Abstract
Zearalenone* is a non-steroidal mycotoxin with oestrogenic properties, which is produced mainly by fungi belonging to Fusarium (*6-(10-hydroxy-6-oxo-trans–1–undecenyl)-β-resorcylic acid lactone). The toxin-producing ability of Fusaria is greatly influenced by environmental factors. Therefore, it was expected that the different weather conditions occurring during the vegetation period would be associated with differences in the preharvest occurrence of Fusarium toxins. Sustainable food systems research and practice concentrate on the study of the level of these mycotoxins in soils and crops. However, some experiments show that zearalenone can also act as a hormonal substance and have a favourable effect on the development of plants and animals. This chapter gives an overview of the possible effect of low concentrations of zearalenone on some physiological processes in crops. It has been shown that exogenous application of zearalenone and its derivatives can stimulate generative development in winter plants, which suggest its participation in the mechanism of flowering. Moreover, treatment with zearalenone had an effect on calli proliferation and cell differentiation. The effect of zearalenone was similar to the activity of auxins in in vitro cultures, which may confirm the hormonal properties of zearalenone in plants. Watering and soaking wheat and soybean grains with zearalenone solution resulted in higher yields of these plants. These observations, compared with the possibility of weather-related changes in the exogenous content of zearalenone in soils, can be useful in determining the optimal zearalenone dose that would show the favourable effect of this substance in plant development.
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15.1 Introduction
Zearalenone is a mycotoxin produced by several Fusarium species. The term mycotoxin refers to a large number of chemically diverse toxic secondary metabolites formed by fungi imperfectly growing on agricultural commodities. Since the discovery of the aflatoxins in 1960 and subsequent recognition that mycotoxins are of significant health concern to both humans and animals, regulations gradually developed for mycotoxins in food and feed. Fusarium diseases of wheat, barley, and maize cause significant yield losses worldwide and are therefore of great economic importance (Sutton 1982; Diekman and Green 1992; Parry et al. 1995; Miedaner 1997; Mesterhazy et al. 1999; Malekinejad et al. 2007). The influence of host cultivars on the pathogenicity and toxicity of Fusarium fungi has been extensively reviewed (Miedaner 1997; Mesterhazy et al. 1999; Miedaner et al. 2001; Magg et al. 2002). Mycotoxins can contaminate grains in the field when environmental conditions favour fungal infection, and levels can increase dramatically if storage conditions are favourable for fungal growth. 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 (Doohan et al. 2003). Therefore, it was expected that the different climatic conditions during the years surveyed would be associated with differences in the preharvest occurrence of Fusarium toxins. The European Commission has recently specified the maximum levels of Fusarium toxins that will be allowed from July 2006 onwards. Maximum levels of 200 and 100 μg/kg have been specified for zearalenone in unprocessed corn and unprocessed cereals other than corn, respectively (Javier et al. 2007; Hans et al. 2007)
In spite of the fact that contamination of cereals and grains and related products with mycotoxins causes food and feed-borne intoxications in man and livestock, zearalenone in low concentrations can be treated as a plant hormone which influences the development and yield of crop plants (Biesaga-Kościelniak 2001). This review focuses on the effect of low doses of zearalenone on the stimulation of selected physiological processes in plants important for agriculture production.
15.2 Chemical Structure of Zearalenone
Zearalenone, 6-(10-hydroxy-6-oxo-trans–1–undecenyl)-β-resorcylic acid lactone, is a non-steroidal mycotoxin with oestrogenic properties. It was first isolated from extracts of fungus Gibberella zeae (Fusarium graminearum) by Stob et al. (1962). This component is believed to act as an endogenous regulator of the sexual stage of development of their producer fungi. In the organisms of warm-blooded animals, the lactones mimic endogenous 17 β-estradiol, i.e. they stimulate the growth of muscle tissue and affect the functions of the reproductive system (Burkin et al. 2002). Its chemical structure was determined by Urry et al. (1966), and its name is derived from G. zeae, the name of the first studied organism that produces it; resorcylic acid lactone, the generic name for this group of natural products; ene, the standard suffix indicating the presence of the C-1′ to C-2′ double bond; and one, the standard suffix indicating the presence of the C-6′ ketone (Fig. 15.1). Nowadays zearalenone is produced commercially by fermentation (Hidy et al. 1977) for use in the manufacture of zeranol (zearalanol) by catalytic hydrogenation (Hodge et al. 1966). It is a secondary fungal metabolite produced by several species of Fusarium, mainly by F. graminearum and F. culmorum. These species are known to colonize maize, barley, oats, wheat and sorghum (Eppley et al. 1974; Mirocha et al. 1974; Jemmali et al. 1978; Bennett and Shotweli 1979; Farnworth and Neish 1980; Kuiper-Goodman et al. 1987; Kuiper et al. 1988; Tanaka et al. 1988; Bennett and Klich 2003) and tend to develop during prolonged cool, wet growing and harvest seasons in the temperate and warm regions of the world (Velluti et al. 2000). Of numerous zearalenone derivatives that can be produced by Fusarium spp., only trans-α-zearalenol has been found to occur naturally in cereal grains (Richardson et al. 1985). After consumption of zearalenone, the two stereoisomeric metabolites, α- and β-zearalenole (Fig. 15.1), are produced in mammals by reduction of the keto-group at C-6′. Another structurally similar compound is zearalanol (zeranol, Ralgro), which is synthetically produced from zearalenone and is used as a growth promoter in animals and has been banned in the European Union since 1985 (Hagler et al. 2001; Nsahlai et al. 2002). Zearalanol is distinguished from zearalenone by lack of a C-1′–C-2′ double bond. This substance can also be formed in vivo from zearalenone and α-zearalenole, which can be carried over from contaminated feed stuff to animals. Zearalenone and zearalenoles (α and β) act as estrogens because they can adopt a conformation which sufficiently resembles 17 β-estradiol and other natural estrogens to enable binding to the estrogen receptor (King et al. 1978; Miksicek 1994). The physiological effects of zearalanol are similar to those of zearalenone, but zearalanol is generally considered to produce estrogenic effects five to ten times greater than those of zearalenone (Schollenberger et al. 2006).
Owing to their frequent occurrence, zearalenone and zearalenoles are an important class of endocrine disrupters. Their estrogenic potential is comparable to that of the naturally occurring estrogens estrone and estriol and is several orders of magnitude higher than those of well-known environmental estrogens, e.g. organochlorine pesticides (Mirocha et al. 1971, 1974; Krska and Josephs 2001; Dai et al. 2004).
15.3 Chemical and Physical Properties
Zearalenone is a white crystalline compound, which exhibits blue-green fluorescence when excited by long-wavelength UV light (360 nm) and a more intense green fluorescence when excited by short-wavelength UV light (260 nm). In methanol, UV absorption maxima occur at 236, 274 and 316 nm. The molecular formula of zearalenone is C18H22O5, its molecular weight is 318.4 g/mol and its melting point is 162–163°C (Blackwell et al. 1985; Josephs et al. 2003). The maximum fluorescence in ethanol occurs with irradiation at 314 nm and with emission at 450 nm. Its solubility in water is about 0.002 g/100 ml. In an aqueous solution of inositol, the presence of zearalenone can change the crystal structure of this alcohol, which indicates the possibility of interaction between both substances (our observations). Moreover, zearalenone is slightly soluble in hexane and progressively more so in benzene, acetonitrile, methylene chloride, methanol, ethanol and acetone. However, it is readily soluble in aqueous alkali.
In fungal cultures a number of closely related metabolites are formed, but there is only limited evidence that these occur in foodstuffs, although there is experimental evidence for some transmission of zearalenone and α- and β-zearalenols into the milk of sheep, cows and pigs fed with these substances at high concentrations. Zearalenone does not degrade at high temperatures (Zinedine et al. 2007), but may be partly decomposed by heat. Approximately 60% of zearalenone remained unchanged in bread while about 50% survives in the production of noodles. Extrusion cooking may result in significant reduction of zearalenone with higher reductions of this substance at 120–140°C than at 160°C (Mateo et al. 2002).
15.4 Analytical Methods
Because estrogenic mycotoxins usually occur at microgram per kilogram (μg/kg) levels there is special interest in analytical procedures for reliable detection of zearalenone and its metabolites between 10 and 100 μg/kg. In response to the risk of a great economic loss to the industry and the threat to human health as a result of exposure to zearalenone, several methods have been developed for the quantification of zearalenone and its metabolites in different foods, feeds, animal tissues, blood and urine. Detailed reviews have been given by Steyn et al. 1991; Betina 1993; Frisvad and Thrane 1993; Scott 1993; Steyn 1995 and Lawrence and Scott 2000. The determination of zearalenone in cereals can be divided into five steps: grinding of the sample, extraction of the sample, clean-up, separation and detection.
In this regard several sophisticated chromatographic methods, with a quantification limit down to about 0.2 ng/g, have been developed and published for the determination of zearalenone. The methods were mainly based on high-performance liquid chromatography (HPLC) with fluorescence detection (Krska 1998; Visconti and Pascale 1998; Schuhmacher et al. 1998; Tanaka et al. 2000), but HPLC with mass spectrometry detection was also used (Shirai et al. 2000; Josephs et al. 2001).
Another method which uses capillary electrophoresis with laser-induced fluorescence detection can also be employed to detect zearalenone (Maragos and Appell 2007). In order to analyse trace amounts of zearalenone in plants, a sensitive, quick and accurate method, the enzyme-linked immunosorbent assay (ELISA) was developed by Chen et al. 1989.
15.5 Occurrence of Zearalenone in Plants
The occurrence of a zearalenone-like compound as a substance existing endogenously in plants was first reported by Li et al. (1980) and Li and Meng (1989). The aseptic culture of analysed shoot apices of the overwintering wheat plant confirmed that this substance was not due to fungal contamination, but was synthesized endogenously by the plants themselves. It was later confirmed by Meng et al. (1989) and Chen et al. (1989) using the enzyme-linked immunosorbent assay. This substance was identified by them as zearalenone.
The endogenous existence of zearalenone in plants served as a spur to further studies and its identification in different species. Han and Meng (1986) found zearalenone in rape, Meng et al. (1986) in winter wheat, Li and Meng (1989) in Apium gaveoleus, Que et al. (1990) in cotton, Han and Meng (1991) in Lemna perpusilla and Fu and Meng (1994) in tobacco buds. Moreover, Meng et al. (1996) suggested the occurrence of this substance in more than 30 species of plants among others in onion, corn, rice, cotton, carrot, celery and apple. These data were not confirmed by other authors and the difficulty with their verification is connected with the fact that the majority of these articles are published in Chinese. However, our unpublished data indicate that small amounts of endogenous zearalenone can exist in winter wheat, soybean and spring rape. These measurements (high-performance liquid chromatography) were performed on plants cultured in vitro in sterile conditions.
15.6 Influence of Exogenous Zearalenone on Plant Generative Development
For agriculture plants, effective flowering is a very important process. In this process, a vegetative meristem changes into a reproductive meristem which is capable of forming floral organs and in this way completes the reproductive life cycle of higher plants (Bernier and Périllex 2005). How the vegetative meristem is able to perceive and interpret signals from the environment as well as from the plant itself is largely unknown. The process by which vernalization – the exposure of a germinating seed or a juvenile plant to a prolonged period of low temperature – promotes flowering in an adult plant has remained a mystery for many years (Michales and Amasimo 2000). Vernalization is an important control for many agricultural and horticultural production species in temperate regions.
Some studies indicated that exogenous zearalenone influences plant growth and development. For example, zearalenone stimulated the initiation of the vegetative bud in tobacco pith callus tissue (Mirocha et al. 1968), inhibited the cell membrane transport of maize roots (Vianello and Macri 1981) and enhanced the a-amylase and b-glucosidase activities of germinating maize seeds.
Meng et al. (1992) found that zearalenone was an endogenous regulator controlling induction of generative development in winter plant. An increase in endogenous zearalenone during vernalization was also recorded by Fu and Meng (1994) in many winter plants. Moreover, they suggested that exogenous zearalenone can partly replace the low temperature requirement for flowering in winter wheat.
In combination with greatly shortened vernalization (14 days, 5°C) zearalenone completely eliminated the flowering blockade of winter wheat cv. Grana, which usually requires vernalization of 8–9 weeks (Biesaga-Kościelniak 1998) (Table 15.1). Moreover, zearalenone in the concentration 2 mg/dm3 reduced the length of the vegetative phase by as much as about 50 days in comparison with the control sample (Biesaga-Kościelniak 2001) (Fig. 15.2). The stimulating effect of zearalenone on the induction of heading was observed also in other wheat varieties, and its effectiveness was highest in those varieties which needed longer time of low temperature treatment to flowering induction (Table 15.2). Some zearalenone derivatives exercised a greater influence on the induction of heading and the rate of generative development of winter wheat cv. Grana than this substance itself (Table 15.3). Very strong activity has been demonstrated, in particular, by α-zearalanol, which after only 7 days of vernalization at 5°C induced the heading of almost all plants and greatly reduced the duration of the vegetative phase. The effectiveness of zearalenone was increased by an addition of spermidine and tissue extracts from inflorescences of some plant species. The effect of zearalenone on the growth process of wheat was to some extent contrary to its effect on the generative development, since it inhibited the elongation of the shoots, and also reduced their ability to accumulate biomass. The role of zearalenone in inducing flowering of winter wheat plants was confirmed by experiments with an exogenous application of a zearalenone synthesis inhibitor (malathion). This inhibitor decreased the plants’ heading ability even after long vernalization (Table 15.4).
The influence of zearalenone on the generative development of winter rape was much weaker in comparison with that of wheat. None of the concentrations which stimulated wheat plants induced the flowering of rape plants. Zearalenone treatment stimulated only the first step of the process of the shoot apices generative differentiation (Biesaga-Kościelniak 2001).
Biochemical analysis indicated that the stimulation of the generative differentiation in wheat shoot apices after short vernalization, but in the presence of zearalenone was connected with an intensified emission of heat and a decrease in the value of the electric potential of the cells (Biesaga-Kościelniak 2001). Additionally, during vernalization of these plants and after vernalization, zearalenone induced changes in the composition of fatty acids in the fractions of membrane glycolipids and phospholipids. Zearalenone treatment resulted in the increase in content unsaturated fatty acids (calculated as 18:3 to 18:2 ratio). Such an increase in fatty acid unsaturation is usually a result of changes in cell membranes being exposed to low temperatures. On the other hand, zearalenone somewhat hampered the adjustment of the fluidity of the cell membranes, which was indicated by an increase in the content of campesterol and cholesterol in the seedlings. The observed dual effect of this substance on membrane composition is that it can stabilize membrane structure at low temperature, which allows specific domains located on membranes to become more prominent. Such changes may be involved in the pathway of induction of generative development of winter plants induced by vernalization. The involvement of zearalenone in the vernalization process was suggested by Meng et al. (1996) who indicated two specific zearalenone-binding proteins (39.8 and 12.5 kDa) in the vernalized embryos of winter wheat. They postulated that these proteins might act as activators of certain genes controlling the vernalization process in plants.
The role of zearalenone in generative induction was also confirmed in photoperiodic plants (Meng et al. (1992, 1996; Fu et al. (1995, 2000), which suggests its importance in flowering stimulation. In the short-day plant L. perpusilla 6746 and the long-day plant L. gibba G3, zearalenone enhanced flowering. In the day-neutral tobacco (Nicotiana tabacum L. cv. Samsun), zearalenone was one of the important flower stimuli and was related to the flower gradient in shoots (Meng et al. 1996). In the studies of Fu et al. (2000) a connection between zearalenone and flower bud formation in thin-cell layer explants of N. tabacum L was indicated. During the formation of flower buds, the authors observed two peaks in the endogenous zearalenone level, one at day 3 and the other at day 9 after the outset of the culture. The inhibitor of zearalenone biosynthesis (malathion), inhibited the biosynthesis of endogenous zearalenone and at the same time flower bud neoformation. Exogenous zearalenone application reduced the effect of malathion and stimulated flower bud neoformation.
15.7 The Effect of Zearalenone in Culture In Vitro
The presence of hormones (auxins and cytokinins or substances of similar action) is required for the induction, proliferation and differentiation of cells in in vitro cultures (Maheshwari et al. 1995). The dynamic development and the introduction of in vitro techniques to micropropagation and to the study of mechanisms of physiological processes have resulted in the need for the search for new groups of substances playing a role similar to those of plant hormones. Fusicoccine, cotynine, helmintosporine, pestalocine and some other metabolites isolated from fungi belong to this group (Muller et al. 1991).
In tissue culture of wheat and rape, the influence of zearalenone greatly resembled that of 2,4-dichlorophenoxyacetic acid (2,4-D), a synthetic analogue of auxin (Biesaga-Kościelniak 2001; Biesaga-Kościelniak et al. 2003). Zearalenone completely replaced 2,4-D or increased its effect under in vitro conditions. It increased the percentage of wheat calli capable of regenerating shoots by more than 2,4-D, and especially the process of effectively regenerating shoots from poorly differentiated wheat calli. Zearalenone enabled the breaking of the blockade of the regeneration of shoots from callus of winter rape cv. “Górczański”. Additionally, the application of thidiazurone to theses media increased the percentage of plant regenerated from callus for both wheat and rape. Therefore, it is possible to use zearalenone as an alternative to auxin or as a supplementary hormone analogue in in vitro culture of plants. This could be especially important when indirect regeneration of plants via callus induction is planned (Biesaga-Kościelniak et al. 2003; Szechyńska-Hebda et al. 2007).
Moreover, zearalenone stimulated the growth of cell suspension of winter wheat and winter rape (in aqueous media) by more than 2,4-D, contributing to the increment in the volume and dry weight of cells during the culture period (Biesaga-Kościelniak 2001). In the suspension culture of wheat, the addition of zearalenone to a medium containing 2,4-D caused not only an increase in the dry weight of cells, but also an increase in the population of living cells in the culture.
The maize pollination system was used as a model to compare the activity of zearalenone with 2,4-D (Biesaga-Kościelniak 1998). Zearalenone in a concentration 50 times lower than that of 2,4-D demonstrated a similar effectiveness in stimulating the development of haploid embryos in wheat flowers after pollination with maize pollen (Biesaga-Kościelniak et al. 2003). The concentration of zearalenone (6 mM) was most effective in inducing ovary swelling (84 swollen ovaries/100 pollinated florets) and increasing the frequency of embryo induction (18.9 embryos/100 pollinated florets), but these embryos were severely deformed. They had low capability to germinate in vitro, while callus was easily formed and indirect regeneration of plants was possible. The results showed that zearalenone had some of the properties of an auxin analogue, while other effects of its actions were unique.
Zearalenone was also found to be more effective than cytokinin treatment in inducing shoots in in vitro winter wheat production. Moreover, both zearalenone and cytokinins increased the activity of antioxidant enzymes in wheat callus undergoing regeneration, and it is very likely that they also stimulated the plant regeneration process (Szechyńska-Hebda et al. 2007). The effectiveness of regeneration on media containing zearalenone shows the possibility of using zearalenone as an alternative hormone also to cytokinins in winter wheat callus culture.
15.8 Modifying Plant Growth and Yield Using Zearalenone
Our studies show that zearalenone can be used to increase the yield of wheat (Biesaga-Kościelniak et al. 2006a, b). Plants that were sprayed with zearalenone during the heading stage increased their number of grains per ear and their weight per 1,000 grains. Watering and soaking wheat grains produced even better effects in comparison to spraying (Biesaga-Kościelniak et al. 2006a). Zearalenone-treated plants had a higher number and weight per ear and weight per 1,000 grains. The reproduction of plants was also increased. The best results (yield increase) were noted for a zearalenone concentration of 4 mg/dm3. In soybean cultivation, treating plants with zearalenone also increased their yield (Biesaga-Kościelniak et al. 2006b) (Fig. 15.3). Watering seedlings, soaking seeds and spraying plants increased the yield, the number of pods and the number of grains per pod and per soybean plants. The increase in the yield of soybean and wheat cultivars in comparison to controls (without zearalenone treatment) was 22% and 19% in terms of the number of seeds (grains) and 28% and 24% in terms of the weight of seeds (grains), respectively.
The effect of zearalenone on crop development may be connected to its influence on the status and functioning of the photosynthetic apparatus (Kościelniak et al. 2008). The after-effects of zearalenone on the growth of soybean and wheat plants, net photosynthesis and transpiration rates, stomatal conductance, photochemical efficiency of photosystem 2 and on final seeds yield were determined. Modifications in leaf area were more pronounced in soybean than in wheat, and this tendency increases in successive developmental phases. The net photosynthesis was stimulated during the juvenile phase and during that of the final one by about 13.6% (average) in soybean plants. Stimulation of transpiration was also observed after zearalenone treatment on both plant species. The response of CO2 assimilation in wheat plants was less pronounced when compared to that in soybean. Additionally, the quantum yield of photosystem 2 photochemistry in soybean plants increased rapidly after the seeds were treated with zearalenone, and was higher in wheat plants where this parameter increased constantly during whole period of growth (Kościelniak et al. 2008).
The observed effects of zearalenone action on plant development may be connected to the properties of zearalenone, as a component of mycotoxines. It is known that some stress factors (also toxic chemicals) accelerate plant development and stimulate their generative induction. However, our results (data in preparation) indicate that zearalenone may protect cells from some forms of stress. In drought, stresses induced by either NaCl or changes in water potential (poly(ethylene glycol)content), zearalenone applied in concentrations 2 and 4 mg/dm3 decreased the inhibiting effect of both these stresses on wheat seedlings and significantly increased the dry mass and length of plants. This effect was especially visible in parts of plants aboveground where an increase of about 84% was detected. In roots, zearalenone stimulated about 42% increase in mass in NaCl conditions in comparison to the control (non-zearalenone-treated) plants. Moreover, at the water potential of −0.5 MPa, the dry mass of shoots in plant cultures treated with zearalenone was 58% higher than that of the control (0 MPa). This protective effect of zearalenone may be a result of its ability to increase the metabolism of seedlings. This effect was confirmed by calorimetric measurements, which indicated an increase in the heat energy emitted by wheat plants treated with zearalenone, where this metabolism parameter increased by about 16% in comparison to non-zearalenone-treated plants.
15.9 Conclusion
Temperature, water availability and light are key climatic factors influencing the production of Fusarium. In terms of manipulating environmental conditions to control Fusarium spp. diseases, adjustment of soil temperature and moisture has been successfully applied in many countries (Katan 1981; Doohan et al. 2003). Although zearalenone is ubiquitous and toxic, it globally presents a potential danger for animal and human health only when it is absorbed in high amounts or over a long period of exposure (Zinedine et al. 2007). Small amounts of zearalenone act as stimulating factors for plant development, and can serve as plant hormone in induction of physiological processes. Thus, low zearalennone concentration in growth media may be useful to stimulate development of crops and to accelerate the flowering of winter plants, which can be an important factor in agriculture production in changing environmental conditions. A particularly interesting question for future research is the possibility of determining the optimal zearalenone concentration in soil (and in crops) to balance the toxic and favourable action of this substance on both plant development and animal health.
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Biesaga-Kos´cielniak, J., Filek, M. (2010). Occurrence and Physiology of Zearalenone as a New Plant Hormone. In: Lichtfouse, E. (eds) Sociology, Organic Farming, Climate Change and Soil Science. Sustainable Agriculture Reviews, vol 3. Springer, Dordrecht. https://doi.org/10.1007/978-90-481-3333-8_15
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