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Aptitude of endophytic microbes for production of novel biocontrol agents and industrial enzymes towards agro-industrial sustainability

Beni-Suef University Journal of Basic and Applied Sciences volume 10, Article number: 61 (2021) Cite this article

Abstract

Background

Endophytes have continued to receive increased attention worldwide, probably, due to the enormous biotechnological potentials spanning through various industrial sectors. This paper outlines the biotechnological potentials of endophytes in biocontrol and industrial enzyme production, and the possible contribution towards achieving agro-industrial sustainability using published articles on endophytes in both Web of Science and Scopus (1990–2020).

Main body of the abstract

This review discusses the potential of endophytes to produce novel secondary metabolites with effective biocontrol activity against insect pests and plant pathogens. More so, the aptitude of endophytes for production of a wide range of enzymes with potential applications in agriculture, energy and health is discussed in this review. Furthermore, this review highlights the emerging potentials of endophytes in the production of exopolysaccharide and fatty acids. This paper also advocates the need for bioprospecting endophytes for novel biocontrol agents against termites, which are known for causing significant damage to forest and stored products.

Short conclusion

Exploration of endophytes for biocontrol and production of biomolecules of industrial significance could contribute significantly towards agricultural and industrial sustainability.

1 Background

One of the fundamentals of Sustainable Development Goals (SDGs) as set by the United Nations (UN) is to achieve food security and engender agricultural sustainability by 2030. A major challenge confronting food security globally is the activity of insect pests and plant diseases, with resultant negative implications on annual agricultural produce, hence threatening food security. Achieving zero hunger with increasing world’s population necessitates an increase in annual agricultural productivity globally. It is, therefore, important to take proactive steps towards improving crop yield. Unarguably, effective control of crop pests and phytopathogens is vital to improving crop yield. Even though, there are efficient chemical methods for pest control, the approaches are accompanied by possible health risks [1]. Thus, biological control of pest and pathogens is a promising alternative as the method is environmentally-friendly with limited health hazards.

Interestingly, endophytes hold great dexterity for biological control of phyto-diseases as the microbes protect their host plants from pathogens’ attack through antagonism [2, 3]. The microbes have also displayed abilities for production of secondary metabolites with antimicrobial activity [4], which could be explored for biocontrol of different pathogens. Moreover, endophytes produce some enzymes as a defence response mechanism of the host against pathogens while other enzymes from endophytes promote plant growth [5, 6]. Thus, bioprospecting endophytes for production of novel biocontrol agents will contribute significantly towards improving agricultural productivity.

Furthermore, some studies have implicated endophytes in the production of enzymes of industrial significance including amylase, cellulase, lipase and laccase [7]. Specifically, Bezerra et al. [8] reported the potential of various endophytic fungi in a Brazilian medicinal plant, Bauhinia forficate for the production of some extracellular and hydrolytic enzymes such as cellulases and xylanases, with potential applications in biorefinery. The ability of endophytes to produce lignocellulolytic enzymes (Laccase, cellulases, xylanases etc.) is significant to achieving affordable and clean energy, which is the seventh of the SDGs. While ligninolytic enzymes play the role of delignification during pretreatment of feedstock for biofuel production, cellulases are responsible for cellulose hydrolysis, which enables the release of fermentable sugars during biofuel production. The complementary roles of these enzymes would indeed promote sustainable energy through optimum utilization of renewable biomass as feedstock for biofuel production. Besides, discovery of endophytes with exceptional ability for improved enzyme production would favour industrial sustainability since poor enzyme yield is a major problem militating against industrial application of enzymes. Undoubtedly, exploration of endophytes for biocontrol and production of industrial enzymes could contribute positively towards agricultural and industrial sustainability (Fig. 1). This review, therefore, brings to the fore scientific evidences that attest to the prospect of endophytes in biocontrol and production of industrial biomolecules with the possible implication on SDGs.

Fig. 1
figure 1

Scheme of endophytes potentials in biocontrol and production of biomolecules

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2 Main text

2.1 Endophyte articles identification strategy

The study identified endophyte-related research articles hosted in WoS and Scopus within the timespan 1990–2020 (07/07/2020). The articles were identified using the term ‘endophyt*’ for inclusion of different indexes including ‘endophyte’, ‘endophytes’, and ‘endophytic’ restricted to the title-field. The retrieved article sets were finally limited to primary research articles, downloaded in CSV format and de-duplicated in ScientoPy package [9]. The topics of interest related the objectives of the review were mined from the processed article datasets based on the average growth rate or relevant author-keywords using Eq. 1 [9]:

$${\text{Topic}}\,\left( {{\text{average}}\,{\text{growth}}\,{\text{rate}}} \right) = \left( {\mathop \sum \limits_{{i = 2017_{b} }}^{{2020_{c} }} {\text{AS}}_{i} - {\text{AS}}_{i - 1} } \right)/\left( {2020_{c} - 2017_{b} } \right) + 1$$
(1)

2017b = start year; 2020c = end year; ASb = number of endophyte-related articles connected to sustainable biocontrol, enzyme and biomolecule production in 2017; ASc = number of endophyte-related articles related to sustainable biocontrol, enzyme and biomolecule production in 2020.

The topics considered include biocontrol potential (biological control, pest control, parasitoidal, biopesticidal, microbial control) and enzymes (glucoamylase, laccase, xylanase, 1-aminocyclopropane-1-carboxylate deaminase, alpha-amylase, alpha-glucosidase, ascorbate peroxidase, beta-glucosidase, chitinase, inulinase, L-asparaginase, asparaginase, glucuronidase, hemicellulose, keratinase, lipase, cellobiohydrolase, glutaminase, amylase, endoglucanase, protease, oxalate oxidase, polyphenol oxidase, glucanase), fatty acid and polysaccharide (fatty acid, polysaccharide, exopolysaccharide). The discussion was limited to recent studies under various subtopics.

2.2 Bioprospecting endophytes for agricultural sustainability and food security

There is plethora of chemical pesticides, bactericides and fungicides in the market, however, some of them have shown negative effects on soil and plant health [1]. Even though, chemical control of insect pests and plant diseases is efficient, it is characterized with environmental hazards [1]. There is therefore, the need to explore novel sources of pesticides and plant disease control agents with little or no negative impact on consumers. A major progress in this direction is the exploitation of endophytes for biological control of plant pathogens. Several studies have documented the efficacy of endophytic microbes to produce secondary metabolites with insecticidal and biological control activities. A survey of published articles on endophytes as identified by Eq. 1 in the study databases showed that 760 articles (Additional file 1: Table S1) have reported the biocontrol activity of endophytes, out of which 36 percent was published within the last two years. There are 40 additional articles that reported the biological control properties of endophytic microbes: pest control (19 articles), parasitoid (11 articles), biopesticide (6 articles) and microbial control (4 articles) (Additional file 1: Table S1). The aforementioned keywords form an integral part of the biocontrol potential of endophytes. There are overwhelming evidences of the enormous potential of endophytes in biocontrol of pests and plant pathogens.

In this section, we accentuate some of the most recent reports on the biological control activity of endophytes (Table 1) and the implication on agricultural productivity. Ramakuwela et al. [10] established the biocontrol activity of Beauveria bassiana against two pecan pests: Melanocallis caryaefoliae and Monellia caryella. In their study, Ramakuwela et al. [10] showed that populations of the pecan aphids significantly reduced on pecan leaves colonized with B. bassiana. This, therefore, confirms the aptitude of B. bassiana for application in pecan pest management as its usage will reduce the pest-damaging effects on foliage and shucks of pecan, thereby increasing the rate of photosynthesis with consequent effect on crop yield. Also, a number of chloramphenicol derivatives isolated from Acremonium vitellinum, a marine-alga endophyte showed considerable insecticidal activity against the cotton bollworm, Helicoverpa armigera [11]. Recent studies have also reported the potential use of extracts from endophytic microbes and their bioactive compounds as antifeedants for biological control of pests such as Plutella xylostella larvae and Myzus persicae [12, 13].

Table 1 Biocontrol potential of endophytes against insect pest and phytopathogens
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Moreover, endophytic microbes have shown effective antagonistic activity against phytopathogens. Chen et al. [19] reported the biocontrol activity of Lactobacillus plantarum CM-3, an endophytic lactic acid bacterium against Botrytis cinereal, which causes “grey mold”, a sternly destructive strawberry disease. A Streptomyces species showed a promising biocontrol potential against “anthracnose”, also a strawberry disease but caused by Glomerella cingulata as the endophytic bacteria was reported to suppress the development of “strawberry anthracnose” lesions [20]. Meanwhile, Latz et al. [21] identified Penicillium olsonii ML37 and Acremonium alternatum ML38 as promising biocontrol agents against wheat Septoria tritici blotch (STB). It is noteworthy that the identified endophytic fungi were effective for the control of the disease in the two wheat cultivars investigated: cv. Sevin and cv. Mariboss. Bacillus velezensis 8–4, an endophytic bacterium isolated from potato was reported to have exhibited robust inhibitory effect on Streptomyces galilaeus, a causative agent of potato scab, a severe soil-borne disease of potato [22]. Likewise, the endophytic bacterium was effective against four other potato pathogens of fungal origin including Phoma foveata, Rhizoctonia solani, Fusarium avenaceum and Colletotrichum coccodes [22]. It is remarkable that the Bacillus strain exhibited higher control efficiency against potato scab over other types of treatments with resultant improvement on potato yield. Similarly, Huang et al. [23] documented the control efficacy of two hundred and eighty-eight endophytic fungal strains against cucumber Rhizoctonia root rot with about 33 percent showing above 80 percent control efficiency against the disease while approximately 74 percent of the endophytic fungi exhibited over 50 percent control efficiency against Rhizoctonia solani. Also, an endophytic bacterium isolated from boxwood leaves and identified as a member of Burkholderia cepacia complex displayed an impressive biocontrol activity against Calonectria pseudonaviculata, implicated in boxwood blight disease [24]. The endophytic bacterial strain significantly reduced spore formation by the pathogen, thus, alleviated the occurrence of blight by about 90 percent [24]. Koohakan et al. [32] showed that an unidentified endophytic bacterium reduced the occurrence and severity of Fusarium wilt disease of tomato. Besides, coating of tomato seed with the endophytic bacteria improved growth performance of tomato plant and production quality [32]. Furthermore, Bacillus subtilis SCB-1, an endophytic bacterium from sugarcane, displayed a remarkable biocontrol activity as it exhibited powerful antagonistic activity against a wide range of sugarcane pathogens belonging to the following genera: Saccharicola, Cochliobolus, Alternaria and Fusarium [1]. In addition, treatment of mung bean seeds with Bacillus subtilis SCB-1 extract resisted infection by Fusarium. The authors associated the significant biocontrol activity of Bacillus subtilis SCB-1 against phytopathogens with lipopeptide surfactin, an antifungal compound detected in the bacterial extract [1].

Endophytes with biocontrol activities have transcended fungi and bacteria as Khunnamwong et al. [25] reported the antagonistic potential of yeasts against some phytopathogens. Specifically, different strains of Wickerhamomyces anomalus exhibited impressive antagonistic property against Curvularia lunata, Fusarium moniliforme and Rhizoctonia solani, which are causative agents of rice dirty panicle disease, corn stalk rot disease and rice sheath blight disease, respectively. However, Kodamae ohmeri repressed the development of only F. moniliforme, which is implicated in the pathogenesis of rice bakanae disease. The antagonistic behavior of the yeasts was attributed to the production of secondary metabolites such as “3-methyl-1-butyl acetate and 3-methyl-1-butanol”; “β-1,3-glucanase and chitinase”, with the capacity to degrade fungal cell wall; and “siderophores”. Solubilization of PO43− and ZnO was also identified as a possible antagonistic mechanism employed by the yeast strains against the different plant pathogens [25]. This is corroborated by Wonglom et al. [26], who implicated volatile organic compounds (VOCs) secreted by Trichoderma asperellum in the biocontrol of Corynespora cassiicola and Curvularia aeria, which are responsible for the pathogenesis of lettuce leaf spot disease. Moreover, VOCs elicited increased chitinase and β-1,3-glucanase activity, which probably arose from increased degradation of the fungal pathogen’s cell wall by the enzymes. Besides, VOCs from Trichoderma asperellum stimulated lettuce growth and improved chlorophyll content, which is significant to photosynthesis. Similarly, Rojas-Solis et al. [15] attributed the impressive antagonistic and antifungal activity exhibited by two novel endophytic bacterial strains: Pseudomonas stutzeri E25 and Stenotrophomonas maltophilia CR71 against B. cinerea to production of VOCs, specifically, dimethyl disulphide (DMDS). DMDS elicited its biocontrol activity through mycelial inhibition mechanism. It is noteworthy that the endophytic bacterial strains also promoted the growth of tomato plants and as well improved the chlorophyll content [15]. Four different strains of endophytic Hypoxylon anthochroum emitted VOCs (majorly sesquiterpenes and monoterpenes) with inhibitory activity against F. oxysporum growth on cherry tomatoes [16]. It is evident from these studies that VOCs from endophytes are promising biocontrol agents against phytopathogens with plant growth stimulatory potentials. Therefore, researchers should continue to explore the biodiversity of endophytic microbes for novel VOCs and other secondary metabolites with excellent antagonistic property against pathogens affecting crop yield.

Addtionally, Gao et al. [27] reported the antagonistic activity of Streptomyces albidoflavus OsiLf-2 (an endophytic bacterium isolated from rice) against Magnaporthe oryzae, which is implicated in rice blast pathogenesis. The endophyte displayed its biocontrol activity by impeding the pathogen’s mycelial growth. Likewise, metabolites in the endophyte culture supernatant were reported to have obstructed mycelial development and sporulation as well as “appressorial formation” in the pathogen [27]. Streptomyces albidoflavus OsiLf-2 also exhibited significant antifungal activity, which may be linked to its ability to produce “antimicrobial compounds”, “cell wall lytic enzymes”, “siderophore” and “phytohormones”. Besides, treatment of rice with the endophytic bacterial stimulated diverse defence responses including enzyme activation, buildup of hydrogen peroxide and increased expression of salicyclic acid. It is evident that this endophytic bacterial strain is an auspicious candidate for managing rice blast disease.

A recent development in the application of endophytes as biocontrol agents is the introduction of nanotechnology for production of ecofriendly biocontrol agents as a substitute for conventional chemical fungicides. Ibrahim et al. [31] biosynthesized silver nanoparticles using an endophytic bacterium (Pseudomonas poae CO) from garlic. The biosynthesized nanoparticles showed antagonistic activity against Fusarium graminearum, which causes wheat Fusarium head blight by inhibiting the “mycelium growth, spore germination and mycotoxin production” by the pathogen [31]. The study indicated that biosynthesized nanoparticles from endophytic microbes may play a significant role in the management of phyto diseases. However, there is need for researchers to leverage the biocontrol potential of endophytes for development of nanoparticles with biological control activity against a wide range of plant pathogens.

The ability of endophytes to produce a wide range of secondary metabolites, (majorly VOCs) characterized by remarkable pesticidal, bactericidal, fungicidal, antinematicidal, herbicidal and algicidal properties, suggests the potential of endophytes to contribute significantly to achieving sustainable agriculture because integrated pest management (IPM) is one of the key sustainable farming practices. More so, biological control of pests is an integral part of IPM. Exploitation of endophytes for production of biocontrol agents will further minimize the use of chemical pesticides in line with the IPM [33]. Economically, effective pest management through the use of biocontrol agents from endophytes would definitely improve agricultural productivity, thereby ensuring farmers’ profitability. Overall, biological control using endophytes-derived compounds would further protect the environment and enhance public health, which are hallmarks of sustainable agriculture.

2.3 Aptitude of endophytes for enzyme production

Given the high utility of enzymes in different industrial sectors, there is increased market demand for purified enzymes. Hence, the need for exploration of novel sources of various classes of industrial enzymes, with robust production yield and improved enzyme titre. Endophytic microbes have shown excellent aptitude for production of a wide range of enzymes with industrial and biotechnological significance. A survey of published articles on endophytes over the last three decades as available in WoS and Scopus databases revealed that the following enzymeshave been produced by endophytes: cellulase, chitinase, α-glucosidase, protease, L-asparaginase, amylase, laccase, lipase, xylanase, β-glucosidase,glutaminase, endoglucanase, keratinase etc. A summary of enzyme production by some endophytic microbes is presented in Table 2.

Table 2 Aptitude of endophytes for enzyme production
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One of the most desirable industrial enzymes globally is cellulases, which comprise of exoglucanases, endoglucanases and β-glucosidase. The increased interest in cellulases is, perhaps, attributed to the robust industrial application potentials in biorefinery as well as paper and pulp industry. Cellulases are involved in cellulose hydrolysis by cleaving the β-1,4 linkages in the complex structure thereby releasing the sugars for fermentation during biofuel production. Another enzyme of significance in biorefinery is xylanase because it has the ability to break the varied β-1,4-glycoside linkage in xylan to release xylose, hence, its involvement in hemicellulose degradation. Undoubtedly, cellulases, xylanases and other accessory enzymes from microbes can be used as “emerging green tool” [66] for biofuel production from lignocellulose biomass.

To achieve goal 7 of the UN SDGs: ensuring access to affordable and clean energy, there is an unarguable need for sustainable production of cellulases and xylanases. Hence, bioprospecting of endophytes as bioresources for enhanced and sustainable cellulase and xylanase production is imperative. The good news is that there are recent research efforts toward exploring diverse endophytic microbes for production of lignocellulolytic enzymes (Table 2). One of such research endeavours is the work of Robl et al. [39], where optimum xylanase production (458 U/mL) by an endophytic fungus: Aspergillus niger DR02 was reported in a “constant fed-batch” fermentation. Interestingly, proteomics of the endophytic fungus revealed the activity of other enzymes including cellobiohydrolase, beta-glucosidase and beta-xylosidase, which also play important role in biofuel production. Cellobiohydrolase involves in the degradation of cellulose by breaking the 1,4-β-D-glycosidic bonds, leading to the cleavage of cellobiose unit from the cellulose chain ends while beta-glucosidase works in synergy with endo-β-1,4-glucanases and cellobiohydrolases to convert cellobiose to glucose [67] for biofuel production. Also, beta-xylosidase is an integral part of the enzyme battery (cellulases and hemicellulases) involved in the degradation of lignocellulose biomass [68]. Similarly, A. terreus, an endophyte from Corchorus olitorius exhibited excellent xylanase production with improved production of the enzyme achieved using the host plant and pea peel as substrate [41]. It is worthy of note that hydrolysis of wheat bran by crude xylanase from A. terreus generated significant fermentable sugars and improved saccharification, suggesting that xylanase could play a significant role in the utilization of wheat bran as feedstock for biofuel production. Besides, it has potential for application in various other industrial processes including clarification of juice, bread production, biobleaching and deinking of waste paper [66].

Apart from Aspergillus, endophytes belonging to other fungal genera such as Fusarium, Trichoderma, Botryosphaeria, Saccharicola and Diaporthe have shown vigorous potential for cellulolytic enzymes production. Out of fourteen endophytic fungi screened by Marques et al. [45] for their ability to produce cellulolytic enzymes, Botryosphaeria sp. AM01 and Saccharicola sp. EJC 04 displayed auspicious potential for production of cellulases and xylanases, with prospect in sugarcane bagasse saccharification. Furthermore, two different endophytic fungal strains of Fusarium genus (Fusarium sambucinum and Fusarium sp.) have been reported to show impressive capability for production of lignin peroxidase, manganese-dependent peroxidase and laccase [53], which are significant in delignification of feedstock for biofuel production [69]. In the same study, Trichoderma camerunense expressed appreciable cellulase and xylanase activity [53]. The production of lignocellulolytic enzymes by endophytes is a desirable trait for sustainable biorefinery as the enzyme system is a promising alternative to chemical pretreatment of feedstock for biofuel production. However, Goukanapalle et al. [61] reported the expression of the following cellulases: filter paperase, carboxymethyl cellulase and β-glucosidase by Pestalotiopsis microspora TKBRR. It is remarkable that cellulase production is not limited to endophytic fungi alone as some endophytic bacteria isolated from Capsicum chinese plant have shown the potential for production of endoglucanase and filter paper cellulase [60]. Likewise, some Streptomyces species isolated from plants in Brazil exhibited remarkable potential as hemicellulase producers while the extracts from the endophytic strains showed prospect for lignocellulose biomass deconstruction and biofuel production [52].

Another enzyme of industrial significance reported to have been produced by endophytes is laccase. Apart from being a lignin-degrading biocatalyst, laccase is characterized by several other application potentials including juice clarification, dye decolourization, degradation of emerging environmental pollutants and so on. The diverse applications of laccase in different industrial sectors have necessitated exploration of new sources with enhanced production capacity to meet the increasing demand. It is noteworthy that a few of the laccase-producing endophytic fungi discussed in this paper belong to Phomopsis genus. Wang et al. [34] detected a new laccase gene in Phomopsis liquidambari, which was subsequently cloned and expressed. The expressed P. liquidambari laccase exhibited remarkable industrial properties as it was acidotolerant and thermostable, with about 50% of the enzyme activity being retained after 20 h. Besides, the enzyme displayed prospective application in the agricultural sector as it promoted peanut growth in the study and as well reduced soil phenolic contents. Likewise, Phomopsis sp.exhibited improved laccase production with about twofold due to its exposure to “electron beam radiation” [48]. The enzyme was metallotolerant and displayed good thermostability, with potential application in remediation of synthetic dyes. Moreover, γ-irradiation of the aforementioned endophytic fungus boosted laccase production [65] and improved the enzyme catalytic efficiency, which was evident in the effective degradation of a recalcitrant dye, aniline blue and textile effluent [65]. More so, members of Fusarium genus have exhibited robust laccase-producing potential. This was demonstrated by Muthezhilan et al. [35] who identified Fusarium sp. AEF17 as the most promising laccase-producer in a screening that involved twenty-nine endophytic fungi from different coastal sand dune plants. Interestingly, purified laccase from Fusarium sp. AEF17 exhibited outstanding remediation potential as it showed significant decolourization activity on a wide range of synthetic dyes [35]. Furthermore, endophytic fungal strains belonging to Hormonema, Pringsheimia, Ulocladium and Neofusicocum genera have also shown promising potential for laccase production [40].

Apart from the popular industrial enzymes discussed in the earlier paragraphs, endophytes have also shown emerging potential for production of some relatively rare and unique enzymes such as inulinase, pullulanase and L-asparaginase. Two endophytic fungi of Humicola and Fusarium genera have shown dexterity for production of inulinase [50], an industrial food biocatalyst that hydrolyzes inulin into simple sugars, particularly fructose. Inulinase activity has promoted utilization of inulin as an alternative to starch in various food industries [49]. Moreover, inulinase has shown promising application potential in biorefinery as inulin-containing biomass has been utilized for production of biofuels [49]. Pullulanase, a debranching enzyme, was also secreted by an endophyte, Aspergillus sp. [59]. The ability of endophytes to produce pullulanase holds enormous potential in the starch industry because of the enzyme peculiarity in hydrolyzing the α-1,6-glucosidic linkages of pullulan. Another enzyme that has recently been produced by endophytes is L-asparaginase, which is used as a chemotherapeutic agent for the treatment of lymphoblastic leukemia [55]. Production of L-asparaginase has been reported in a wide range of endophytic fungi including Fusarium, Penicillium, Aspergillus, Alternaria and Talaromyces species [56, 58, 64].The potential of endophytic bacterial strains for asparaginase production has also been reported [63]. However, endophytic bacteria seemed to be underexplored for the production of asparaginase, hence, researchers should channel more efforts towards exploring novel endophytic bacteria for asparaginase production as this would further alleviate the pains of patients with leukemia.

Furthermore, endophytes have shown prospect for production of agriculture-relevant enzymes including 1-aminocyclopropane-1-carboxylate deaminase (ACCD) and chitinase [5, 6]. Chitinase is usually produced by endophytes as a defence response mechanism of the host plants against pests and pathogens whereas ACCD promotes plant growth and stress tolerance by hydrolyzing 1-aminocyclopropane-1-carboxylate to alpha-ketobutyrate and ammonia, thereby reducing ethylene concentration in the host plant. Apart from the plant-health promoting significance of the enzymes produced by endophytic microbes, most of these enzymes have specific industrial applications, which are articulated in the previous paragraphs.

The use of endophytes-derived enzymes in industrial processes is capable of improving the economic performance of various industries [70]. For instance, lignocellulolytic enzymes from endophytes could stimulate the use of lignocellulose waste biomass as cheap feedstock for biofuel production. This is not only cost-effective for the industry but also environmentally-friendly and sustainable. More so, production of plant-health and -growth promoting enzymes by endophytes would enhance agricultural productivity and as such contribute to agro-industrial sustainability. Therefore, it is important for biotechnologists and researchers to continue to harness the biodiversity of endophytes for enhanced enzyme production towards achieving industrial sustainability.

2.4 Prospect of endophytes in polysaccharide and fatty acid production

Apart from enzymes, a copious number of endophytic microbes have displayed the potential for production of other biomolecules including exopolysaccharides and lipids (Table 3). Interestingly, polysaccharides are characterized by enormous therapeutic potential as some have been reported to possess remarkable antioxidant properties [71,72,73] while others exhibited promising anticancer, antitumor and antiproliferative activities [11]. Table 3 gives a summary of endophytic polysaccharides: their compositions and bioactivity. Bacillus amyloliquefaciens isolated from Ophiopogon japonicus produced polysaccharides with anticancer property [74] but the composition of the biomolecule was not determined in the study, as such, it is difficult to ascertain the bioactive component of the polysaccharide. Likewise, Zheng et al. [75] reported the production of an uncharacterized exopolysaccharide by an endophytic Bacillus species from Artemisia annua L, which exhibited antioxidant property and prevented oxidative deoxyribonucleic acid damage. Another uncharacterized polysaccharide which was produced by a Staphylococcus species isolated O. japonicusdisplayed antitumor activity [76]. Similarly, Chen et al. [77] reported exopolysaccharide production by an endophytic Bacillus strain from Codonopsispilosula. The study also revealed the anticancer activity of polysaccharide with the following compositions: galactose, glucose, rhamnose, fucose, arabinose and mannose. Just recently, Glutamicibacterhalophytocola showed the dexterity for production of polysaccharide with excellent antioxidant activity [73].

Table 3 Polysaccharide and fatty acid production by endophytes
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Moreover, a broader range of endophytic fungi have shown intrinsic ability for production of polysaccharides. A Chaetomium species isolated from Gynostemma pentaphyllaproduced polysaccharide with the following composition: glucose, mannose, arabinose and galactose [81]. It is noteworthy that the Chaetomium exopolysaccharide showed antioxidant property and inhibited cell proliferation. In the same vein, two endophytic Diaporthe species from Piper hispidum were able to produce exopolysaccharide with characteristic ability to inhibit cell proliferation. Furthermore, Zeng et al. [84] reported the production of a galactoglucan by a member of Fusarium genus from Dendrobium officinale. The polysaccharide was biologically active as it enhanced immune response, hence it could be used for the development of functional food for the treatment of patients with hypo-immunity. However, a Fusarium species from Fritillaria unibracteata produced a polysaccharide with entirely different composition: “mannose, rhamnose, glucose, galactose, xylose, arabinose and pyranose” [71] but was characterized by efficient antioxidant and cell proliferation inhibitory activities [71]. Other endophytic fungi with polysaccharide production potential include Alternaria tenuissima and Pilidiella guizhouensis [72, 85]. Meanwhile, Mangrovhabitansendophyticus, in addition to exopolysaccharide, produced lipid with the following composition: diphosphatidyl glycerol, phosphatidyl ethanolamine, and phosphatidyl inositol [83]. More so, linoleic, oleic and sciadonic acids were produced by an endophytic fungus isolated from Torreya grandis, Bionectria ochroleuca [79]. Linoleic and oleic acids are polyunsaturated fatty acids with enormous health benefits [86]. Specifically, linoleic acid is one of the major fatty acids essential in human diets as it cannot be synthesized in the body. Endophytes may be a promising source of linoleic acid and other polyunsaturated fatty acids.

3 Conclusions

Endophytes, indeed, possess robust aptitude in biocontrol of phytopathogens and enzyme production, which are significant to agro-industrial sustainability. Nevertheless, there is still dearth of research on the application of endophytes in the biocontrol of termites, which are known for causing substantial damage to agriculture, specifically forest products, with consequent huge economic loss. More so, chemical methods of controlling termites are characterized by low efficiency and high cost. As well, they are not eco-friendly. Future studies should, therefore, explore endophytes for production of novel biocontrol agents against termites.

Furthermore, literature survey showed that endophytes have been poorly explored for production of versatile peroxidase (VP) and dye decolourizing peroxidase (DyP), which are integral part of the ligninolytic enzyme system, with promising potentials in biofuel production and bioremediation. Research effort in this direction is therefore imperative.

Despite the effectiveness of endophytes in biological control of plant pathogens, care must be taken in the direct usage of endophytes so as not to introduce pathogenic microbes in the environment. Researchers can however, exploit the biocontrol potential of endophytes for development of nanoparticles with biocontrol activity against a wide range of phytopathogens. Future studies should focus more on isolating bioactive compounds from endophytes for development of effective biocontrol agents as part of integrated pest management. Therefore, there is a need for metagenomics study of endophytes so as to explore the diversity of endophytic microbes towards discovering novel secondary metabolites of industrial and agricultural significance. It is also important to decipher the biosynthetic pathway of biocontrol agents and enzyme production in endophytes as this can be exploited for large scale production through genetic engineering.

Availability of data and materials

Not applicable.

Abbreviations

ACCD:

1-Aminocyclopropane-1-carboxylate deaminase

DyP:

Dye decolourizing peroxidase

STB:

Septoria tritici blotch

SDGs:

Sustainable development goals

UN:

United nations

VP:

Versatile peroxidase

VOCs:

Volatile organic compounds

WoS:

Web of science

References

  1. Hazarika DJ, Goswami G, Gautom T, Parveen A, Das P, Barooah M, Boro RC (2019) Lipopeptide mediated biocontrol activity of endophytic Bacillus subtilis against fungal phytopathogens. BMC Microbiol 19:71. https://doi.org/10.1186/s12866-019-1440-8

    Article  PubMed  PubMed Central  Google Scholar 

  2. Xiang L, Gong S, Yang L, Hao J, Xue MF, Zeng FS, Zhang XJ, Shi WQ, Wang H, Yu D (2015) Biocontrol potential of endophytic fungi in medicinal plants from Wuhari botanical garden in China. Biol Control. https://doi.org/10.1016/j.biocontrol.2015.12.002

    Article  Google Scholar 

  3. Liu X, Dru D, Ma Y (2016) Potential of endophytes from medicinal plants for biocontrol and plant growth promotion. J Gen Plant Pathol. https://doi.org/10.1007/s10327-016-0648-9

    Article  Google Scholar 

  4. Chen HY, Liu TK, Shi Q, Yang XL (2019) Sesquiterpenoids and diterpenes with antimicrobial activity from Leptosphaeria sp. XL026, an endophytic fungus in Panax notoginseng. Fitoterapia 137:UNSP 104243. https://doi.org/10.1016/j.fitote.2019.104243

    Article  CAS  Google Scholar 

  5. Tian L, Jiang Y, Chen C, Zhang G, Li T, Tong B, Xu P (2014) Screening and identification of an endophytic bacterium with 1-aminocyclopropane-1-carboxylate deaminase activity from Panax ginseng and its effect on host growth. Acta Microbiol Sin 54:760–769

    CAS  Google Scholar 

  6. Dolatabad HK, Javan-Nikkhah M, Shier WT (2017) Evaluation of antifungal, phosphate solubilisation, and siderophore and chitinase release activities of endophytic fungi from Pistacia vera. Mycol Prog 16:777–790

    Article  Google Scholar 

  7. Toghueo RMK, Zabalgogeazcoa I, Vazquez de Aldana BR, Boyom FF (2017) Enzymatic activity of endophytic fungi from the medicinal plants Terminalia catappa, Terminalia mantaly and Cananga odorata. S Afr J Bot 109:146–153

    Article  CAS  Google Scholar 

  8. Bezerra JDP, Nascimento CCF, Barbosa RN, Da Silva DCV, Svedese VM, Silva-Nogueira EB, Gomes BS, Paiva LM, Souza-Motta CM (2015) Endophytic fungi from medicinal plant Bauhinia forficate: diversity and biotechnological potential. Braz J Microbiol 46:49–57

    Article  PubMed  PubMed Central  Google Scholar 

  9. Ruiz-Rosero J, Ramirez-Gonzalez G, Viveros-Delgado J (2019) Software survey: ScientoPy, a scientometric tool for topics trend analysis in scientific publications. Scientometrics 121:1165–1188

    Article  Google Scholar 

  10. Ramakuwela T, Hatting J, Bock C, Vega FE, Wells L, Mbata GN, Shapiro-Ilan D (2020) Establishment of Beauveria bassiana as a fungal endophyte in pecan (Carya illinoinensis) seedlings and its virulence against pecan insect pests. Biol Control 140:104102. https://doi.org/10.1016/j.biocontrol.2019.104102

    Article  CAS  Google Scholar 

  11. Chen D, Zhang P, Liu T, Wang XF, Li ZX, Li W, Wang FL (2018) Insecticidal activities of chloramphenicol derivatives isolated from a marine alga-derived endophytic fungus, Acremonium vitellinum, against the cotton bollworm, Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). Molecules 23:2995

    Article  PubMed Central  CAS  Google Scholar 

  12. Ratnaweera PB, Jayasundara JMNM, Herath HHM, Williams DE, Rajapaksha SU, Nishantha KMD, de Silva ED, Andersen RJ (2020) Antifeedant, contact toxicity and oviposition deterrent effects of phyllostine acetate and phyllostine isolated from the endophytic fungus Diaporthemiriciae against Plutellaxylostella larvae. Pest Manag Sci 76:1541–1548

    Article  CAS  PubMed  Google Scholar 

  13. Kaushik N, Diaz CE, Chhipa H, Julio LF, Andres MF, Gonzalez-Coloma A (2020) Chemical composition of an aphid antifeedant extract from an endophytic fungus, Trichoderma sp. EFI671. Microorganisms 8:420. https://doi.org/10.3390/microorganisms8030420

    Article  CAS  PubMed Central  Google Scholar 

  14. Zhang HR, Wang XQ, Li RF, Sun XC, Sun SW, LiQ XuCP (2017) Preparation and bioactivity of exopolysaccharide from an endophytic fungus Chaetomium sp of the medicinal plant Gynostemma pentaphylla. PharmacognMag 13:477–482

    CAS  Google Scholar 

  15. Rojas-Solis D, Zetter-Salmon E, Contreras-Perez M, Rocha-Granados MD, Macias-Rodriguez L, Santoyo G (2018) Pseudomonas stutzeri E25 and Stenotrophomonas maltophilia CR71 endophytes produce antifungal volatile organic compounds and exhibit additive plant growth-promoting effects. BiocatalAgric Biotechnol 13:46–52

    Google Scholar 

  16. Macias-Rubalcava ML, Sanchez-Fernandez RE, Roque-Flores G, Lappe-Oliveras P, Medina-Romero YM (2018) Volatile organic compounds from Hypoxylon anthochroum endophytic strains as postharvest mycofumigation alternative for cherry tomatoes. Food Microbiol 76:363–373

    Article  CAS  PubMed  Google Scholar 

  17. Zhu HMY, Pan YZ (2019) A novel antimicrobial protein of the endophytic Bacillus amyloliquefaciens and its control effect against Fusarium chlamydosporum. Biocontrol 64:737–748

    Article  CAS  Google Scholar 

  18. Ben Slama H, Cherif-Silini H, Bouket AC, Qader M, Silini A, Yahiaoui B, Alenezi FN, Luptakova L, Triki MA, Vallat A, Oszako T, Rateb ME, Belbahri L (2019) Screening for Fusarium antagonistic bacteria from contrasting niches designated the endophyte Bacillus halotolerans as plant warden against Fusarium. Front Microbiol 9:3236. https://doi.org/10.3389/fmicb.2018.03236

    Article  Google Scholar 

  19. Chen C, Cao Z, Li J, Tao C, Feng Y, Han Y (2020) A novel endophytic strain of Lactobacillus plantarum CM-3 with antagonistic activity against Botrytis cinerea on strawberry fruit. Biol Control 148:104306. https://doi.org/10.1016/j.biocontrol.2020.104306

    Article  CAS  Google Scholar 

  20. Marian M, Ohno T, Suzuki H, Kitamura H, Kuroda K, Shimizu M (2020) A novel strain of endophytic Streptomyces for the biocontrol of strawberry anthracnose caused by Glomerella cingulate. Microbiol Res 234:126428. https://doi.org/10.1016/j.micres.2020.126428

    Article  CAS  PubMed  Google Scholar 

  21. Latz MAC, Jensen B, Collinge DB, Jorgensen HJL (2020) Identification of two endophytic fungi that control Septoria tritici blotch in the field, using a structured screening approach. Biol Control 141:104128

    Article  CAS  Google Scholar 

  22. Cui LX, Yang CD, Wei LJ, Li TH, Chen XY (2020) Isolation and identification of an endophytic bacteria Bacillus velezensis 8–4 exhibiting biocontrol activity against potato scab. Biol Control 141:104156. https://doi.org/10.1016/j.biocontrol.2019.104156

    Article  CAS  Google Scholar 

  23. Huang LQ, Niu YC, Su L, Deng H, Lyu H (2020) The potential of endophytic fungi isolated from cucurbit plants for biocontrol of soilborne fungal diseases of cucumber. Microbiol Res 231:126369. https://doi.org/10.1016/j.micres.2019.126369

    Article  CAS  PubMed  Google Scholar 

  24. Kong P, Hong CX (2020) A potent Burkholderia endophyte against boxwood blight caused by Calonectriapseudonaviculata. Microorganisms 8:310

    Article  CAS  PubMed Central  Google Scholar 

  25. Khunnamwong P, Lertwattanasakul N, Jindamorakot S, Suwannarach N, Matsui K, Limtong S (2020) Evaluation of antagonistic activity and mechanisms of endophytic yeasts against pathogenic fungi causing economic crop diseases. Folia Microbiol 65:573–590

    Article  CAS  Google Scholar 

  26. Wonglom P, Ito S, Sunpapao A (2020) Volatile organic compounds emitted from endophytic fungus Trichoderma asperellum T1 mediate antifungal activity, defense response and promote plant growth in lettuce (Lactuca sativa). Fungal Ecol 43:100867. https://doi.org/10.1016/j.funeco.2019.100867

    Article  Google Scholar 

  27. Gao Y, Zeng XD, Ren B, Zeng JR, Xu T, Yang YZ, Hu XC, Zhu ZY, Shi LM, Zhou GY, Zhou Q, Liu XM, Zhu YH (2020) Antagonistic activity against rice blast disease and elicitation of host-defence response capability of an endophytic Streptomyces albidoflavus OsiLf-2. Plant Pathol 69:259–271

    Article  CAS  Google Scholar 

  28. Barra-Bucarei L, Iglesias AF, Gonzalez MG, Aguayo GS, Carrasco-Fernandez J, Castro JF, Campos JO (2020) Antifungal activity of Beauveria bassiana endophyte against Botrytis cinerea in two Solanaceae crops. Microorganisms 8:65

    Article  CAS  Google Scholar 

  29. Rong SH, Xu H, Li LH, Chen RJ, Gao XL, Xu ZJ (2020) Antifungal activity of endophytic Bacillus safensis B21 and its potential application as a biopesticide to control rice blast. PesticBiochem Phys 162:69–77

    CAS  Google Scholar 

  30. Rezvani V, Taheri P, Pourianfar HR, Drakhshan A (2020) Biocontrol and plant growth promotion activities of endophytic and rhizospheric fungi from almond trees (Prunus dulcis) indigenous in the Northeast of Iran. Curr Res Environ Appl Mycol 10:50–62

    Article  Google Scholar 

  31. Ibrahim E, Zhang MC, Zhang Y, Hossain A, Qiu W, Chen Y, Wang YL, Wu WG, Sun GC, Li B (2020) Green-synthesization of silver nanoparticles using endophytic bacteria isolated from garlic and its antifungal activity against wheat Fusarium head blight pathogen Fusarium graminearum. Nanomaterials 10:219

    Article  CAS  PubMed Central  Google Scholar 

  32. Koohakan P, Prasom P, Sikhao P (2020) Application of seed coating with endophytic bacteria for Fusarium wilt disease reduction and growth promotion in tomato. Int J Agric Technol 16:55–62

    CAS  Google Scholar 

  33. Alam MZ, Crump AR, Haque MM, Islam MS, Hossain E, Hasan SB, Hasan SB, Hossain MS (2016) Effects of integrated pest management on pest damage and yield components in a rice agro-ecosystem in the Barisal region of Bangladesh. Front Environ Sci. https://doi.org/10.3389/fenvs.2016.00022

    Article  Google Scholar 

  34. Wang HW, Zhu H, Liang XF, Du W, Dai CC (2014) Molecular cloning and expression of a novel laccase showing thermo- and acid-stability from the endophytic fungus Phomopsis liquidambari and its potential for growth promotion of plants. Biotechnol Lett 36:167–173

    Article  CAS  PubMed  Google Scholar 

  35. Muthezhilan R, Vinoth S, Gopi K, Jaffar Hussain A (2014) Dye degrading potential of immobilized laccase from endophytic fungi of coastal sand dune plants. Int J ChemTech Res 6:4154–4160

    CAS  Google Scholar 

  36. Costa-Silva TA, Souza CRF, Oliveira WP, Said S (2014) Characterization and spray drying of lipase produced by the endophytic fungus Cercosporakikuchii. Braz J Chem Eng 31:849–858

    Article  Google Scholar 

  37. Choudhury P (2015) Industrial application of lipase: a review. Biopharm J 11:41–47

    Google Scholar 

  38. Chun-Zhu S, Dong-Hong C (2015) Identification of a novel endophytic Bacillus pumilus lipase from the seed of Pistacia chinensisbunge. Res J Biotechnol 10:19–25

    Google Scholar 

  39. Robl D, Delabona PD, Costa PD, Lima DJD, Rabelo SC, Pimentel IC, Buchli F, Squina FM, Padilla G, Pradella JGD (2015) Xylanase production by endophytic Aspergillus niger using pentose-rich hydrothermal liquor from sugarcane bagasse. Biocatal Biotransformation 33:175–187

    Article  CAS  Google Scholar 

  40. Fillat U, Martin-Sampedro R, Macaya-Sanz D, Martin JA, Ibarra D, Martinez MJ, Eugenio ME (2016) Screening of eucalyptus wood endophytes for laccase activity. Process Biochem 51:589–598

    Article  CAS  Google Scholar 

  41. Ahmed SA, Saleh SAA, Mostafa FA, Abd El Aty AA, Ammar HAM (2016) Characterization and valuable applications of xylanase from endophytic fungus Aspergillus terreus KP900973 isolated from Corchorus olitorius. Biocatal Agric Biotechnol 7:134–144

    Article  Google Scholar 

  42. El-Gendy MMAA, Taha TM, Abo-Dahab NF, Hassan FSM (2016) Process optimization of l-glutaminase production; a tumour inhibitor from marine endophytic isolate Aspergillus sp. ALAA-2000. Int J PharmTech Res 9:256–267

    CAS  Google Scholar 

  43. Prakash O, Nimonkar Y, Chavadar MS, Bharti N, Pawar S, Sharma A, Shouche YS (2017) Optimization of nutrients and culture conditions for alkaline protease production using two endophytic Micrococci: Micrococcus aloeverae and Micrococcus yunnanensis. Indian J Microbiol 57:218–225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Orlandelli RC, Santos MS, Polonio JC, de Azevedo JL, Pamphile JA (2017) Use of agro-industrial wastes as substrates for a-amylase production by endophytic fungi isolated from Piper hispidum Sw. Acta Scientiarum-Technol 39:255–261

    Article  Google Scholar 

  45. Marques NP, Pereira JD, Gomes E, da Silva R, Araujo AR, Ferreira H, Rodrigues A, Dussan KJ, Bocchini DA (2018) Cellulases and xylanases production by endophytic fungi by solid state fermentation using lignocellulosic substrates and enzymatic saccharification of pretreated sugarcane bagasse. Ind Crops Prod 122:66–75

    Article  CAS  Google Scholar 

  46. Mani VM, Soundari AJPG, Preethi K (2018) Enzymatic and phytochemical analysis of endophytic fungi on Aegle marmelos from Western Ghats of Tamil Nadu, India. Int J Life Sci Pharm Res 8:L1–L8

    CAS  Google Scholar 

  47. Dorra G, Ines K, Imen BS, Laurent C, Sana A, Olfa T, Pascal C, Thierry J, Ferid L (2018) Purification and characterization of a novel high molecular weight alkaline protease produced by an endophytic Bacillus halotolerans strain CT2. Int J Biol Macromol 111:342–351

    Article  CAS  PubMed  Google Scholar 

  48. Navada KK, Sanjeev G, Kulal A (2018) Enhanced biodegradation and kinetics of anthraquinone dye by laccase from an electron beam irradiated endophytic fungus. Int Biodeterior Biodegradation 132:241–250

    Article  CAS  Google Scholar 

  49. Mohan A, Flora B, Girdhar M (2018) Inulinase: an important microbial enzyme in food industry. In: Singh J, Sharma D, Kumar G, Sharma N (eds) Microbial bioprospecting for sustainable development. Springer, Singapore, pp 237–248

    Chapter  Google Scholar 

  50. Silvera D, Luthfin I, Aulia A, Wahyu PN, Saryono S (2018) Optimization of process parameters for inulinase production from endophytic fungi Fusarium solani LBKURCC67, Humicolafuscoatra LBKURCC68 and Fusarium oxysporum LBKURCC69. Res J Chem Environ 22:71–78

    Google Scholar 

  51. Felber AC, Specian V, Orlandelli RC, Costa AT, Polonio JC, Mourao KSM, Pamphile JA (2019) Endoglucanase production by endophytic fungi isolated from Vitis labrusca L. with peanut hull and sawdust as substrates. Biosci J 35:933–940

    Article  Google Scholar 

  52. Robl D, Mergel CM, Costa PD, Pradella JGD, Padilla G (2019) Endophytic actinomycetes as potential producers of hemicellulases and related enzymes for plant biomass degradation. Braz Arch Biol Technol 62:e19180337. https://doi.org/10.1590/1678-4324-2019180337

    Article  CAS  Google Scholar 

  53. Martinho V, Lima LMD, Barros CA, Ferrari VB, Passarini MRZ, Santos LA, Sebastianes FLD, Lacava PT, de Vasconcellos SP (2019) Enzymatic potential and biosurfactant production by endophytic fungi from mangrove forest in Southeastern Brazil. AMB Express 9:130. https://doi.org/10.1186/s13568-019-0850-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Ben Mefteh F, Frikha F, Daoud A, Bouket AC, Luptakova L, Alenezi FN, Al-Anzi BS, Oszako T, Gharsallah N, Belbahri L (2019) Response surface methodology optimization of an acidic protease produced by Penicillium bilaiae isolate TDPEF30, a newly recovered endophytic fungus from healthy roots of date palm trees (Phoenix dactylifera L.). Microorganisms 7:74. https://doi.org/10.3390/microorganisms7030074

    Article  CAS  PubMed Central  Google Scholar 

  55. Cachumba JJM, Antunes FAF, Peres GFD, Brumano LP, Santos JCD, Da Silva SS (2016) Current applications and different approaches for microbial L-asparaginase production. Braz J Microbiol 47:77–85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Bhosale H, As-Suhbani AE (2019) Screening of fungal endophytes isolated from medicinal plants for glutaminase free L-asparaginase activity. J Exp Biol Agric Sci 7:396–402

    CAS  Google Scholar 

  57. Alrumman SA, Mostafa YS, Al-izran KA, Alfaifi MY, Taha TH, Elbehairi SE (2019) Production and anticancer activity of an L-asparaginase from Bacillus licheniformis isolated from the Red Sea. Saudi Arabia. Sci Rep 9:3756

    Article  CAS  PubMed  Google Scholar 

  58. Bhavana NS, Prakash HS, Nalini MS (2019) Antioxidative and L-asparaginase potentials of fungal endophytes from Rauvolfia densiflora (Apocynaceae), an ethnomedicinal species of the Western Ghats. Czech Mycol 71:187–203

    Article  Google Scholar 

  59. Naik B, Goyal SK, Tripathi AD, Kumar V (2019) Screening of agro-industrial waste and physical factors for the optimum production of pullulanase in solid-state fermentation from endophytic Aspergillus sp. Biocatal Agric Biotechnol 22:101423. https://doi.org/10.1016/j.bcab.2019.101423

    Article  Google Scholar 

  60. Sharma A, Singh P, Sarmah BK, Nandi SP (2020) Isolation of cellulose-degrading endophyte from Capsicum chinense and determination of its cellulolytic potential. Biointerface Res Appl Chem 10:6964–6973

    Article  CAS  Google Scholar 

  61. Goukanapalle PKR, Kanderi DK, Rajoji GS, Kumari BS, Bontha RR (2020) Optimization of cellulase production by a novel endophytic fungus PestalotiopsismicrosporaTKBRR isolated from Thalakona forest. Cellulose 27:6299–6316

    Article  CAS  Google Scholar 

  62. Cardoso VM, Campos FF, Santos ARO, Ottoni MHF, Rosa CA, Almeida VG, Grael CFF (2020) Biotechnological applications of the medicinal plant Pseudobrickelliabrasiliensis and its isolated endophytic bacteria. J Appl Microbiol. https://doi.org/10.1111/jam.14666

    Article  PubMed  Google Scholar 

  63. Prihanto AA, Yanti I, Murtazam MA, Jatmiko YD (2020) Optimization of glutaminase-free L-asparaginase production using mangrove endophytic Lysinibacillus fusiformis B27. F1000 Res 8:1938. https://doi.org/10.12688/f1000research.21178.2

    Article  CAS  Google Scholar 

  64. Krishnapura PR, Belur PD (2020) L-Asparaginase Production using solid-state fermentation by an endophytic Talaromycespinophilusisolated from rhizomes of Curcumaamada. J Pure Appl Microbio 14:307–318

    Article  CAS  Google Scholar 

  65. Navada KK, Kulal A (2020) Enhanced production of laccase from gamma irradiated endophytic fungus: A study on biotransformation kinetics of aniline blue and textile effluent decolourisation. J Environ Chem Eng 8:UNCP 103550. https://doi.org/10.1016/j.jece.2019.103550

    Article  CAS  Google Scholar 

  66. Bhardwaj N, Kumar B, Verma PA (2019) A detailed overview of xylanases: an emerging biomolecule for current and future prospective. Bioresour Bioprocess 6:40

    Article  Google Scholar 

  67. Treebupachatsakul T, Shioya K, Nakazawa H, Kawaguchi T, Morikawa Y, Shida Y et al (2015) Utilization of recombinant Trichoderma reesei expressing Aspergillus aculeatus β-glucosidase I (JN11) for a more economical production of ethanol from lignocellulosic biomass. J Biosci Bioeng 120:657–665

    Article  CAS  PubMed  Google Scholar 

  68. Jordan DB, Wagschal K (2010) Properties and applications of microbial β-D-xylosidases featuring the catalytically efficient enzyme from Selenomonas ruminantium. Appl Microbiol Biotechnol 86:1647–1658. https://doi.org/10.1007/s00253-010-2538-y

    Article  CAS  PubMed  Google Scholar 

  69. Falade AO, Nwodo UU, Iweriebor BC, Green E, Mabinya LV, Okoh AI (2017) Lignin peroxidase functionalities and prospective applications. MicrobiologyOpen 6:e00394

    Article  CAS  Google Scholar 

  70. Parida V, Sjodin D, Reim W (2019) Reviewing literature on digitalization, business model innovation, and sustainable industry: past achievements and future promises. Sustainability 11:391. https://doi.org/10.3390/su11020391

    Article  Google Scholar 

  71. Pan F, Hou K, Li DD, Su TJ, Wu W (2019) Exopolysaccharides from the fungal endophytic Fusarium sp. A14 isolated from Fritillaria unibracteata Hsiao et KC Hsia and their antioxidant and antiproliferation effects. J Biosci Bioeng 127:231–240

    Article  CAS  PubMed  Google Scholar 

  72. Zhang J, Yang B, Chen H (2020) Identification of an endophytic fungus Pilidiellaguizhouensis isolated from Eupatorium chinense L. and its extracellular polysaccharide. Biologia. https://doi.org/10.2478/s11756-020-00465-3

    Article  Google Scholar 

  73. Xiong YW, Ju XY, Li XW, Gong Y, Xu MJ, Zhang CM, Yuan B, Lv ZP, Qin S (2020) Fermentation conditions optimization, purification, and antioxidant activity of exopolysaccharides obtained from the plant growth-promoting endophytic actinobacterium Glutamicibacterhalophytocola KLBMP 5180. Int J Biol Macromol 153:1176–1185

    Article  CAS  PubMed  Google Scholar 

  74. Chen YT, Yuan Q, Shan LT, Lin MA, Cheng DQ, Li CY (2013) Antitumor activity of bacterial exopolysaccharides from the endophyte Bacillus amyloliquefaciens sp. isolated from Ophiopogon japonicus. Oncol Lett 5:1787–1792

    Article  PubMed  PubMed Central  Google Scholar 

  75. Zheng LP, Zou T, Ma YJ, Wang JW, Zhang YQ (2016) Antioxidant and DNA damage protecting activity of exopolysaccharides from the endophytic bacterium Bacillus cereus SZ1. Molecules 21:174

    Article  PubMed Central  CAS  Google Scholar 

  76. Xu WJ, Yang YL, Yang YG, Lu ZX, Lu QY, Chen YT (2018) Exopolysaccharides from an Ophiopogon japonicus endophyte inhibit proliferation and migration in MC-4 human gastric cancer cells. TranslCancer Res 7:1567–1576

    CAS  Google Scholar 

  77. Chen M, Li YY, Liu Z, Qu YJ, Zhang HJ, Li DW, Zhou J, Xie SB, Liu M (2018) Exopolysaccharides from a Codonopsis pilosula endophyte activate macrophages and inhibit cancer cell proliferation and migration. Thorac Cancer 9:630–639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Guo SD, Mao WJ, Yan MX, Zhao CQ, Li N, Shan JM, Lin C, Liu X, Guo T, Guo TT, Wang SY (2014) Galactomannan with novel structure produced by the coral endophytic fungus Aspergillus ochraceus. CarbohydrPolym 105:325–333

    CAS  Google Scholar 

  79. Yang Y, Jin ZH, Jin QC, Dong MS (2015) Isolation and fatty acid analysis of lipid-producing endophytic fungi from wild Chinese Torreya Grandis. Microbiol 84:710–716

    Article  CAS  Google Scholar 

  80. Mahapatra S, Banerjee D (2016) Production and structural elucidation of exopolysaccharide from endophytic Pestalotiopsissp BC55. Int J Biol Macromol 82:182–191

    Article  CAS  PubMed  Google Scholar 

  81. Zhang X, Zhou YY, LiY FuXC, Wang Q (2017) Screening and characterization of endophytic Bacillus for biocontrol of grapevine downy mildew. Crop Prot 96:173–179

    Article  Google Scholar 

  82. Orlandelli RC, Corradi da Silva MDL, Vasconcelos AFD, Almeida IV, Vicentini VEP, Prieto A, Hernandez MDD, Azevedo JL, Pamphile JA (2017) β-(1→3, 1→6)-D-glucans produced by Diaporthe sp. endophytes: Purification, chemical characterization and antiproliferative activity against MCF-7 and HepG2-C3A cells. Int J Biol Macromol 94:431–437

    Article  CAS  PubMed  Google Scholar 

  83. Liu SW, Tuo L, Li XJ, Li FN, Li J, Jiang MG, Chen L, Hu L, Sun CH (2017) Mangrovihabitansendophyticus gen. Nov., sp. nov., a new member of the family Micromonosporaceae isolated from Bruguiera sexangular. Int J Syst Evol Microbiol 67:1629–1636

    Article  CAS  PubMed  Google Scholar 

  84. Zeng YJ, Yang HR, Wang HF, Zong MH, Lou WY (2019) Immune enhancement activity of a novel polysaccharide produced by Dendrobium officinale endophytic fungus Fusarium solani DO7. J Funct Foods 53:266–275

    Article  CAS  Google Scholar 

  85. Wang YG, Li YL, Li SW, Li QY, Fan WG, Kiatoukosin L, Chen JX (2019) Extracellular polysaccharides of endophytic fungus Alternaria tenuissima F1 from Angelica sinensis: production conditions, purification and antioxidant properties. Int J Biol Macromol 133:172–183

    Article  CAS  PubMed  Google Scholar 

  86. Jandacek RJ (2017) Linoleic acid: a nutritional quandary. Healthcare (Basel) 5:20

    Google Scholar 

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  1. Department of Biochemistry, Faculty of Basic Medical Sciences, University of Medical Sciences, Ondo, 351101, Ondo State, Nigeria

    Ayodeji O. Falade & Kayode E. Adewole

  2. Department of Biological Sciences, Faculty of Science, University of Medical Sciences, Ondo, 351101, Ondo State, Nigeria

    Temitope C. Ekundayo

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Falade, A.O., Adewole, K.E. & Ekundayo, T.C. Aptitude of endophytic microbes for production of novel biocontrol agents and industrial enzymes towards agro-industrial sustainability. Beni-Suef Univ J Basic Appl Sci 10, 61 (2021). https://doi.org/10.1186/s43088-021-00146-3

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