1. State of the art

Cereals are a major source of calories consumed by people worldwide on a daily basis. With increasing global population, food production needs to increase by 50 to 70% in the next 30 years to avoid global food insecurity [1]. The danger of food insecurity is particularly serious for the developing countries especially sub-Saharan Africa where more people are suffering from hunger and this situation is expected to deteriorate in the future [2]. The challenge of safely and securely feeding these people, has to be faced in a world with a shrinking arable

© 2016 The Author(s). Licensee InTech. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and eproduction in any medium, provided the original work is properly cited. © 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

land, with less and more expensive fossil fuels, increasingly limited supplies of water, social unrest, economic uncertainty and within a scenario of a rapidly changing climate. Moreover the impact of plant diseases cannot be overestimated. The impact of fungal diseases and new variants of existing pathogens on agriculturally important crops is considered to be one of the main threats to worldwide food availability and safety. It was figured that diseases on our most important agricultural crops resulted in damages that were enough to feed 8.5% of the world's population [3]. The mission of providing food to the growing world population can therefore not be accomplished without a good control of these plant diseases. An important group of plant pathogens are toxigenic plant pathogens which produce mycotoxins, secondary metabolites of unrelated chemical structures and biological properties with a very broad toxic effects to humans and livestock, so in addition to posing a threat for food security, these pathogens also pose a threat to food safety [4–6].

Management of plant diseases can be done by adopting several strategies such as the cultivation of resistant cultivars, the use of sound crop rotation schemes and the use of chemical control. The harmful impact of plant protection products on the environment and human and animal health have prompted the European Union (EU Directive 2009/128/EC) to encourage research on alternative and ecofriendly solutions such as integrated pest management and the use of biological control agents (BCAs). Biological control, henceforth called biocontrol, in plant pathology, aims at utilizing microorganisms to prevent the colonization and/or suppress the spread of harmful plant pathogens [7]. BCAs in this chapter are defined as beneficial microorganisms that are able to antagonize plant pathogens and protect the plant [8–11]. Although the definition includes both pre-harvest and post-harvest strategies, this chapter will focus on pre-harvest biocontrol measures [12, 13].

due to borders rejection when mycotoxin concentrations exceed the maximum permissible levels. Although the production of mycotoxins by these toxigenic plant pathogens is of economic importance, many research groups do not take them into account when studying biological control strategies. These studies are then limited to the fungicidal or fungistatic effects of the BCAs while the effect of the BCAs on mycotoxin production is often overlooked. Figure 2A subscribes this issue and shows the number of papers on mycotoxigenic fungi with and without considering mycotoxins under in vitro, greenhouse and field conditions over the last 30 years. The figures presented in Figure 2A are even an underestimation, as they comprise research on A. flavus (Figure 2B). Many of these papers deal with "Aflasafe" and all include aflatoxin measurements. Omitting these A. flavus data provides a more correct view on the lack of studies investigating the effects of BCAs on mycotoxin

Figure 1. Overview of the number of papers published between 1989 and 2017 which use biological control strategies

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In view of the importance of mycotoxins for animal and human health, this review will focus on the effect of BCAs on the mycotoxin production by toxigenic plant pathogenic fungi. In a first part, we will provide an overview on the diverse modes of action BCAs can have. Secondly, a more in depth insight into the effect of BCAs on production of the major mycotoxins is provided. Finally, we end by providing some perspectives for future research and

production (Figure 2C).

hurdles that might have to be taken.

against, mycotoxigenic plant pathogenic fungi in different crops.

The most studied mycotoxin producing plant pathogenic genera are Fusarium, Alternaria, Claviceps, Stachybotrys and Aspergillus spp. [4, 14–16]. These genera infect a wide array of commodities including cereals, nuts, beans, sugarcane, and sugar beet in the field (e.g. Fusarium, Alternaria and Claviceps spp.) and/or during storage (e.g. Aspergillus spp.). Figure 1 illustrates, in term of biological control, the most studied mycotoxigenic fungi in pre-harvest in different crops. Fusarium graminearum is a predominant pathogen in wheat and maize, Fusarium verticillioides contaminates maize while Aspergillus flavus infects groundnuts and maize. Other mycotoxigenic plant pathogens such Alternaria alternata, Claviceps purpurea, and other members of the genera Fusarium (e.g. F. avenaceum, F. acuminatum, and F. proliferatum) and Aspergillus (e.g. A. carbonarius, A. niger, and A. parasiticus) received less attention in research to date.

Mycotoxins are ubiquitous in agricultural crops and their production occurs under certain environmental conditions during and/or after plant colonization [4, 17]. Exposure to mycotoxins either in a short and/or long term can lead to diverse toxic effects on a wide range of organisms [5, 6, 14, 17, 18]. Often, these fungal toxins are not only harmful for vertebrates and invertebrates (mycotoxins) but also for plants (phytotoxins). Economically, these natural contaminants hamper the international trade and significantly affect the world economy

Biological Control of Mycotoxigenic Fungi and Their Toxins: An Update for the Pre-Harvest Approach http://dx.doi.org/10.5772/intechopen.76342 61

land, with less and more expensive fossil fuels, increasingly limited supplies of water, social unrest, economic uncertainty and within a scenario of a rapidly changing climate. Moreover the impact of plant diseases cannot be overestimated. The impact of fungal diseases and new variants of existing pathogens on agriculturally important crops is considered to be one of the main threats to worldwide food availability and safety. It was figured that diseases on our most important agricultural crops resulted in damages that were enough to feed 8.5% of the world's population [3]. The mission of providing food to the growing world population can therefore not be accomplished without a good control of these plant diseases. An important group of plant pathogens are toxigenic plant pathogens which produce mycotoxins, secondary metabolites of unrelated chemical structures and biological properties with a very broad toxic effects to humans and livestock, so in addition to posing a threat for food security, these pathogens

Management of plant diseases can be done by adopting several strategies such as the cultivation of resistant cultivars, the use of sound crop rotation schemes and the use of chemical control. The harmful impact of plant protection products on the environment and human and animal health have prompted the European Union (EU Directive 2009/128/EC) to encourage research on alternative and ecofriendly solutions such as integrated pest management and the use of biological control agents (BCAs). Biological control, henceforth called biocontrol, in plant pathology, aims at utilizing microorganisms to prevent the colonization and/or suppress the spread of harmful plant pathogens [7]. BCAs in this chapter are defined as beneficial microorganisms that are able to antagonize plant pathogens and protect the plant [8–11]. Although the definition includes both pre-harvest and post-harvest strategies, this chapter will

The most studied mycotoxin producing plant pathogenic genera are Fusarium, Alternaria, Claviceps, Stachybotrys and Aspergillus spp. [4, 14–16]. These genera infect a wide array of commodities including cereals, nuts, beans, sugarcane, and sugar beet in the field (e.g. Fusarium, Alternaria and Claviceps spp.) and/or during storage (e.g. Aspergillus spp.). Figure 1 illustrates, in term of biological control, the most studied mycotoxigenic fungi in pre-harvest in different crops. Fusarium graminearum is a predominant pathogen in wheat and maize, Fusarium verticillioides contaminates maize while Aspergillus flavus infects groundnuts and maize. Other mycotoxigenic plant pathogens such Alternaria alternata, Claviceps purpurea, and other members of the genera Fusarium (e.g. F. avenaceum, F. acuminatum, and F. proliferatum) and Aspergillus (e.g. A. carbonarius, A. niger, and A. parasiticus) received less attention in research

Mycotoxins are ubiquitous in agricultural crops and their production occurs under certain environmental conditions during and/or after plant colonization [4, 17]. Exposure to mycotoxins either in a short and/or long term can lead to diverse toxic effects on a wide range of organisms [5, 6, 14, 17, 18]. Often, these fungal toxins are not only harmful for vertebrates and invertebrates (mycotoxins) but also for plants (phytotoxins). Economically, these natural contaminants hamper the international trade and significantly affect the world economy

also pose a threat to food safety [4–6].

60 Mycotoxins - Impact and Management Strategies

focus on pre-harvest biocontrol measures [12, 13].

to date.

Figure 1. Overview of the number of papers published between 1989 and 2017 which use biological control strategies against, mycotoxigenic plant pathogenic fungi in different crops.

due to borders rejection when mycotoxin concentrations exceed the maximum permissible levels. Although the production of mycotoxins by these toxigenic plant pathogens is of economic importance, many research groups do not take them into account when studying biological control strategies. These studies are then limited to the fungicidal or fungistatic effects of the BCAs while the effect of the BCAs on mycotoxin production is often overlooked. Figure 2A subscribes this issue and shows the number of papers on mycotoxigenic fungi with and without considering mycotoxins under in vitro, greenhouse and field conditions over the last 30 years. The figures presented in Figure 2A are even an underestimation, as they comprise research on A. flavus (Figure 2B). Many of these papers deal with "Aflasafe" and all include aflatoxin measurements. Omitting these A. flavus data provides a more correct view on the lack of studies investigating the effects of BCAs on mycotoxin production (Figure 2C).

In view of the importance of mycotoxins for animal and human health, this review will focus on the effect of BCAs on the mycotoxin production by toxigenic plant pathogenic fungi. In a first part, we will provide an overview on the diverse modes of action BCAs can have. Secondly, a more in depth insight into the effect of BCAs on production of the major mycotoxins is provided. Finally, we end by providing some perspectives for future research and hurdles that might have to be taken.

2. Modes of action of BACs

virulence or kill the pathogenic fungi.

by occupying the same niche [26, 27].

one which eventually causes death of the host pathogen [28–30].

thereafter curtails the growth or kills the pathogen.

A. Enzymes hydrolyzing fungal cell wall

defense responses, thus enhancing resistance against plant pathogens [31, 32].

genic fungi in each crop.

2.1. Antibiosis

the medium [38].

The main modes of action of BCAs are antibiosis, competition, mycoparasitism, and stimulation or enhancement of plant defense [7]. BCAs usually relay on more than one mode of action to antagonize the pathogen i.e. presence of one dominant mode of action does not exclude the others. Table 1 summarizes the reported modes of action used against mycotoxi-

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(i) Antibiosis encompasses the production of secondary metabolites such as antibiotics [19–21], lytic enzymes [22] and other proteins [23] that are able to suppress the growth, weaken the

(ii) Competition occurs when two or more fungi compete for the same essential nutrients required for their growth and development [24, 25]. Another type of competition is exclusion

(iii) Mycoparasitism or hyperparasitism is a direct parasitic attack of one fungus by another

(iv) Colonization of the plant, by beneficial micro-organisms can trigger local or systemic

Production of a wide range of antibiotics, enzymes and other antifungal compounds which contribute to adverse impacts on plant pathogen are characteristic features of different fungal BCAs such as Trichoderma spp. and Clonostachys spp. [8, 11, 24, 33]; bacterial BCAs such as Bacillus spp., Pseudomonas spp., Streptomyces spp. and Lactobacillus spp. [19, 20, 34, 35]; and yeast BCAs such as Cryptococcus spp., Kluyveromyces spp. and Saccharomyces spp. [10, 36]. All these BCAs have an arsenal of metabolites targeting different structures of the pathogen which

The fungal cell wall is a complex structure containing mainly glucan polymers and chitin. For several BCAs, molecules which interfere with this cell wall have been described. Peptaibols, linear oligopeptides produced by Trichoderma spp., inhibit beta-glucan synthase which prevents the pathogen from reconstructing its cell wall [37]. Culture filtrates of a T. harzianum isolate changed the colony color of A. flavus and had a clear effect on the growth. A microscope study showed alterations in the morphology of A. flavus represented by abnormal vesicle formation and various aberrant conidial heads reflecting cell wall deformity [38]. Production of some extracellular enzymes (amylolytic, cellulolytic, pectinolytic, lipolytic and proteolytic) were also demonstrated, however the inhibition was directly associated with source of carbon (glucose or sucrose) or nitrogen (L-alanine or other) available in

Figure 2. Number of published papers between the period of 1988–2017 addressing biocontrol of mycotoxigenic fungi with and without considering the effect on mycotoxins.
