2.3. Mycoparasitism

B. Production of metabolites that affect fungal membrane

64 Mycotoxins - Impact and Management Strategies

F. graminearum [19].

and cell wall effects

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.

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

C. Production of antifungal compounds having antibiotic effects not related to membrane

Where antibiotics have been described as powerful allies in the battle against bacterial contaminants, several molecules have been described which are fungicidal. The polyketide compound 2,4-diacetylphloroglucinol (DAPG) produced by P. fluorescens has received a particular consideration due to the broad spectrum activity against various fungal pathogens [43–46]. The molecule was isolated from Pseudomonas spp. strain F113 present in the rhizosphere of sugar beets [46] and has later been isolated from the rhizosphere of different crops [47]. DAPG has

Although antibiosis has been proven to be a major weapon against plant pathogenic, fungal resistance might arise. One example is known for F. verticillioides in which a Lactamase encoding gene (FVEG\_08291) has been identified which enables the pathogen to resist benzoxazinoid phytoanticipins produced in plant but also possibly microbial xenobiotic lactam compounds [49]. This information therefore raises an important question about the ability of mycotoxigenic plant pathogens to cope with the antifungal compounds produced by BCAs. In case that reported fungal resistance may be present against BCAs, this may

Competition for niche or competitive exclusion is a restriction of access to the habitat of a pathogen on the plant or seeds by another microorganism while competition for nutrients happens when two or more microorganisms compete for the same source of macro- and

One of the most famous and promising examples on competition for ecological niche and nutrition is found in A. flavus control [26]. However, competition of other mycotoxigenic pathogens such as F. pseudograminearum through nutrient competition [50] and F. culmorum and F. graminearum [51] were also reported. It has been demonstrated that atoxigenic A. flavus

micro-nutrients required for growth and secondary metabolites production [7].

been shown to have antifungal effects against Fusarium and Alternaria spp. [48].

necessitate the continuous exploration of new antibiotics.

2.2. Competition for niche and nutrition

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

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 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 pathogen [24].

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

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

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

changes in plants and protect the plants from diseases and abiotic stresses [97].

by mycotoxin producing fungi were scarcely studied [107, 108].

Pistachio nuts

Mode of action of BCAs

Alternaria alternata Wheat ✓ ✓✓ [48, 107]

Aspergillus terreusHAP1 Apple ✓ ✓✓ [110]

for niche / nutrients

Peanuts ✓ ✓✓ [58–61, 66, 115–119] Maize ✓ ✓✓ ✓ [27, 55, 56, 65, 67, 84, 95, 118,

Rice ✓ ✓✓ [75, 109]

carbonarius Grape ✓ ✓ [111, 112] flavus Cottonseed ✓ [52–54]

niger Peanuts ✓ [125]

parasiticus Peanuts ✓ [59, 60]

acuminatum Maize ✓ [126]

Fusarium Maize ✓ [121]

Grape ✓ ✓ [111]

Sorghum ✓ [126]

Indirect through the plant

✓ ✓ [113, 114]

References

http://dx.doi.org/10.5772/intechopen.76342

67

120–124]

Pathogen Host Mycoparasitism Antibiosis Competition

Trichoderma spp. have mostly been tested as a BCA against F. graminearum in wheat [38, 51, 76–78]. In a field trial, T-22 strain, reduced formation of perithecia of F. graminearum by 70% [77].

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 cell wall of F. culmorum [81].

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.
