**4.4 Fungal endophytes**

### *4.4.1 Agriculturally important enzyme production*

Degradation of the dead soil biomass by fungal endophytic is a major step in bringing the utilized nutrients back to the ecosystem that improves soil quality. Endophytic fungi is reported to produce various extracellular hydrolases including cellulase, laccase, pectinase, phosphatase, lipase, xylanase, and proteinase as a resistance mechanism against pathogenic invasion [77] and to obtain nutrition from host as these enzymes break macromolecules such as lignin, sugar-based polymers, proteins, organic phosphate, and carbohydrates to micromolecules that are transported throughout the cells for metabolism and help in host symbiosis process [78]. Sunitha et al. [79] isolated and identified approximately 50 endophytic fungal strains having amylase, laccase, cellulase, pectinase, lipase and protease enzymes. Study conducted by He et al. [80] explained that endophytic fungal species have ability to decompose organic components, including lignin,

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cellulose, and hemicelluloses that facilitates nutrient cycling. Chathurdevi and Gowrie [81] reported that the endophytic fungi species isolated from medicinal plant *Cardiospermum halicacabum* can support plant growth to overcome the adverse conditions through producing different extracellular enzymes. Fungal chitinases enzyme have vital role in degradation and cycling of carbon and nitrogen from chitin molecule. Chitin molecule is a linear homopolymer of β-1,4N-acetylglucosamine can be obtained from insect's exoskeleton, crustacean's shells, and fungal cell wall. Many fungal endophytes isolated from leaves of trees of Southern India have shown the production of chitinases [82]. An endophyte, *Acremonium zeae*, isolated from maize is reported to produce the extracellular enzyme hemicellulase, which may be used in the bioconversion of lignocellulosic

Agricultural productivity is significantly threatened by various abiotic stresses. Environmental stresses such as drought, salinity, temperature can collectively cause more than 50% yield losses worldwide [84]. Plants can tolerate abiotic stress by two mechanisms: (i) via activation of response systems directly after exposure to stress [67] (ii) biochemical compounds that are synthesized by fungal endophytes, acts as anti-stress agents [85]. Experimental studies also confirmed that endophytic fungi can help the host plants from environmental stress conditions such as drought, salts, high temperatures and heavy metals and can thus increase the plant growth.

Among the abiotic stresses, water stress commonly, known as 'drought', is considered as one of the major challenges to crop production worldwide [86]. Drought has a negative impact on the plant growth rate, germination rates, membrane loss of its integrity, repression of photosynthesis, and increase in the productivity of reactive oxygen species [87, 88]. Fungal endophyte infected plants enhance drought tolerance by increased accumulation of solutes in tissues, or by reduced leaf conductance and a slowdown of the transpiration stream, or due to formation of thicker cuticle as compared to non-infected plants [67]. Chippa et al. [89] reported that endophytic, *Neotyphodium* spp. is reported to enhance drought tolerance in grass plant by stomatal and osmoregulations and protect plants in drought and nitrogen starvation. Experimental studies on lavender plants inoculated with *Glomus* spp. showed that these plants accumulated solutes in tissues thereby exhibiting better drought tolerance by improving water contents, N and P contents and root biomass [90, 91]. Moreover, plants harboring endophytes consumes significantly less water and had enhanced biomass than non-symbiotic plants. For instance, endophytes *Chaetomium globosum* and *P. resedanum* isolated from sweet pepper (*Capsicum annuum*) plants enhanced shoot length and biomass of the host plants challenged by drought stress [92, 93]. Similarly, Redman et al. [72] found that inoculation of endophytes *Fusarium culmorum* and *Curvularia protuberata* in drought-affected rice plants resulted in increased biomass than of non-inoculated plants. Fungal endophyte colonization also results in higher chlorophyll content and leaf area in plants under drought stress than non-colonized plant. Higher chlorophyll concentration is related with higher photosynthetic rate [94]. For instance, enhanced photosynthesis rate was recorded in drought stressed *C. annuum* plants

colonized by endophytes *C. globosum* [95] and *P. resedanum* [96].

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

biomass into fermentable sugars [83].

**5.1 Drought stress**

**5. Fungal endophytes: Abiotic stress management**

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

cellulose, and hemicelluloses that facilitates nutrient cycling. Chathurdevi and Gowrie [81] reported that the endophytic fungi species isolated from medicinal plant *Cardiospermum halicacabum* can support plant growth to overcome the adverse conditions through producing different extracellular enzymes. Fungal chitinases enzyme have vital role in degradation and cycling of carbon and nitrogen from chitin molecule. Chitin molecule is a linear homopolymer of β-1,4N-acetylglucosamine can be obtained from insect's exoskeleton, crustacean's shells, and fungal cell wall. Many fungal endophytes isolated from leaves of trees of Southern India have shown the production of chitinases [82]. An endophyte, *Acremonium zeae*, isolated from maize is reported to produce the extracellular enzyme hemicellulase, which may be used in the bioconversion of lignocellulosic biomass into fermentable sugars [83].

### **5. Fungal endophytes: Abiotic stress management**

Agricultural productivity is significantly threatened by various abiotic stresses. Environmental stresses such as drought, salinity, temperature can collectively cause more than 50% yield losses worldwide [84]. Plants can tolerate abiotic stress by two mechanisms: (i) via activation of response systems directly after exposure to stress [67] (ii) biochemical compounds that are synthesized by fungal endophytes, acts as anti-stress agents [85]. Experimental studies also confirmed that endophytic fungi can help the host plants from environmental stress conditions such as drought, salts, high temperatures and heavy metals and can thus increase the plant growth.

#### **5.1 Drought stress**

*Sustainable Crop Production*

**4.3 Fungal endophytes**

*4.3.1 Phytohormone production*

important parasitic nematode on banana.

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

Endophytes can actively or passively regulate the plant growth by solubilization of phosphate, enhance uptake of phosphorus (P), and/ or plant hormones such as auxin, abscisins, ethylene, gibberellic acid (GA), and indole acetic acid (IAA) [67, 68], among these Gibberellic acid is an important phytohormone. The phytohormone GA, a diterpenoid complex, controls the growth of plants, and promotes flowering, stem elongation, seed germination, and ripening [69, 70]. Fungal endophytes *Sebacina vermifera*, *Piriformospora indica, Colletotrichum* and *Penicillium* are distinguished to have better plant growth promoting effects under unfavorable conditions due to their ability to synthesize enzymes and bioactive metabolites [71–73]. Hamayun et al. [69] reported that fungal endophyte, *Cladosporium sphaerospermum* isolated from soybean plant (*Glycine max*) produced gibberellic acid that induced plant growth in rice and soybean. Metabolite pestalotin analogue, isolated from the endophytic *Pestalotiopsis microspora* exhibited significant gibberellin activity in winter-hazel seeds (*Distylium chinense*) and increased their germination rate [74]. Endophytes, *Fusarium tricinctum* and *Alternaria alternata* produced derivatives of plant hormone indole acetic acid that enhanced the plant growth [75]. A study conducted by Johnson et al. [76] on root colonizing endophyte *P. indica* found that association of fungal endophytes with roots modulated phytohormones involved with growth and development of host plant and enhanced nutrient uptake and translocation especially of phosphorus and nitrogen

Degradation of the dead soil biomass by fungal endophytic is a major step in bringing the utilized nutrients back to the ecosystem that improves soil quality. Endophytic fungi is reported to produce various extracellular hydrolases including cellulase, laccase, pectinase, phosphatase, lipase, xylanase, and proteinase as a resistance mechanism against pathogenic invasion [77] and to obtain nutrition from host as these enzymes break macromolecules such as lignin, sugar-based polymers, proteins, organic phosphate, and carbohydrates to micromolecules that are transported throughout the cells for metabolism and help in host symbiosis process [78]. Sunitha et al. [79] isolated and identified approximately 50 endophytic fungal strains having amylase, laccase, cellulase, pectinase, lipase and protease enzymes. Study conducted by He et al. [80] explained that endophytic fungal species have ability to decompose organic components, including lignin,

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from the soil.

**4.4 Fungal endophytes**

*4.4.1 Agriculturally important enzyme production*

Among the abiotic stresses, water stress commonly, known as 'drought', is considered as one of the major challenges to crop production worldwide [86]. Drought has a negative impact on the plant growth rate, germination rates, membrane loss of its integrity, repression of photosynthesis, and increase in the productivity of reactive oxygen species [87, 88]. Fungal endophyte infected plants enhance drought tolerance by increased accumulation of solutes in tissues, or by reduced leaf conductance and a slowdown of the transpiration stream, or due to formation of thicker cuticle as compared to non-infected plants [67]. Chippa et al. [89] reported that endophytic, *Neotyphodium* spp. is reported to enhance drought tolerance in grass plant by stomatal and osmoregulations and protect plants in drought and nitrogen starvation. Experimental studies on lavender plants inoculated with *Glomus* spp. showed that these plants accumulated solutes in tissues thereby exhibiting better drought tolerance by improving water contents, N and P contents and root biomass [90, 91]. Moreover, plants harboring endophytes consumes significantly less water and had enhanced biomass than non-symbiotic plants. For instance, endophytes *Chaetomium globosum* and *P. resedanum* isolated from sweet pepper (*Capsicum annuum*) plants enhanced shoot length and biomass of the host plants challenged by drought stress [92, 93]. Similarly, Redman et al. [72] found that inoculation of endophytes *Fusarium culmorum* and *Curvularia protuberata* in drought-affected rice plants resulted in increased biomass than of non-inoculated plants. Fungal endophyte colonization also results in higher chlorophyll content and leaf area in plants under drought stress than non-colonized plant. Higher chlorophyll concentration is related with higher photosynthetic rate [94]. For instance, enhanced photosynthesis rate was recorded in drought stressed *C. annuum* plants colonized by endophytes *C. globosum* [95] and *P. resedanum* [96].

#### **5.2 Salinity stress**

High salinity due to extreme climatic conditions and misuse of agricultural land over the past few decades has led to high salinity, which is a limiting factor to global agricultural productivity [97]. Soil salinity is the accumulation of water soluble salts in soil that affects its physical and chemical properties thereby reducing soil's agricultural output [98]. Reactive oxygen species (SOD, CAT, APX) are formed in plants on onset of salt and osmotic stress. Endophytic *Piriformospora indica* induces salt stress tolerance by elevation of antioxidant enzymes [99]. These are involved in the removal of reactive oxygen species either directly or indirectly via regeneration of ascorbate and glutathione in the cell. Experimental studies by Rodriguez et al. [100] reported that constant exposure of non-symbiotic plants dunegrass (*Leymus mollis*) to 500 mmol/l NaCl solution, became severely wilted and desiccated within 7 days and were dead after 14 days. In contrast, symbiotic plants infected with *F. culmorum* showed wilting symptoms only after they were exposed to 500 mmol/l NaCl solution for 14 days.

#### **5.3 Temperature stress (low and high)**

High temperature is a major obstacle in crop production that results in major cellular damage such as protein degradation and aggregation [101]. Whereas, low temperature can cause impaired metabolism due to inhibition of enzyme reactions, interactions among macromolecules, changes in protein structure, and modulating cell membrane properties [102]. Endophytic, *Curvularia* spp. is proven to confer thermal tolerance ability plants like tomato, watermelon, and wheat [103]. Herbal plant wooly rosette grass (*Dichanthelium lanuginosum*) that lives in the areas where soil temperatures can reach up to 57°C, the presence of endophytic fungi *Curvularia* sp. protects the plant from temperature stress better than endophyte free plants [104]. Experimental demonstration by Redman et al. [103] showed that grass *D. lanuginosum* survival in soil temperatures ranging between 38 and 65°C is directly linked to its association with the fungus *C. protuberata* and its mycovirus, *Curvularia* thermal tolerance virus (CThTV). Moreover, cold stress tolerance was conferred in germinated seeds of rice under laboratory conditions by *C. protuberata* isolated from *D. lanuginosum* thriving in geothermal soils [72].

#### **5.4 Heavy metal stress**

Heavy metal contamination due to increased industrialization has recently received attention because heavy metals cannot be itself degraded [105]. Toxicity by heavy metals can cause the loss of about 25–80% of various cultivated crops. Heavy metals being very toxic to roots of cultivated crop plants can cause poor development of the root system [106]. Endophytic fungi possess metal sequestration or chelation systems that increases tolerances of their host plants to heavy metals via enhancements of antioxidative system thereby changing heavy metal distribution in plant cells and detoxification of heavy metal, thus assisting their hosts to survive in contaminated soil [107, 108]. For instance, dark septate root endophytes (DSEs), *Phialocephala fortinii* can produce the black biopolymer melanin, which can be synthesized from phenolics and binds heavy metals [109] that keep heavy metal ions away from living, plant cells [110]. Siderophores being metal-chelating compounds [111, 112] released from roots into the rhizosphere can be helpful in inhibiting absorption of heavy metals into plant cells as siderophores can form complexes with heavy metals which are not easily absorbed by plant

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

enhance crop production and protection is also required.

roots. Yamaji et al. [113] recorded that endophytes *P. fortinii* and *Rhizodermea veluwensis* showed an ability to produce siderophores that probably affects heavy

Fungal endophytes can be a significant component of sustainable agriculture, being safe, cost-effective, have ability to produce various compounds like phytohormones, defensive compounds, solubilize phosphates, extracellular enzymes, siderophore production, inhibiting plant pathogens, and promoting plant growth. Over the last decade, sharp rise in study of fungal endophytes is seen as they hold huge potential in agricultural sector. However, most of the research on endophytes is still at an experimental level in lab or greenhouse. For permitting the practical use of these endophytes in agriculture it is extremely necessary to encourage field experiments to determine the effectiveness of the endophytes under real world conditions. Simultaneously, it is also necessary to build awareness of this new research field among farmers to improve interactions and collaboration with scientists working in different fields, thereby encouraging the adoption of endophytes in agriculture and maximizing their benefits. If endophytes become feasible in agricultural sector, their practical aspects will also have to be researched so that farmers can learn how to integrate these endophyte species within pre-existing eco-friendly agricultural methods so as to ensure continuity in the approach to sustainability. Moreover, scientific research has to be also focused on use of genetically modified endophytes made by combining endophytes having two or more different ecological roles, such as the suppression of diseases and insect pests to simultaneously improve plant yields and its defensive properties. Thus, optimization of microbial functions to

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

metal exclusion in the rhizosphere.

**6. Conclusion**

**Conflict of interest**

**Abbreviations**

No conflict of interest is indulged.

HPA 3-hydroxypropionic acid

APx ascorbate peroxidase

CThTV *Curvularia* thermal tolerance virus DSEs dark septate root endophytes

P phosphorus GA Gibberellic acid IAA indole acetic acid SOD superoxide dismutase

CAT catalase

roots. Yamaji et al. [113] recorded that endophytes *P. fortinii* and *Rhizodermea veluwensis* showed an ability to produce siderophores that probably affects heavy metal exclusion in the rhizosphere.
