2.4. Indirect through the plant

Enhancement of systemic plant resistance using plant growth-promoting rhizobacteria, which results an effective protection against a broad spectrum of pathogens, has been well described [85–87]. P. fluorescens is known to produce various plant growth regulators such as indole acetic acid, gibberellins and cytokinins which interfere with plant signaling [88]. In addition, it also produces antibiotics, volatile compounds, enzymes [21, 89]. The production of indole-3 acetic acid by P. fluorescens MPp4 is triggered by the presence of some pathogens such as F. verticillioides M1 which in turn contributes into its antagonistic activity [90]. P. fluorescens CHA0 prevented the carbon diversion and plant biomass reduction due to F. graminearum infection in barley [91]. The antagonistic activity of P. fluorescens MKB158 against F. culmorum was documented by Khan et al., however, the author mentioned that an indirect effect through enhancement of the plant systemic resistant is involved in the antagonistic activity [92]. Lysobacter enzymogenes strain C3 exerts also its biocontrol effect though induction of resistance in wheat against F. graminearum beside the production of lytic enzymes [93]. Effective reduction of the pathogen after heat treatment of C3 broth cultures to inactivate the bacterial cells and lytic enzymes was a confirmation for the presence of some fungal elicitors.

Besides rhizobacteria, the fungus T. harzianum, while, has also been shown to promote plant growth, increase nutrient availability and enhance the resistance against fungal diseases through colonization of plant roots [24, 37, 70]. Extensive research has been done to use Trichoderma spp., against F. verticillioides [94], F. graminearum [78] and A. flavus [95]. T. harzianum was reported to limit F. verticillioides in maize through the induction of systemic resistance by inducing ethylene and jasmonate signaling pathways [96]. Recently, novel species of Trichoderma (T. stromaticum, T. amazonicum, T. evansii, T. martiale, T. taxi and T. theobromicola) are classified as true endophytes as they have been reported to invade the plant tissue away from the root and induce transcriptomic changes in plants and protect the plants from diseases and abiotic stresses [97].

electron microscopic observations. The same experimental setup was previously done using the same BCA on rice but against Alternaria alternata and similar results and conclusions were reported [75]. Upon fungal cell wall degradation by chitinases produced by Trichoderma spp., another type of enzymes called exochitinases are secreted and the attack starts to kill the

Trichoderma spp. have mostly been tested as a BCA against F. graminearum in wheat [38, 51, 76–78].

Clonostachys is another genus famous for mycoparasitism and demonstrates a promising BCA against a wide range of plant pathogens including F. graminearum, F. verticillioides, F. poae, and F. culmorum. However, compared to Trichoderma, Clonostachys spp. are poorly studied. Within Clonostachys spp., C. rosea is the most researched and has been associated with multiple modes of action such as antibiosis [33], induction of plant resistance, [79], and niche and nutrient competition [80]. The fungus C. rosea secretes a number of antibiotics such as peptaibols, gliotoxin, trichoth as well as cell wall degrading enzymes such as chitinases, glucanases. C. Rosa ACM941 was reported to produce chitin-hydrolysing enzymes capable of degrading

Recently, Sphaerodes spp. have been discovered as a potential biocontrol agent against Fusarium spp. relying on mycoparasitism tactics with promising results. Among these species Sphaerodes mycoparasitica was isolated in association with Fusarium spp. from wheat and asparagus fields [82] and has shown its ability to limit Fusarium infection in both 3-ADON and 15-ADON chemotypes and limit DON synthesis both in vivo and in planta [82, 83]. For bacterial BCAs, Palumbo et al. [84] reported the production of antifungal metabolites and chitinase by P. fluorescens (strains JP2034 and JP2175) which had negative effects on the growth of A. flavus and F. verticillioides.

Enhancement of systemic plant resistance using plant growth-promoting rhizobacteria, which results an effective protection against a broad spectrum of pathogens, has been well described [85–87]. P. fluorescens is known to produce various plant growth regulators such as indole acetic acid, gibberellins and cytokinins which interfere with plant signaling [88]. In addition, it also produces antibiotics, volatile compounds, enzymes [21, 89]. The production of indole-3 acetic acid by P. fluorescens MPp4 is triggered by the presence of some pathogens such as F. verticillioides M1 which in turn contributes into its antagonistic activity [90]. P. fluorescens CHA0 prevented the carbon diversion and plant biomass reduction due to F. graminearum infection in barley [91]. The antagonistic activity of P. fluorescens MKB158 against F. culmorum was documented by Khan et al., however, the author mentioned that an indirect effect through enhancement of the plant systemic resistant is involved in the antagonistic activity [92]. Lysobacter enzymogenes strain C3 exerts also its biocontrol effect though induction of resistance in wheat against F. graminearum beside the production of lytic enzymes [93]. Effective reduction of the pathogen after heat treatment of C3 broth cultures to inactivate the bacterial cells and

Besides rhizobacteria, the fungus T. harzianum, while, has also been shown to promote plant growth, increase nutrient availability and enhance the resistance against fungal diseases through

lytic enzymes was a confirmation for the presence of some fungal elicitors.

In a field trial, T-22 strain, reduced formation of perithecia of F. graminearum by 70% [77].

pathogen [24].

66 Mycotoxins - Impact and Management Strategies

cell wall of F. culmorum [81].

2.4. Indirect through the plant

Another approach to enhance the plant resistance is through colonization. Extensive research is being done to discover endophytic microorganisms which colonize plant (tissue) without harming the plant [98] to reduce the plant diseases and mycotoxins in crops [99–103]. Endophytes can enhance plant growth and fitness, and offer protection against biotic and abiotic stresses by inducing plant defense responses. However, it should be noted that some of them are pathogenic to the plant in some phases of their lifecycle or under certain environmental conditions [98]. Some endophytes exert its role to enhance the host immune system against several fungal pathogens through the improvement of the nutrient uptake from the soil such as Piriformospora indica, a cultivable root fungal endophyte belonging to the order Sebacinales in Basidiomycota [104, 105]. The ability of Piriformospora indica to protect barley from root rot caused by F. graminearum was confirmed [103]. This was supported by a positive correlation between the relative amount of fungal DNA and disease symptoms and the absence of an inhibition on the growth of F. graminearum when co-inoculated with Piriformospora indica in an in vitro assay. Another endophyte such as Epicoccum nigrum has also proven its biocontrol activity against several plant pathogens [106], however it is ability to control diseases caused by mycotoxin producing fungi were scarcely studied [107, 108].



3. Biocontrol and mycotoxins

Fusarium head blight (FHB) and Fusarium ear rot (FER) are two of the most serious diseases affecting wheat and maize respectively throughout the world [130, 131, 139]. Over the last few years, FHB was predominantly caused by three species of Fusarium: F. graminearum, F. avenaceum and F. culmorum [108, 159] while FER is mainly caused by F. verticillioides, F. proliferatum, F. subglutinans, and F. graminearum [154, 156]. However FHB mostly occurs as a complex of several species [14, 160]. Each disease has multi-destructive effects on the crop through reducing the yield and grain quality. Over 180 types of trichothecenes are produced by Fusarium spp. contaminating mainly agricultural staples such as maize, wheat, and barley [14, 15]. The most prominent members are deoxynivalenol (DON), nivalenol (NIV) and T-2 Toxin. The biochemical importance of DON for fungal growth and development is not fully clear yet; however, it may have an important role during fungal infection and colonization and act as a virulence factor [160]. In animals, DON interferes with the cellular protein synthesis and clinically causing animal feed refusal and vomiting while NIV may induce genotoxic effect and leucopenia on long term exposure [4, 5, 17]. T-2 toxin triggers apoptosis to immune cells [161]. Due to the complexity of the life cycle of Fusarium spp., researchers mostly tried two application strategies to biologically control the disease, treatment of the crop residue with the antagonist or treatment of wheat ears at anthesis [162]. Most of the performed experiments used bacterial BCAs rely on antibiosis mainly to control the diseases and DON level. Less research discussed the effect of BCAs on

Biological Control of Mycotoxigenic Fungi and Their Toxins: An Update for the Pre-Harvest Approach

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An isolate of Trichoderma, T. gamsii 6085, was selected as a potential antagonist against F. culmorum and F. graminearum. The strain exhibited the capacity to negatively affect DON production by both pathogens up to 92% [72]. A field experiment on winter wheat for two seasons was conducted to evaluate the efficacy of different BCAs against ear blight and associated DON presence. Two strains of F. equiseti were the best performing strains and decreased the mycotoxins level produced by F. culmorum and F. graminearum by 70 and 94%, respectively. However, low levels of NIV in the cereals treated with F. equiseti were detected [51]. Recently, Piriformospora indica has proven its promising ability to reduce the severity the disease caused by F. graminearum and mycotoxin DON contamination in wheat by 70–80% and increase the total grain weight of F. graminearum-inoculated samples by 54% [100]. Novel bacterial endophytes predicted to be Paenibacillus polymyxa and Citrobacter were able to detoxify DON in vitro, but the performance of some of these isolated strains under field condition or

Three stains of the yeast Cryptococcus spp. (Cryptococcus nodaensis OH182.9, Cryptococcus spp. OH 71.4, and Cryptococcus spp. OH 181.1) were tested in several field experiments and they could control the disease by 50–60% on susceptible winter wheat. However DON content was the same as control [137]. Later, the same group cultivated another strain, Cryptococcus flavescens OH 182.9, and applied it at early anthesis but found no effects on DON level [142]. Besides fungal and yeast BCAs, bacteria have also been used to control DON produced by F. graminearum in wheat [35, 139, 144, 163] and in maize [99]. A complete reduction in DON

3.1. Trichothecenes toxins

NIV [51] and T-2 toxin [107].

in green house has not been reported yet [99].

Table 1. Different modes of action used by BCAs against mycotoxigenic fungi.
