|Year : 2018 | Volume
| Issue : 3 | Page : 121-128
This era of biotechnological tools: an insight into endophytic mycobiota
Ghoson M Daba1, Waill A Elkhateeb2, Paul W Thomas3
1 Department of Chemistry of Natural and Microbial Products, Pharmaceutical Industries Division, National Research Center, Giza, Egypt
2 Department of Chemistry of Natural and Microbial Products, Pharmaceutical Industries Division, National Research Center, Giza; Laboratory of Microbial Technology, Department of Bioscience and Biotechnology, Faculty of Agriculture, Kyushu University, Fukuoka, Egypt
3 Mycorrhizal Systems Ltd, Lancashire; University of Stirling, Stirling, UK
|Date of Submission||05-Sep-2018|
|Date of Acceptance||01-Oct-2018|
|Date of Web Publication||07-Dec-2018|
Dr. Ghoson M Daba
Department of Chemistry of Natural and Microbial Products, National Research Centre, Dokki, Giza 12311
Source of Support: None, Conflict of Interest: None
Owing to the outbreak of fatal diseases that require searching for new compounds with high activity and/or novel action mechanisms, screening for promising sources of biologically active compounds that fulfill the current needs of humanity is a matter of life and death. Fungi generally and endophytic ones specifically represent future factories and potent biotechnological tools for production of bioactive natural substances, which could extend healthy life span of humanity (as done by penicillin from centuries), and are considered promising alternatives for some high costly produced chemicals and drugs. The present review highlights some bioactive secondary metabolites, produced by fungal endophytes, involved in medical, pharmaceutical, agricultural, and industrial applications.
Keywords: biological activities, biotechnology, endophytic fungi, pigments, secondary metabolites, taxol
|How to cite this article:|
Daba GM, Elkhateeb WA, Thomas PW. This era of biotechnological tools: an insight into endophytic mycobiota. Egypt Pharmaceut J 2018;17:121-8
|How to cite this URL:|
Daba GM, Elkhateeb WA, Thomas PW. This era of biotechnological tools: an insight into endophytic mycobiota. Egypt Pharmaceut J [serial online] 2018 [cited 2019 May 19];17:121-8. Available from: http://www.epj.eg.net/text.asp?2018/17/3/121/247075
| Introduction|| |
Endophytic mycobiota are fungi that commonly spend their life cycle (or part of it) inhabiting intercellular and/or intracellular spaces in the tissues of healthy plants without harmful aspects ,. Literally, the word endophyte indeed describes location of these microorganisms: ‘endo’ means inside and ‘phyte’ means plants. These endophytes have key roles in enhancing the adaptation of host plants to environmental stresses such as salinity  and temperature . Moreover, endophytes play important roles in promoting plant growth , and protecting the host plant from some pathogens ,,.
Endophytes have been isolated from almost all plants, trees, palms, sea grasses, and lichens ,,. Many reports described the isolation process of endophytes from different plants as well as the predominance of some genera in a given plant species. However, the presence of such endophytes depends on many factors including environmental factors such as the geographical and topographic patterns, growing season, total soluble salts and pH of the soil, as well as nature and age of the host plant ,.
Various biological activities such as antitumor, antibacterial, antiviral, antimalarial, antidiabetic, hypocholesterolemic, and immunomodulatory are reported ([Figure 1]) for some metabolites secreted by endophytic fungi, such as phenols, alkaloids, isoprenoids, steroids, isocoumarines, perylene derivatives, quinones, furandiones, xanthones, terpenoids, depsipeptides, cytochalasin, polyketides, proteins, peptides, lipids, shikimates, and glycosides ,. Furthermore, endophytes produce various low-molecular-weight volatile organic compounds such as alcohols, ketones, esters, acids, and hydrocarbons . On the contrary, many enzymes produced by endophytes are used nowadays in the industries of food, cosmetics, biofuels, paper, cellulose, textile, fine chemicals, detergents, biomaterials, and leather ,.
|Figure 1 Biological activities exerted by metabolites produced by endophytic fungi.|
Click here to view
This review highlights some of the biotechnological applications of some fungal endophytes’ secondary metabolites. Understanding the industrial, agriculture and/or medical importance of such products encourages screening for novel endophytic isolates, which represent an inexhaustible source for secondary metabolites, with potential biological activities and numerous benefits in different fields of biotechnology.
Antitumor medication (taxol)
Taxol (Paclitaxel) is a tetracyclic diterpene lactam that has been approved as a human cancer medication by the Food and Drug Administration owing to its high potency, low toxicity, and broad-spectrum anti-tumor activity . Taxol was first isolated from western yew (Taxus brevifolia) , and its action mechanism includes inhibiting of microtubule depolymerization during cell cycle and cell growth, and then initiating cell apoptosis .
Nowadays, endophytic fungi are used as a biotechnological tool to produce taxol in short time and high productivity in comparison with the traditional production of taxol from yew tree species, as extraction of 1 kg of taxol requires cutting of ∼300 trees, which is a huge ecological loss ,. It is worth noting that full course in cancer treatment requires consuming ∼2.5–3.0 g of taxol .
Taxol was produced for the first time from endophytes in 1993 by Stierle et al.  using the endophytic fungus Taxomyces andreanae, which colonizes yew trees. Successive studies have been reported investigating endophytic fungi capable of producing taxol, such as Pestalotiopsis microspora isolated from the Himalayan yew (Taxus wallichiana) , Bartalinia robillardoides Tassi isolated from Indian bael (Aegle marmelos Correa ex Roxb) , Chaetomella raphigera isolated from Arjun tree (Terminalia arjuna) , Gliocladium sp. isolated from English yew (Taxus baccata) , Fusarium oxysporum from a mangrove tree (Rhizophora annamalayana) , Guignardia mangiferae isolated from Anglojap yew (Taxus media) , Fusarium redolens isolated from east Himalayan yew (Taxus baccata L. subsp. wallichiana Zucc.) , Phoma medicaginis isolated also from Himalayan yew (T. wallichiana var. mairei)  and Grammothele lineata isolated from Jute mallow (Corchorus olitorius) .
Most of the natural dyes are eco-friendly (nontoxic and nonpolluting), have low cost of production, are less hazardous to health , and usually causes no allergic reactions in comparison with synthetic dyes. Moreover, some of these natural dyes have extra advantages over synthetic dyes such as having antioxidant and antimicrobial activities ,.
Generally, the produced pigments were tested for their color stability, by applying the dye on a set of four pieces of cloth (cotton, silk, wool, and polyester), and then their color properties were characterized . Some mushroom extracts give colorful dyes such as Bankera violascens, which produces green dye; Agaricus arvensis, which generates blue shades; Chroogomphus vinicolor, which gives red dye; and Collybia iocephala, which gives a purple-blue dye . However, cultivating these mushrooms under laboratory conditions is very difficult, and hence such mushrooms are not suitable for industrial production of dyes.
On the contrary, many ascomycetous and basidiomycetous fungi produce pigments such as anthraquinones, anthraquinone carboxylic acids and pre-anthraquinones as secondary metabolites, and these pigments can be extracted and then used in industries such as textile dying, cosmetics, as a food coloring ingredient, and in pharmaceuticals . Some dematiaceous fungi such as Curvularia lunata and Alternaria alternata produce stable pigments used in textile dyeing , Monascus roseus produces pink to orange shades , Helminthosporium avenae produces bronze coloration , Penicillium purpurogenum produces red dye  and Paecilomyces sinclairii produces red dye .
Endophytes participate also in pigment production. A red dye was produced by an endophytic fungus identified as Penicillium sp., isolated from the leaves of the medicinal plant Polygonum multiflorum . The reddish orange pigment lawsone (hennotannic acid) was produced by the endophytic fungus Gibberella moniliformis isolated from the leaf tissues of henna tree .
Biodegradation of polymers
Fungi have the most sophisticated and complex enzymatic machinery that are involved in countless applications in all biotechnological fields, owing to their magical capability of performing chemically difficult reactions. An example of the use of fungal enzymes is plastic biodegradation. Hence, fungi have been screened for their ability to degrade polymers. Many species were capable of doing such a mission, thanks to laccase enzymes, which have nonspecific oxidative action mechanism . Myceliophthora sp. is one of the most potent reported fungi so far in terms of its ability to biodegrade polymer through metabolizing insoluble polymer and partially solubilizing it .
Laccases are used also in the detoxification of pollutants and in bioremediation of phenolic and nonphenolic compounds . Moreover, these enzymes can successfully biodegrade wood, azo dyes , and jet fuel into simple compounds that can be used as nutrients. Moreover, these enzymes are involved in pulp delignification, in paper processing, in textile industry to improve the whiteness during conventional bleaching of cotton , and in the synthesis of some fine chemicals ,,,.
Laccases were produced by many endophytes such as Monotospora sp., isolated from Bahama grass (Cynodon dactylon) , Colletotrichum gloeosporioides gr. Isolated from Piper beetle , Daldinia sp. isolated from the leaves of Himalayan cypress (Cupressus torulosa) , and Myrothecium verrucaria isolated from pigeon pea .
Other enzymes used in applications
According to global markets, enzymes occupy an extremely important position in terms of sales as biotechnological tools. Enzymes are involved in leather tanning, starch and food processing, textile industry, protein hydrolysis, pharmaceutical and chemical manufacturing, detergent production, and as biofuel ,,,,,,,. Moreover, many enzymes are involved in biodegradation of residual wastes ,, and in detoxification of heavy metals and many other toxic compounds ,.
Many fungi are capable of producing more than one enzyme efficiently; here, we will focus on some enzyme production, such as proteases, which are one of the largest and most diverse families of enzymes occupying a superior position in the list of total worldwide enzyme sales . Proteases have a wide range of applications especially as analytical tools in basic research and molecular biology , peptides synthesis , leather processing , detergent production , meat tenderization , cheese manufacture, pharmaceutical industry , and many other industrial applications ,. Endophytes such as Acremonium typhinum isolated from Poa ampla secrete proteinase , whereas F. oxysporum isolated from Musa sp. (Banana); A. alternate, isolated from Eremophila longifolia (Berrigan), and A. alternata isolated from gymnosperm tree C. torulosa (Himalayan cypress) produce protease ,,.
On the contrary, fungal pectinases represent ∼25% of the sales of global food and industrial enzymes . Pectinases are involved in many industrial applications such as improving extraction of juices  and decreasing the viscosity of fruit juices . They have other applications related to plant–fungal interactions . Generally, pectinases are secreted by endophytes to facilitate their entrance through the cell wall of the host plant . Aspergilli were the most potent genera used for commercial production of pectinases in the field of food processing . Many endophytic fungi have the ability to synthesis pectinases such as Talaromyces sp. isolated from the medicinal plant Calophyllum inophyllum (Alexandrian laurel balltree) , and Aspergillus japonicus isolated from Opuntia ficus-indica Mill. (Forage cactus) .
Another example of the important enzyme group is amylases, which are also ranked among the most important enzymes used in many biotechnological, food and pharmaceutical applications, especially those concerned with starch hydrolysis and cyclodextrin production . Amylases were secreted by endophytes such as Discosia sp. isolated from C. inophyllum (Alexandrian laurel balltree) , Cylindrocephalum sp. isolated from Alpinia calcarata (Haw.) Roscoe (Cardamom ginger) , and Preussia minima isolated from E. longifolia (berrigan) .
There is an endless list of enzymes used enormously in various fields, and fungi are the ideal producers of such enzymes. Therefore, research and screening for new fungal isolates that produce enzymes, investigating new biotechnological application, and studying those enzymes biochemical characteristics might lead to identification of novel enzymes with novel and improved applications.
Antimicrobial and antiviral activities
Many reports have described endophytic fungi exerting antimicrobial activities ,, such as Phomopsis sp., which produces phomopsichalasin ; the antifungal compound, cryptocandin, produced by Cryptosporiopsis cf. quercina ; and the antiparasitic metabolite, cercosporin, produced by Mycosphaerella sp. . On the contrary, cytonic acid A and B were isolated from Cytonaema sp. These compounds are inhibitor of human cytomegalovirus protease .
Endophytes as biocontrol agents and plant growth promoters
Endophytes can protect and promote the growth of their host plant in different ways such as by synthesizing phytohormones, increasing their host plant tolerance to external stress, inducing its defense system, and/or acting as a biocontrol agent that vanquishes pathogen threats in their host plant ,,,. Many endophytes were reported to inhibit specific plant pathogens in vivo and in vitro. For example, C. gloeosporioides isolated from Cacao is used to biologically control Phytophthora sp. and Moniliophthora roreri, causing frosty pod rot and witches broom diseases in cacao, respectively . Plants pathogens Aspergillus flavus and Fusarium verticillioides were sensitive to Pyrrocidines A and B produced by the endophytic fungus, Acremonium zeae, isolated from maize . Phomopsis cassiae secretes cadinane sesquiterpenes that protects its host Cassia spectabilis from the pathogenicity of Cladosporium sphaerospermum, and C. cladosporioides . Trichoderma harzianum isolated from onion stalks showed antagonistic activity in vitro against the onion purple blotch pathogen Alternaria porri .
On the contrary, endophytes have a well-established role as an economical and eco-friendly plant growth promoter, which leads to an increase in crop production . For example, the endophytic fungus Piriformospora indica isolated from roots of many plants was commonly used as a plant growth promoter .
There are unlimited uses of the numerous promising secondary metabolites originated and secreted by endophytes, and many examples are listed in [Table 1]. The chemical structures of some of these important metabolites are illustrated in [Figure 2]. Screening and isolation of new endophytes can be the low-cost alternative for many currently used compounds. More studies are encouraged to understand and investigate metabolites secreted by these microorganisms and study activities and action mechanisms of novel ones, in addition to elucidating the relation between these endophytes and their host plant. Finally, further work is required to commercialize the production of biologically active compounds by endophytic fungi.
|Table 1 List of some endophytes, their host plants, and their isolated biologically active metabolites|
Click here to view
|Figure 2 Chemical structure of some important metabolites produced by endophytic mycobiota.|
Click here to view
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
(DUPHAT 2019: www.duphat.ae)
| References|| |
Zhang HW, Song YC, Tan RX. Biology and chemistry of endophytes. Nat Prod Rep 2006; 23:753–771.
Rodriguez RJ, White JF, Arnold AE, Redman RS. Fungal endophytes: diversity and functional roles. New Phytologist 2009; 182:314–330.
Rodriguez RJ, Redman RS, Henson JM. The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adapt Strat Global Change 2004; 9:261–272.
Redman RS, Sheehan KB, Stout RG, Rodrigues RJ, Henson JM. Thermotolerance conferred to plant host and fungal endophyte during mutualistic symbiosis. Science 2002; 298:1581.
Krings M, Taylor TN, Hass H, Kerp H, Dotzler N, Hermsen EJ. Fungal endophytes in a 400-million-yr-old land plant: infection pathways, spatial distribution, and host responses. New Phytol 2007; 174:648–657.
Strobel GA, Dirkse E, Sears J, Markworth C. Volatile antimicrobials from Muscodor albus
, a novel endophytic fungus. Microbiology 2001; 147:2943–2950.
Arnold AE, Mejia IC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA. Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 2003; 100:15649–15654.
Ownley BH, Gwinn KD, Vega FE. Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. BioControl 2010; 55:113–128.
Frohlich J, Hyde K, Petrini O. Endophytic fungi associated with palms. Mycol Res 2000; 104:1202–1212.
Alva P, McKenzie EH, Pointing SB, Muralla R, Hyde KD. Do sea grasses harbour endophytes?. Fungal Divers Res Series 2002; 7:167–178.
Li WC, Zhou J, Guo SY, Guo LD. Endophytic fungi associated with lichens in Baihua mountain of Beijing, China. Fungal Divers 2007; 25:69–80.
Elkhateeb WA. Some mycological, phytopathological and physiological studies on mycobiota of selected newly reclaimed soils in Assiut governorate, Egypt [master thesis]. Assiut, Egypt: Faculty of Science, Assiut University (Doctoral dissertation). 2005.
dos Santos S, dos Santos T. Endophytic fungi in economically important plants: ecological aspects, diversity and potential biotechnological applications. J Bioenergy Food Sci 2017; 4:113–126.
Mayer AM, Rodriguez AD, Berlinck RG, Fusetani N. Marine pharmacology in 2007-2008: marine compounds with antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiprotozoal, antituberculosis, and antiviral activities; affecting the immune and nervous system, and other miscellaneous mechanisms of action. Comp Biochem Physiol Toxicol Pharmacol 2011; 153:191–222.
Elkhateeb WA, Zohri AA, Mazen MB, Hashem M, Daba GM. Investigation of diversity of endophytic, phylloplane and phyllosphere mycobiota isolated from different cultivated plants in new reclaimed soil, Upper Egypt with potential biological applications. Int J MediPharm Res 2016; 2:23–31.
Korpi A, Järnberg J, Pasanen AL. Microbial volatile organic compounds. Crit Rev Toxicol 2009; 39:139–193.
Barrett AJ, Rawlings ND, Woessner JF. The handbook of proteolytic enzymes. 2nd ed. London: Academic Press; 2003.
Corrêa RC, Rhoden SA, Mota TR, Azevedo JL, Pamphile JA, de Souza CGM et al.
Endophytic fungi: expanding the arsenal of industrial enzyme producers. J Ind Microbiol Biotechnol 2014; 41:1467–1478.
Kasaei A, Mobini-Dehkordi M, Mahjoubi F, Saffar B. Isolation of taxol-producing endophytic fungi from Iranian yew through novel molecular approach and their effects on human breast cancer cell line. Curr Microbiol 2017; 74:702–709.
Wani MC, Taylor HL, Wall ME, Coggon P, McPhail AT. Plant antitumor agents. VI. Isolation and structure of taxol, a novel antileukemic and antitumor agent from Taxus brevifolia
. J Am Chem Soc 1971; 93:2325–2327.
Diaz JF, Barasoain I, Souto AA, Amat-Guerri F, Andreu JM. Macromolecular accessibility of fuorescent toxoids bound at a paclitaxel binding site in the microtubule surface. J Biol Chem 2005; 280:3928–3937.
Zhou X, Zhu H, Liu L, Lin J, Tang K. A review: recent advances and future prospects of Taxol-producing endophytic fungi. Appl Microbiol Biotechnol 2010; 86:1707–1717.
Somjaipeng S, Medina A, Magan N. Environmental stress and elicitors enhance taxol production by endophytic strains of Paraconiothyrium variabile
and Epicoccum nigrum
. Enzyme Microbiol Tech 2016; 90:69–75.
Bedi YS, Ogra RK, Koul K, Kaul BL, Kapil RS. Yew (Taxus
spp.). A new look on utilization, cultivation and conservation. In Handa SS, Kaul MK, eds. Supplement to cultivation and utilization of medicinal plants. Jammu-Tawi, India: Regional Research Laboratory; 1996. 443–456.
Stierle A, Strobel G, Stierle D. Taxol and taxane production by Taxomyces andreanae
, an endophytic fungus of Pacific yew. Science 1993; 260:214–216.
Strobel GA, Yang XS, Sears J, Robert K, Sidhu RS, Hess WH. Taxol from Pestalotiopsis microspora
, an endophytic fungus of Taxuus wallachiana
. Microbiology 1996; 142:435–440.
Gangadevi V, Muthumary J. Taxol, An anticancer drug produced by an endophytic fungus Bartalinia robillardoides
Tassi, isolated from a medicinal plant, Aegle marmelos
Correa ex Roxb. World J Microbiol Biotechnol 2007; 23:1653–1808.
Gangadevi V, Muthumary J. A novel endophytic Taxol-producing fungus Chaetomella raphigera
isolated from a medicinal plant, Terminalia arjuna
. Appl Biochem Biotechnol 2009; 158:675–684.
Sreekanth D, Sushim GK, Syed A, Khan BM, Ahmad A. Molecular and morphological characterization of a Taxol-producing endophytic fungus, Gliocladium
sp., from Taxus baccata
. Mycobiology 2011; 39:151–157.
Elavarasi A, Rathna GS, Kalaiselvam M. Taxol producing mangrove endophytic fungi Fusarium oxysporum
from Rhizophora annamalayana
. Asian Pac J Trop Biomed 2012; S1081–S1085.
Xiong ZQ, Yang YY, Zhao N, Wang Y. Diversity of endophytic fungi and screening of fungal paclitaxel producer from Anglojap yew, Taxus x media
. BMC Microbiol 2013; 13:71.
Garyali S, Reddy MS. Taxol production by an endophytic fungus, Fusarium redolens
, isolated from Himalayan yew. J Microbiol Biotechnol 2013; 23:1372–1380.
Zaiyou J, Li M, Xiqiao H. An endophytic fungus efficiently producing paclitaxel isolated from Taxus wallichiana
var. mairei. Medicine 2017; 96:1–4.
Das A, Rahman MI, Ferdous AS, Rahman MM, Nahar N, Uddin MA et al.
An endophytic Basidiomycete, Grammothele lineata
, isolated from Corchorus olitorius
, produces paclitaxel that shows cytotoxicity. PloS ONE 2017; 12:e0178612.
Nelson D, Maria FS, Roseli D, Elisa E. Ecological friendly pigments from fungi. Crit Rev Food Sci Nut 2002; 42:53–66.
Vendruscolo F, Tosin I, Giachini AJ, Schmidell W, Ninow JL. Antimicrobial activity of Monascus
pigments produced in submerged fermentation. J Food Process Preserv 2014; 38:1860–1865.
Mani VM, Priya MS, Dhaylini S, Preethi K. Antioxidant and antimicrobial evaluation of bioactive pigment from Fusarium
sp. isolated from stressed environment. Int J Curr Microbiol Appl Sci 2015; 4:1147–1158.
Aishwarya A. Extraction of natural dyes from fungus − an alternate for textile dyeing. J Natl Sci Res 2014; 4:1–6.
Korumilli T. Studies on pigment production by microorganisms using raw materials of agro-industrial origin [doctoral dissertation, Orissa, India]. 2015.
Mapari SA, Nielsen KF, Larsen TO, Frisvad JC, Meyer AS, Thrane U. Exploring fungal biodiversity for the production of water-soluble pigments as potential natural food colorants. Curr Opin Biotechnol 2005; 16:231–238.
Sharma P, Jha AB, Dubey RS, Pessarakli M. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012; 2012:1–26.
Malik K, Tokkas J, Goyal S. Microbial pigments: a review. Int J Microbial Res Technol 2012; 1:361–365.
Mendez A, Pérez C, Montañéz JC, Martínez G, Aguilar CN. Red pigment production by Penicillium purpurogenum
GH2 is influenced by pH and temperature. J Zhejiang Uni Sci B 2011; 12:961–968.
Cho YJ, Park JP, Hwang HJ, Kim SW, Choi JW, Yun JW. Production of red pigment by submerged culture of Paecilomyces sinclairii
. Lett Appl Microbiol 2002; 35:195–202.
Jiang Y, Li HB, Chen F, Hyde KD. Production potential of water-soluble Monascus
red pigment by a newly isolated Penicillium
sp. J Agric Sci Technol 2005; 1:113–126.
Sarang H, Rajani P, Vasanthakumari MM, Kumara PM, Siva R, Ravikanth G, Shaanker RU. An endophytic fungus, Gibberella moniliformis
from Lawsonia inermis
L. produces lawsone, an orange-red pigment. Antonie Van Leeuwenhoek 2017; 110:853–862.
Claus H. Laccases: structure, reactions, distribution. Micron 2004; 35:93–96.
Mohammad IK, Nadeem AR, Riyadh KA. Biodegradation of polymers by fungi isolated from plastic garbage and the optimum condition assessment of growth, Biology Department, College of Science, Mosul University. J Raf Env 2013; 1:33–43.
Chanyal S, Agrawal PK. Preliminary screening for laccase producing endophytic fungi from Cupressus Torulosa
D. Don Int J Sci Eng Manage 2016; 1:85–89.
Blanquez P, Casas N, Font X, Gabarrell X, Sarra M, Caminal G, Vicent T. Mechanism of textile metal dye biotransformation by Trametes versicolor
. J Water Res 2004; 38:2166–2172.
Agrawal SC. Decolorization of textile dye by laccase from newly isolated endophytic fungus Daldiniasp
. Kavaka 2017; 48:33–41.
Viswanath B, Subhosh Chandra M, Pallavi H, Rajasekhar Reddy B. Screening and assessment of laccase producing fungi isolated from different environmental samples. Afr J Biotechnol 2008; 7:1129–1133.
Shraddha RS, Sehgal MK, Kumar A. Laccase: microbial sources, production, purification, and potential biotechnological applications. Enzyme Res 2011; 2011:1–11.
Singh G, Bhalla A, Kaur P, Capalash N, Sharma P. Laccase from prokaryotes: a new source for an old enzyme. Rev Environ Sci Biotechnol 2011; 10:309–326.
Buddolla V, Bandi R, Avilala J, Arthala PK, Golla N. Fungal laccases and their applications in bioremediation. Enzyme Res 2014; 2014:1–21.
Wang JW, Wu JH, Huang WY, Tan RX. Laccase production by Monotospora
sp., an endophytic fungus in Cynodon dactylon. Bioresource Tech 2006; 97:786–789.
Sidhu AK, Agrawal SB, Sable VS, Patil SN, Gaikwad VB. Isolation of Colletotrichum gloeosporioides
gr., a novel endophytic laccase producing fungus from the leaves of a medicinal plant, Piper betle
. Int J Sci Eng Res 2014; 5:1087–1096.
Sun J, Guo N, Niu LL, Wang QF, Zang YP, Zu YG, Fu YJ. Production of laccase by a new Myrothecium verrucaria
MD-R-16 isolated from pigeon pea [Cajanus cajan
(L.) Millsp.], and its application on dye decolorization. Molecules 2017; 22:673.
Kamini NR, Hemachander C, Mala JG, Puvanakrishnan R. Microbial enzyme technology as an alternative to conventional chemicals in leather industry. Curr Sci 1999; 77:80–86.
James J, Simpson BK, Marshall MR. Application of enzymes in food processing. Crit Rev Food Sci Nutr 1996; 36:437–463.
Aehle W, ed. Enzymes in industry: production and applications. United States: John Wiley & Sons; 2007.
Schmid A, Hollmann F, Park JB, Bühler B. The use of enzymes in the chemical industry in Europe. Curr Opin Biotechnol 2002; 13:359–366.
Wells AS, Finch GL, Michels PC, Wong JW. Use of enzymes in the manufacture of active pharmaceutical ingredients, a science and safety-based approach to ensure patient safety and drug quality. Org Process Res Dev 2012; 16:1986–1993.
Kim S, Jiménez-González C, Dale BE. Enzymes for pharmaceutical applications − a cradle-to-gate life cycle assessment. Int J Life Cycle Ass 2009; 14:392–400.
Yeoman CJ, Han Y, Dodd D, Schroeder CM, Mackie RI, Cann IK. Thermostable enzymes as biocatalysts in the biofuel industry. Adv Appl Microbiol 2010; 70:1–55.
Choi YW, Hodgkiss IJ, Hyde KD. Enzyme production by endophytes of Brucea javanica
. J Agric Sci Tech 2005; 1:55–66.
Pérez J, Munoz-Dorado J, de la Rubia TD, Martinez J. Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview. Int Microbiol 2002; 5:53–63.
Chakrabarty AM. Biodegradation and detoxification of environmental pollutants. United Kingdom: CRC Press; 2017.
Sogorb MA, Vilanova E. Enzymes involved in the detoxification of organophosphorus, carbamate and pyrethroid insecticides through hydrolysis. Toxicol Lett 2002; 128:215–228.
Torres E, Bustos-Jaimes I, Le Borgne S. Potential use of oxidative enzymes for the detoxification of organic pollutants. Appl Catal B Environ 2003; 46:1–15.
Nirmal NP, Shankar S, Laxman RS. Fungal proteases: an overview. Int J Biotechnol Biosci 2011; 1:1–40.
Mótyán JA, Tóth F, Tőzsér J. Research applications of proteolytic enzymes in molecular biology. Biomolecules 2013; 3:923–942.
Schellenberger V, Jakubke HD. Protease‐catalyzed kinetically controlled peptide synthesis. Angewandte Chem 1991; 30:1437–1449.
Dayanandan A, Kanagaraj J, Sounderraj L, Govindaraju R, Rajkumar GS. Application of an alkaline protease in leather processing: an ecofriendly approach. J Clean Prod 2003; 11:533–536.
Maurer KH. Detergent proteases. Curr Opin Biotechnol 2004; 15:330–334.
Bekhit AA, Hopkins DL, Geesink G, Bekhit AA, Franks P. Exogenous proteases for meat tenderization. Crit Rev Food Sci Nutr 2014; 54:1012–1031.
Yamamoto A, Taniguchi T, Rikyuu K, Tsuji T, Fujita T, Murakami M, Muranishi S. Effects of various protease inhibitors on the intestinal absorption and degradation of insulin in rats. Pharm Res 1994; 11:1496–1500.
Godfrey T, West S. Textiles. Industrial enzymology. 2nd ed. London, UK: Macmillan Press; 1996. 360–371.
Sawant R, Nagendran S. Protease: an enzyme with multiple industrial applications. World J Pharm Sci 2014; 3:568–579.
Lindstrom JT, Sun S, Belanger FC. A novel fungal protease expressed in endophytic infection of Poa
species. Plant Physiol 1993; 102:645–650.
Ng’ang’a MP, Kahangi EM, Onguso JM, Losenge T, Mwaura P. Analyses of extra-cellular enzymes production by endophytic fungi isolated from bananas in Kenya. Afr J Hortic Sci 2011; 5:1–8.
Zaferanloo B, Quang TD, Daumoo S, Ghorbani MM, Mahon PJ, Palombo EA. Optimization of protease production by endophytic fungus, Alternaria alternata
, isolated from an Australian native plant. World J Microbiol Biotechnol 2014; 30:1755–1762.
Rajput K, Chanyal S, Agrawal PK. Optimization of protease production by endophytic fungus, Alternaria alternata
isolated from gymnosperm tree-Cupressus torulosa
D. Don World J Pharm Sci 2016; 5:1034–1054.
Sunitha VH, Devi DN, Srinivas C. Extracellular enzymatic activity of endophytic fungal strains isolated from medicinal plants. World J Agric Sci 2013; 9:1–9.
Joshi VK, Parmar M, Rana N. Purification and characterization of pectinase produced from apple pomace and evaluation of its efficacy in fruit juice extraction and clarification. Ind J Nat Prod Resorce 2011; 2:189–197.
Kashyap DR, Vohra PK, Chopra S, Tewari R. Applications of pectinases in the commercial sector: a review. Bioresour Technol 2001; 77:215–227.
Gummadi SN, Panda T. Purification and biochemical properties of microbial pectinases: a review. Process Biochem 2003; 38:987–996.
Perombelon M, Hadley G. Production of pectic enzymes by pathogenic and symbiotic Rhizoctonia
strains. New Phytol 1965; 64:144–151.
Koyani RD, Rajput KS. Solid state fermentation: comprehensive tool for utilization of lignocellulosic through biotechnology. J Bioprocess Biotech 2015; 5:258.
Sunitha VH, Ramesha A, Savitha J, Srinivas C. Amylase production by endophytic fungi Cylindrocephalum
sp. isolated from medicinal plant Alpinia calcarata
(Haw.) Roscoe. Braz J Microbiol 2012; 43:1213.
Bezerra JD, Santos MG, Svedese VM, Lima DM, Fernandes MJ, Paiva LM, Souza-Motta CM. Richness of endophytic fungi isolated from Opuntia ficus-indica
Mill. (Cactaceae) and preliminary screening for enzyme production. World J Microbiol Biotechnol 2012; 28:1989–1995.
Aiyer PV. Amylases and their applications. Afr J Biotechnol 2005; 4:1525–1529.
Hegde S, Ramesha A, Srinvas C. Optimization of amylase production from an endophytic fungi Discosia
sp. isolated from Calophyllum inophyllum
. Int J Agric Technol 2011; 7:805–813.
Zaferanloo B, Virkar A, Mahon P, Palombo E. Endophytes from an Australian native plant are a promising source of industrially useful enzymes. World J Microbiol Biotechnol 2013; 29:335–345.
Silva GH, Oliveira CM, Teles HI, Bolzani VS, Araujo AR, Pfenning IH et al.
Citocalasinas produzidas por Xylaria
sp., um fungo endofítico de Piper aduncum (piperaceae). Química Nova 2010; 33:2038–2041.
Budhiraja A, Nepali K, Sapra S, Gupta S, Kumar S, Dhar KL. Bioactive metabolites from an endophytic fungus of Aspergillus
species isolated from seeds of Gloriosa superba
Linn. Med Chem Res 2013; 22:323–329.
Horn WS, Simmonds MS, Schwartz RE, Blaney WM. Phomopsichalasin, a novel antimicrobial agent from an endophytic Phomopsis
sp. Tetrahedron 1995; 51:3969–3978.
Strobel GA, Miller RV, Martinezmiller C, Condron MM, Teplow DB, Hess WM. Cryptocandin, a potent antimycotic from the endophytic fungus Cryptosporiopsis
cf. quercina. Microbiology 1999; 145:1919–1926.
Moreno E, Varughese T, Spadafora C, Arnold E, Coley PD, Kursar TA et al.
Chemical constituents of the new endophytic fungus Mycosphaerella
sp. nov. and their anti-parasitic activity. Nat Prod Commun 2011; 6:835–840.
Guo B, Dai Jin-Rui Ng, Huang Y, Leong C, Ong W, Carte BK. Cytonic acids A and B: novel tridepside inhibitors of hCMV protease from the endophytic fungus Cytonaema species. J Nat Prod 2000; 63:602–604.
Waqas M, Khan AL, Hamayun M, Shahzad R, Kang SM, Kim JG, Lee IJ. Endophytic fungi promote plant growth and mitigate the adverse effects of stem rot: an example of Penicillium citrinum
and Aspergillus terreus
. J Plant Interact 2015; 10:280–287.
Khan AR, Ullah I, Waqas M, Shahzad R, Hong SJ, Park GS et al.
Plant growth-promoting potential of endophytic fungi isolated from Solanum nigrum
leaves. World J Microbiol Biotechnol 2015; 31:1461–1466.
Paguia EF, Valentino MJ. Seed germination promoting activity of fungal endophytes in rice (Oryza sativa L
.) seeds. Asian J Plant Sci Res 2016; 6:37–39.
Mejía LC, Rojas EI, Maynard Z, Van Bael S, Arnold AE, Hebbar P et al.
Endophytic fungi as biocontrol agents of Theobroma cacao
pathogens. Biol Control 2008; 46:4–14.
Wicklow DT, Roth S, Deyrup ST, Gloer JB. A protective endophyte of maize: Acremonium zeae
antibiotics inhibitory to Aspergillus flavus
and Fusarium verticillioides
. Mycol Res 2005; 109:610–618.
Silva GH, Teles HL, Zanardi LM, Marx Young MC, Eberlin MN, Hadad R et al.
Cadinane sesquiterpenoids of Phomopsis cassiae
, an endophytic fungus associated with Cassia spectabilis
(Leguminosae). Phytochemistry 2006; 67:1964–1969.
Abo-elyousr KA, Abdel-hafez SI, Abdel-rahim IR. Isolation of Trichoderma
and evaluation of their antagonistic potential against Alternaria porri
. J Phytopathol 2014; 162:567–574.
Sekar S. Plant growth promoter and biocontrol mechanism of endophytic fungi Botrytis
sp. Braz J Biol Sci 2015; 2:221–233.
Kumar M, Yadav V, Kumar H, Sharma R, Singh A, Tuteja N, Johri AK. Piriformospora indica
enhances plant growth by transferring phosphate. Plant Signal Behav 2011; 6:723–725.
Weber D, Gorzalczany S, Martino V, Acevedo C, Sterner O, Anke T. Metabolites from endophytes of the medicinal plant Erythrina crista-galli
. Z Naturforsch C 2005; 60:467–477.
Strobel GA, Ford E, Worapong J, Harper JK, Arif AM, Grant D et al.
Ispoestacin, an isobenzofuranone from Pestalotiopsis microspora
, possessing antifungal and antioxidant activities. Phytochemistry 2002; 60:179–184.
Leuchtman A. In White J, Bacon CW, Hywel-Jones NL, Spatafora JW, eds. Natural products from plant associated endophytic fungi. New York, NY, USA: Marcel-Dekker. 2003; 341–175.
Raghunath R, Radhakrishna A, Angayarkanni J, Palaniswamy M. Production and cytotoxicity studies of lovastatin from Aspergillus niger
PN2 an endophytic fungi isolated from Taxus baccata
. Int J Appl Biol 2012; 3:342–351.
Zhang Q, Xiao J, Sun QQ, Qin JC, Pescitelli G, Gao JM. Characterization of cytochalasins from the endophytic Xylaria
sp. and their biological functions. J Agric Food Chem 2014; 62:10962–10969.
Lee JC, Lobkovsky E, Pliam NB, Strobel G, Clardy J. Subglutinols A and B: immunosuppressive compounds from the endophytic fungus Fusarium subglutinans
. J Organic Chem 1995; 60:7076–7077.
Ge HM, Shen Y, Zhu CH, Tan SH, Ding H, Song YC, Tan RX. Penicidones A-C, three cytotoxic alkaloidal metabolites of an endophytic Penicillium
sp. Phytochemistry 2008; 69:571–576.
Strobel GA, Knighton B, Kluck K, Ren Y, Livinghouse T, Griffin M et al.
The production of myco-diesel hydrocarbons and their derivatives by the endophytic fungus Gliocladium roseum
(NRRL 50072). Microbiology 2008; 154:3319–3328.
Hassan SED. Plant growth-promoting activities for bacterial and fungal endophytes isolated from medicinal plant of Teucrium polium
L. J Adv Res 2017; 8:687–695.
Chen JL, Sun SZ, Miao CP, Wu K, Chen YW, Xu LH et al.
Endophytic Trichoderma gamsii
YIM PH30019: a promising biocontrol agent with hyperosmolar, mycoparasitism, and antagonistic activities of induced volatile organic compounds on root-rot pathogenic fungi of Panax notoginseng. J Ginseng Res 2016; 40:315–324.
Campos FF, Rosa LH, Cota BB, Caligiorne RB, Rabello ALT, Alves TMA et al.
Leishmanicidal metabolites from Cochliobolus
sp., an endophytic fungus isolated from Piptadenia adiantoides
(Fabaceae). PLoS Negl Trop Dis 2008; 2:e348.
[Figure 1], [Figure 2]