**4.1 Fungal endophytes**

#### *4.1.1 Biocontrol agents*

Fungal endophytes act as biocontrol agents as they can protect their host plants from pathogens and pests [25, 26]. The mechanism whereby endophytes deter herbivory is through production of antiherbivory/bioactive compounds [27–29] or complex interacting factors of metabolic processes in both the fungus and the plant after infection [26, 30]. These defensive compounds may deter feeding (antixenosis) or reduce insect performance (antibiosis) [31, 32]. Endophytic fungi release the specialized biologically active compounds without any observable damage to their host tissues [33]. Defensive compounds may be categorized into various functional groups: alkaloids, terpenoids, isocoumarin derivatives, quinones, flavonoids, chlorinated metabolites, phenol and phenolic acids and many others [7, 34].


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**4.2 Fungal endophytes**

*4.2.1 Nematicidal agents*

*Fungal Endophyte-Host Plant Interactions: Role in Sustainable Agriculture*

spruce budworm, *Choristoneura fumiferana* (Clemens) larvae [54]. Two insect toxins, pimarane and diterpene were isolated from an unidentified endophytic fungus symbiotic with needle of *A. balsamea* [54]. Two benzofuran carrying normonoterpene derivatives, toxic to spruce budworm larvae were characterized from an endophytic culture obtained from wintergreen (*Gaultheria* 

3.**Isocoumarin derivatives:** Toxicity of isocoumarin related metabolites from the conifer endophyte cultures showed toxicity against cells and/ or larvae of

4.**Quinones:** Rugulosin, a metabolite of endophytic fungus *Hormonema dematioides* from balsam fir has been reported to have insecticidal activity [54]. An unidentified endophytic culture isolated from eastern larch (*Larix laricina*) produced a quinone derivative, which was toxic to spruce budworm larvae [55].

5.**Flavonoids:** Among the flavonoids, tricin and related flavone glycosides isolated from endophyte infected blue grass (*Poa ampla*) exhibited toxicity

6.**Chlorinated metabolites:** Insecticidal chlorinated metabolite, heptelidic acid chlorohydrins were isolated from cultures of balsam fir needle endophyte *Phyl-*

7.**Phenol and phenolic acids:** Phenol and phenolic acids are frequently detected in cultures of endophytes and have pronounced biological activities. Singh et al. [58] purified phenolic compound from ethyl acetate extract of endophytic *Cladosporium* sp. isolated from guduchi (*Tinospora cordifolia*), which induced significant mortality and adversely affected development and survival

Since the 1980s, there is accumulating evidence about factors that influence the outcome of grass–endophyte–insect interactions. Webber [59] was probably the first worker to report plant protection given by fungal endophyte *Phomopsis oblonga* in elm trees (*Ulmus* spp.) against the elm bark beetle, *Physocnemum brevilineum* (Say). Majority of studies for herbivore performance on native grass species symbiotic with endophytic fungi are more consistent showing negative effects including increased mortality [60], reduced mass [61, 62] and decelerated development time [63]. Afkhami et al. [62] reported that bird cherry oat aphid, *Rhopalosiphum padi* (Linnaeus) damaged more endophyte free nodding fescue (*Festuca subverticillata*) than endophyte symbiotic *F. subverticillata*, while positive effect of endophyte infection was reported on eastern lubber grasshopper, *Romalea guttata* (Houttuyn) that preferentially consumed endophyte symbiotic *F. subverticillata* over endophyte free. Similarly increase in growth rate was recorded in third to fifth instars of fall armyworm, *Spodoptera frugiperda*

(J.E. Smith) feeding on *N. coenophialum* infected tall fescue [63].

Fungal endophytes act as nematicidal agents as they are known to produce some compounds which are toxic to nematodes. Diedhiou et al. [64] demonstrated reduced

of tobacco cutworm, *Spodoptera litura* (Fabricius).

*DOI: http://dx.doi.org/10.5772/intechopen.92367*

*procumbens*) [55].

spruce budworm [56].

against mosquito larvae [56].

*losticta* spp*.* [57].

*Fungal Endophyte-Host Plant Interactions: Role in Sustainable Agriculture DOI: http://dx.doi.org/10.5772/intechopen.92367*

*Sustainable Crop Production*

**4.1 Fungal endophytes**

Fungal endophytes act as biocontrol agents as they can protect their host plants

from pathogens and pests [25, 26]. The mechanism whereby endophytes deter herbivory is through production of antiherbivory/bioactive compounds [27–29] or complex interacting factors of metabolic processes in both the fungus and the plant after infection [26, 30]. These defensive compounds may deter feeding (antixenosis) or reduce insect performance (antibiosis) [31, 32]. Endophytic fungi release the specialized biologically active compounds without any observable damage to their host tissues [33]. Defensive compounds may be categorized into various functional groups: alkaloids, terpenoids, isocoumarin derivatives, quinones, flavonoids, chlorinated metabolites, phenol and phenolic acids and many others [7, 34].

1.**Alkaloids:** Alkaloids are the first reported fungal metabolites to have insecticidal activity. Alkaloids produced by the fungus or by plant in response to fungal infection increase host resistance to herbivores [4, 35]. Endophyte infected grasses contain a variety of alkaloids such as peramines, ergot alkaloids, lolitrems, loline alkaloids and which are absent in non-infected conspecifics [36, 37]. Alkaloids are the first reported fungal metabolites to have insecticidal activity. Most of the alkaloids have been detected in the cultures of grass associated endophytic fungi, such as sexual *Epichloe* spp. and asexual *Neotyphodium* spp. Fungal isolate determines the types of alkaloids produced and plant/ fungal genotype interaction can modify the quantities of these alkaloids [38]. The alkaloids from fungal endophytes are categorized into three groups, amines and amides, indole derivatives and pyrrolizidines. Among amines and amides, peramine is toxic to insects without being harmful to mammals [39, 40]. It is a strong feeding deterrent for argentine stem weevil and several other insects [41, 42]. The levels of alkaloids and other toxins may be altered qualitatively depending on the plants physiological state. Ball et al. [43] verified that with plant aging, the amount of peramine decreases in leaves and reaches lower levels during inflorescence phase. The second group of amine and amide alkaloids is ergot alkaloids that also provide significant resistance against insect pests [44]. Feeding experiments with a variety of mammals indicate that ergot alkaloids have significant detrimental effects on mammalian health and reproduction [45, 46]. Among indole derivatives, the lolitrem C and F have been shown to confer resistance against a number of insect species [47]. Other indole derivatives namely chanoclavine, agroclavine and elymoclavine isolated from culture of *Neotyphodium* endophyte [34] were reported to be toxic to some insects and mammals [48]. Among Pyrrolizidines, the saturated aminopyrrolizidine alkaloids as norloline, N-formylloline, N-acetylnorloline, N-acetylloline were exclusively found in endophyte infected grasses of *F. arundinacea* (infected with *Neotyphodium coenophialum*) and *Festuca pratensis* (with *Neotyphodium uncinatum*) [49]. A number of feeding experiments have demonstrated the insecticidal and insect feeding deterrent activities of these lolines [50–52]. Lolines in addition to the well documented effect on insects are also nematicidal [53].

2.**Terpenoids:** Second group of endophytic toxins include terpenoids isolated from some endophytic cultures originating from a variety of host plants. Sesquiterpenes and diterpenes are among the identified terpenoids. Sesquiterpenes as of heptelidic acid and hydroheptelidic acid isolated from *Phyllosticta* sp., an endophytic fungus of balsam fir (*Abies balsamea*) exhibited toxicity to

*4.1.1 Biocontrol agents*

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spruce budworm, *Choristoneura fumiferana* (Clemens) larvae [54]. Two insect toxins, pimarane and diterpene were isolated from an unidentified endophytic fungus symbiotic with needle of *A. balsamea* [54]. Two benzofuran carrying normonoterpene derivatives, toxic to spruce budworm larvae were characterized from an endophytic culture obtained from wintergreen (*Gaultheria procumbens*) [55].


Since the 1980s, there is accumulating evidence about factors that influence the outcome of grass–endophyte–insect interactions. Webber [59] was probably the first worker to report plant protection given by fungal endophyte *Phomopsis oblonga* in elm trees (*Ulmus* spp.) against the elm bark beetle, *Physocnemum brevilineum* (Say). Majority of studies for herbivore performance on native grass species symbiotic with endophytic fungi are more consistent showing negative effects including increased mortality [60], reduced mass [61, 62] and decelerated development time [63]. Afkhami et al. [62] reported that bird cherry oat aphid, *Rhopalosiphum padi* (Linnaeus) damaged more endophyte free nodding fescue (*Festuca subverticillata*) than endophyte symbiotic *F. subverticillata*, while positive effect of endophyte infection was reported on eastern lubber grasshopper, *Romalea guttata* (Houttuyn) that preferentially consumed endophyte symbiotic *F. subverticillata* over endophyte free. Similarly increase in growth rate was recorded in third to fifth instars of fall armyworm, *Spodoptera frugiperda* (J.E. Smith) feeding on *N. coenophialum* infected tall fescue [63].

#### **4.2 Fungal endophytes**

#### *4.2.1 Nematicidal agents*

Fungal endophytes act as nematicidal agents as they are known to produce some compounds which are toxic to nematodes. Diedhiou et al. [64] demonstrated reduced nematicidal activity by an endophytic fungus, *Fusarium oxysporum*, against the plant parasitic nematode *Meloidogyne incognita* in tomato plant. Schwarz et al*.* [65] reported that several endophytic fungi isolated from above-ground plant organs produced bioactive compound, 3-hydroxypropionic acid (HPA) extracted by bioactivity-guided fractionation of fungal extracts that showed selective nematicidal activity against *M. incognita* with LD50 values of 12.5–15 μg/ml. Similarly, Felde et al. [66] found that combined inoculations of endophytic fungal isolates *Trichoderma atroviride* and *F. oxysporum* is considered an alternative to improve and increase banana yield that reduces the population of burrowing nematode, *Radopholus similis* (Cobb), an important parasitic nematode on banana.

### **4.3 Fungal endophytes**
