B. Production of metabolites that affect fungal membrane

Production of antifungal metabolites interfering with membrane structures have been described in several BCAs. The most important class is the lipopeptides which interfere with the membrane and the sterols in the membrane [39]. These lipopeptides have been proven to be effective against several genera of toxigenic fungi such as Aspergillus and Fusarium spp.

strains are powerful BCAs to control the toxigenic strains of A. flavus in cottonseed [52–54], maize [27, 55–57] and various types of nuts [58–61]. Currently, different strains of atoxigenic A. flavus are being used depending on the endemic area and sometimes a mixture of strains is used in the field. This competitive exclusion theory has been recently confirmed in situ by coinoculating corn kernels with GFP-labeled AF70 and wild-type AF36. The study showed that there is a population difference (up to 82% reduction) between the co-inoculated kernels with both fungi and the control one inoculated only with GFP-labeled AF70 after visualizing under UV. Furthermore, aflatoxins (AFs) analysis showed a 73% reduction compared to the control [62]. However, AFs are not the only toxic compounds produced by A. flavus. Cyclopiazonic acid (CPA) is another mycotoxin produced by certain strains of A. flavus, including the atoxigenic strains, affecting mainly the liver and muscles of livestock [63, 64]. As an example, the commercially registered BCAs AF36, while it is effective against toxigenic A. flavus, it has been confirmed for its CPA production in cottonseeds. Therefore, researchers screened and tested new strains lacking the production of both toxins for the same previously mentioned crops [65–67]. Testing atoxigenic strains of A. flavus against other AFs producing fungi such as A. parasiticus was less common because A. parasiticus is less virulent and not predominantly

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

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Competition for nutrient and niche can also be seen in Trichoderma and Clonostachys spp. when they are applied before pathogen occurrence [11, 68]. Trichoderma spp., especially T. harzianum, produce siderophores, low-molecular-mass ferric-iron-specific chelators, when the available iron in the environment is low [23]. Siderophores chelate the oxidized ferric ions (Fe + 3) making it available as an iron source [24, 37, 69] and this enables Trichoderma spp. to compete for iron which is an essential element for the development of many plant pathogens [24, 68].

Mycoparasitism is a direct parasitic relationship between one fungus and another fungal host [24]. The mycoparasitic interaction is mediated through certain gene involved in synthesis of some metabolites (mainly chitinases, glucanases, and proteases) allowing the parasitic fungi to degrade and invade the host cells [24, 29, 70]. A wide array of BCAs employ this strategy to compete against several mycotoxigenic pathogens especially against Fusarium spp. Among these, Trichoderma spp., are a widespread mycoparasitic BCA naturally present in the soil and the plant [11, 70, 71]. The fungi are mainly biotrophic, perform mycoparasitic interaction with living fungi, although the species also compete for niche and nutrients, enhance the plant systemic and localized resistance and secrete secondary antifungal metabolites [29, 68]. Upregulation of some chitinase-encoding genes occurred upon mycoparasitic contact of Trichoderma spp. with Fusarium [71, 72]. T. viride showed a potent antagonisms of F. verticillioides in an in vitro assay which was proven by the suppression of radial extension of the fungus by 46% after

On rice, T. harzianum performed very well against F. verticillioides through mycoparasitism and showed a mutual antagonism by contact [74]. Some metabolites such as cell wall-degrading enzymes, chitinases and ß-1,3 glucanases were suggested by the author to be involved in the mechanism as the evidence of mycoparasitism in this study was supported by cryo scanning

occurs in the soil as A. flavus [59].

6 days and by 90% after 14 days [73].

2.3. Mycoparasitism

The presence of two antibiotic lipopeptides, iturin and surfactin, revealed the potent antifungal activity [20] of two Bacillus spp. (P1 and P11) against A. flavus [40]. Similarly, B. subtilis BS119m was able to completely inhibit A. flavus growth which was associated to its ability to produce a high amount of surfactin [41]. Crane et al. monitored iturins produced by B. amyloliquefaciens in wheat under greenhouse and the field conditions and found an inverse relationship between iturins levels and Fusarium disease incidence [42]. Fengycin, another lipopeptide purified from Bacillus subtilis IB culture showed an inhibitory effect against F. graminearum [19].
