the development of Fusarium fungi causing diseases of cereals, although the influence of these climatic factors is not independent of other environmental and host factors. Many gaps exist in our knowledge of the influence of environmental parameters on Fusarium diseases of cereals. A risk assessment model for the forecasting of FHB epidemics in Ireland, based on environmental conditions is currently being developed (van Maanen, Cook and Doohan, unpubl. data). These data will also form
part of an EU risk assessment model (EU RAMFIC project QLRT-1999-31517).
Particularly interesting questions for future research are: the influence of humidity on Fusarium diseases of small-grain cereals and the influence of environmental parameters on both the mycotoxin profiles (rather than individual metabolites) and biological control of Fusarium spp. Knowledge of the influence of climatic conditions on Fusarium diseases may prove useful towards developing novel disease control methods.
ó REFERENCES
Beattie S., Schwarz P.B., Horsley R., Barr J., Casper H.H. 1998. The effect of grain storage conditions on the viability of Fusarium and deoxynivalenol production in infested malting barley. Journal of Food Protection, 61: 103-106
Brennan J.M., Fagan B., Van Maanen A., Cooke B.M., Doohan F.M. 2003. Studies on in vitro growth and pathogenicity of Fusarium fungi. European Journal of Plant Pathology, 109: 577-587
Burgess L.W., Summerell B.A., Backhouse D., Benyon F., Levic J. 1997. Biodiversity and population studies in Fusarium. Sydowia (Special issue March 30, 1997): 1-11
Cahagnier B., Melcion D., Richard-Molard D. 1995. Growth of Fusarium moniliforme and its biosynthesis of fumonisin B1 on maize grain as a function of different water activities. Letters in Applied Microbiology, 20: 247-251
Castella G., Munkvold G.P., Imerman P., Hyde W.G. 1999. Effects of temperature, incubation period and substrate on the production of fusaproliferin by
Fusarium subglutinans ITEM 2404. Natural Toxins, 4: 129-132
Cook R.J., Christen A.A. 1976. Growth of cereal root rot fungi as affected by temperature-water potential interactions. Phytopathology, 66: 193-197
D'Mello J.P.F., Macdonald A.M.C. 1997. Mycotoxins. Animal Feed Science and Technology, 69: 155-166
D'Mello J.P.F., Placinta C.M., Macdonald A.M.C. 1999. Fusarium mycotoxins: A review of global implications for animal health, welfare and productivity. Animal Feed Science and Technology, 80: 183-205
Doohan F.M., Parry D.W., Jenkinson P., Nicholson P. 1998. The use of species-specific PCR-based assays to analyse Fusarium ear blight of wheat. Plant Pathology, 47: 197-205
Etcheverry M., Torres A., Ramirez M.L., Chulze S., Magan N. 2002. In vitro control of growth and fumonisin production by Fusarium verticillioides and F. proliferatum using antioxidants under different water availability and temperature regimes. Journal of Applied Microbiology, 92:
624-632
Francis R.G., Burgess L.W. 1977. Characteristics of Fusarium roseum 'Graminearum ' in Eastern Australia. Transactions of the British Mycological Society, 68: 421-427
Gang G., Miedaner T., Schuhmacher U., Schollenberger M., Geiger H.H. 1998. Deoxynivalenol and nivalenol production by Fusarium culmorum isolates differing in aggressiveness toward winter rye. Phytopathology, 88: 879-884
Greenhlagh R., Neish G.A., Miller J.D. 1983. Deoxynivalenol, acetyl deoxynivalenol, and zearalenone formation in Canadian isolates of Fusarium graminearum on solid substrates. Applied and Environmental Microbiology, 46:
625-629
Homdork S., Fehrmann H., Beck R. 2000. Influence of different storage conditions on the mycotoxin production and quality of Fusarium-infected wheat grain. Journal of Phytopathology, 148: 7-15
Jiménez M., Máñez M., Hernández E. 1996. Influence of water activity and temperature on the production of zearalenone in corn by three Fusarium species.
International Journal of Food Microbiology, 29: 417-421
Keller S.E., Sullivan T.M., Chirtel S. 1997. Factors affecting the growth of Fusarium proliferatum and the production of fumonisin B1: oxygen and pH. Journal of Industrial Microbiology and Biotechnology, 19: 305-309
Kiecana I., Mielniczuk E., Kaczmarek Z., Kostecki M., Golinski P. 2002. Scab response and moniliformin accumulation in kernels of oat genotypes inoculated with Fusarium avenaceum in Poland. European Journal of Plant Pathology, 108: 245-251
Kostecki M., Wisniewska H., Perrone G., Ritieni A., Golinski P., Chelkowski J., Logrieco A. 1999. The effects of cereal substrate and temperature on production of beauvericin, moniliformin and fusaproliferin by Fusarium subglutinans ITEM-1434. Food Additives and Contaminants, 16: 361365
Leslie J.F. 1995. Gibberella fujikuroi: available populations and variable traits. Canadian Journal of Botany 73 (Suppl. 1): 282-291
Leslie J.F., Marasas W.F., Shephard G.S., Sydenham E.W., Stockenstrom S., Thiel P.G. 1986. Duckling toxicity and the production of fumonisin and moniliformin by isolates in the A and E mating populations of Gibberella fujikuroi (Fusarium moniliforme). Applied and Environmental Microbiology, 62: 1182-1187
Logrieco A., Altomare C., Mulè G., Bottalico A. 1992. Alcuni dati sulla presenza e patogenicità di chemiotipi di Fusarium graminearum in Europa. Atti Giornate Fitopatologiche 2: 287-294
Logrieco A., Vesonder R.F., Peterson S.W., Bottalico A. 1991. Reexamination of the taxonomic disposition of and deoxynivalenol production by
Fusarium nivale NRRL 3289. Mycologia, 83: 367370
Lori G.A., Henning C.P., Violante A., Alippi H.E., Varsavsky E. 1990. Relation between the production of deoxynivalenol and zearalenone and the mycelial growth of Fusarium graminearum on solid natural substrates. Microbiologia, 6: 76-82
Magan N., Lacey J. 1984. Effect of water activity, temperature and substrate on interactions between field and storage fungi. Transactions of the British Mycological Society, 82: 83-93
Marín S., Companys E., Sanchis V., Ramos A.J. 1999a. Twodimensional profiles of fumonisin B1 production by Fusarium moniliforme and Fusarium proliferatum in relation to environmental factors and potential for modelling toxin formation in
maize grain. International Journal of Food Microbiology, 51: 159-167
Marín S., Homedes V., Sanchis V., Ramos A.J., Magan N. 1999b. Impact of Fusarium moniliforme and Fusarium proliferatum colonisation of maize on calorific losses and fumonisin production under different environmental conditions. Journal of Stored Food Products, 35: 15-26
Marín S., Companys E., Sanchis V., Ramos A.J. 1998a. Effect of water activity and temperature on competing abilities of common maize fungi. Mycological Research, 120: 959-964
Marín S., Sanchis V., Ramos A.J., Vinas I., Magan N. 1998b. Environmental factors, in vitro interactions, and niche overlap between Fusarium moniliforme, F. proliferatum and F. graminearum, Aspergillus and Penicillium species from maize grain. Mycological Research, 102: 831-837
Marín S., Sanchis V., Teixidó A., Sáenz R., Ramos A.J., Vinas I., Magan N. 1996. Water and temperature relations and microconidial germination of Fusarium moniliforme and Fusarium proliferatum from maize. Canadian Journal of Microbiology, 42: 1045-1050
Marín S., Sanchis V., Magan N. 1995. Water activity, temperature and pH effects on growth of Fusarium moniliforme and Fusarium proliferatum isolates from maize. Canadian Journal of Microbiology, 41: 1063-1070
Martins M.L., Martins H.M. 2002. Influence of water activity, temperature and incubation time on the simultaneous production of deoxynivalenol and zearalenone in corn (Zea mays) by Fusarium graminearum. Food Chemistry, 79: 315-318
Mateo J.J., Mateo R., Jiménez M. 2002. Accumulation of type A trichothecenes in maize, wheat and rice by Fusarium sporotrichioides isolates under diverse culture conditions. International Journal of Food Microbiology, 72: 115-123
Mesterhazy A., Bartok T., Mirocha C.G., Komoroczy R. 1999. Nature of wheat resistance to Fusarium head blight and the role of deoxynivalenol for breeding. Plant Breeding, 118: 97-110
Miedaner T. 1997. Breeding wheat and rye for resistance to Fusarium diseases. Plant Breeding, 116:201-220
Miller J.D. 2001. Factors that affect the occurrence of fumonisin. Environmental Health Perspectives, 109:321-324
Miller J.D. 1994. Epidemiology of Fusarium diseases of cereals. In: Miller J.D., Trenholm H.L. (eds)
Mycotoxins in Grain: Compounds other than Aflatoxins. Eagon Press, St. Paul, MN, USA: 19-36
Miller J.D., Greenhalgh R., Wang Y.Z., Lu M. 1991. Trichothecene chemotype of three Fusarium species. Mycologia, 83: 121-130
Moliszewska E., Pisarek I. 1996. Influence of humic substances on the growth of two phytopathogenic soil fungi. Environment International, 22: 579-584
Moretti A., Logrieco A., Bottalico A., Ritieni A., Fogliano V., Randazzo G. 1997. Diversity in beauvericin and fusaproliferin production by different populations of Gibberella fujikuroi (Fusarium section Liseola). Sydowia (Special issue March 30, 1997): 44-56
Odiemah M., Manninger I. 1994. Inheritance of resistance to Fusarium ear rot in maize. Acta Phytopathological Academiae Scientarum Hungaricae, 17: 91-99
Ono E.Y., Sugiura Y., Homechin M., Kamogac M., Vizzoni E., Ueno Y., Hirooka E.Y. 1999. Effect of climatic conditions on natural mycoflora and fumonisins in freshly harvested corn of the state of Parana Brazil. Mycopathologia, 147: 139-148
ParryD.W., Jenkinson P., McLeod L. 1995. Fusarium ear blight (scab) in small-grain cereals - a review. Plant Pathology, 44: 207-238
ParryD.W., Pettitt T.R., Jenkinson P., Lees A.K. 1994. The cereal Fusarium complex. In: Blakeman P., Willamson B. (eds) Ecology of Plant Pathogens. CAB International, Wallingford, UK: 301-320
Pettitt T.R., Parry D.W., Polley R.W. 1996. Effect of temperature on the incidence of nodal foot rot symptoms in winter wheat crops in England and Wales caused by Fusarium culmorum and Microdochium nivale. Agricultural and Forest Meteorology, 79: 233-242
Placinta C.M., D'Mello J.P.F., Macdonald A.M.C. 1999. A review of worldwide contamination of cereal grains and animal feed with Fusarium mycotoxins. Animal Feed Science and Technology, 78: 21-37
Pomeranz Y., Bechter D.B., Sauer D.B., Seitz L.M. 1990. Fusarium headblight (scab) in cereal grains. Advances in Cereal Science and Technology, 10: 373-433
Rabie C.J., Sydenham E.W., Thiel P.G., Lübben A., Marasas W.F. 1986. T-2 toxin production by
Fusarium acuminatum isolated from oats and barley. Applied and Environmental Microbiology, 52: 594-596
Ryu D., Bullerman L.B. 1999. Effect of cycling temperatures on the production of deoxynivalenol and zearalenone by Fusarium graminearum NRRL 5883. Journal of Food Protection, 62: 1451-1455
Saremi H., Burgess L.W., Backhouse D. 1999. Temperature effects on the relative abundance of Fusarium species in a model plant-soil ecosystem. Soil Biology and Biochemistry, 31: 941-947
Schutt F. 2001. Moniliformin production of Fusarium species under defined conditions. Ph.D. Thesis, Technical University of Berlin, Germany: 135-137.
Sutton J.C. 1982. Epidemiology of wheat head blight and maize ear rot caused by Fusarium graminearum. Canadian Journal of Plant Pathology, 4: 195-209
Szecsi A., Bartok T. 1995. Trichothecene chemotypes of Fusarium graminearum from corn in Hungary. Mycotoxin Research, 11: 85-92
Tekauz A., McCallum B., Gilbert J. 2000. Review: Fusarium head blight of barley in western Canada. Canadian Journal of Plant Pathology, 22: 9-16
Torres A.M., Reynoso M.M., Rojo F.G., Ramirez M.L., Chilze S.N. 2001. Fusarium species (section Liseola) and its mycotoxins in maize harvested in northern Argentina. Food additives and Contaminants, 18: 836-843
Velluti A., Marin S., Bettucci L., Ramos A.J., Sanchis V. 2000. The effect of fungal competition on colonisation of maize grain by Fusarium moniliforme, F. proliferatum and F. graminearum and on fumonisin B1 and zearalenone formation. International Journal of Food Microbiology, 59:
59-66
Vigier B., Reid L.M., Seifert K.A., Stewart D.W., Hamilton R.I. 1997. Distribution and prediction of Fusarium species associated with maize ear rot in Ontario. Canadian Journal of Plant Pathology, 19:
60-65
Yoshizawa T. 1997. Geographic differences in trichothecene occurrence in Japanese wheat and barley. Bulletin of the Institute for Comprehensive Agricultural Sciences Kinki University, Nara, Japan, 5: 23-29