A REVIEW OF THE MUTUALISTIC RELATIONSHIP OF ENDOPHYTIC FUNGI FOR THE PRODUCTION OF BIOACTIVE METABOLITES
HTML Full TextA REVIEW OF THE MUTUALISTIC RELATIONSHIP OF ENDOPHYTIC FUNGI FOR THE PRODUCTION OF BIOACTIVE METABOLITES
Mohd Azharuddin *, Mohammad Saad and Amol R. Kharat
Department of Pharmacognosy, Government College of Pharmacy, Aurangabad, Maharashtra, India.
ABSTRACT: Endophytes constitute a remarkably multifarious group of microorganisms ubiquitous in plants and maintain an imperceptible association with their hosts for at least a part of their life cycle. Their enormous biological diversity, coupled with their capability to biosynthesize bioactive secondary metabolites, has provided the impetus for a number of investigations on endophytes. There is a need to search new ecological niches for the potential of natural bioactive agents for different pharmaceutical, agriculture, and industrial application; these should be renewable, eco-friendly, and easily obtainable natural products discovery in the search for new drugs and is the most potent source for the discovery of novel bioactive compounds. Therefore, a large number of bioactive compounds are isolated from plants, bacteria, fungi, and many other organisms. Endophytic fungi, the most promising of these, have been a source of various such bioactive compounds. Many of these compounds are being used for the treatment of a number of diseases. This review emphasis on the biology of fungal endophytes, their discovery, isolation, identification by morphological and molecular methods, production, purification and structure elucidation of the bioactive compounds.
Keywords: Fungal endophytes, Endophytic fungi, Antimicrobial, Bioactive compounds, Endophytism, Isolation, Bioactive compounds, Structural elucidation
INTRODUCTION: Fungi are important components in every ecosystem, intimately associated with crucial processes like the decomposition, recycling and transportation of nutrients in different environments. It has been estimated that there may be over a million different fungal species on this Earth, of which only a small fraction [approx. 5%] have been identified 1. There are also many bacteria that exist as plant endophytes; in most instances, they coexist with endophytic fungi.
The existence of endophytes has been known for over one hundred years. They live as imperfect fungi most of the time and have been described as benign parasites or true symbionts. It has been suggested that they can influence the host plants' distribution, ecology, physiology, and biochemistry 2. Botanists have conducted much research about the relationship of plant endophytes, especially for grasses such as tall fescue, where it has been exhibited that endophytes produce toxins that discourage insects and other grazing animals 3.
It wasn’t until the past decade that endophytes were extensively studied for their potential as novel sources of effective new drugs. Microbes, both fungi, and bacteria, have provided modern medicine or drugs with valuable, effective treatments, including penicillin from the fungus Penicillium notatum and bacitracin from Bacillus subtilis, a common bacterium. Additionally, a potent chemotherapeutic agent, taxol is synthesized by an endophyte of the Pacific Yew tree. Endophytes represent a huge diversity of microbial adaptations that have developed in special and sequestered environments. Their diversity and specialized habituation make them an exciting field of study in the search for new medicines or novel drug-like molecules. The hunt for new drugs is particularly important in view of the fact that so many microorganisms are developing resistance to some of the current drugs. Endophytic fungi are a group of fungi that colonize living and internal tissues of plants without causing any immediate, overt negative effects 4. Recent studies have revealed these fungi's ubiquity, with an estimated 1 million species of endophytic fungi residing in plants 5 and even lichen 6. Endophytic fungi represent an important and quantifiable component of fungal biodiversity and are known to affect plant community diversity and structure 7. According to 1, only about 100,000 fungal species have been described out of a conservative estimate of 1.5 million. Recent studies of endophytic fungi from tropical and temperate forests support the high estimates of species diversity 8-10.
Relationship between Endophytic Fungi and Host Plant: A variety of relationships exist between fungal endophytes and their host plants, ranging from mutualistic or symbiotic to antagonistic or slightly pathogenic 11. Endophytes may produce an overabundance of substances of potential use in agriculture, industry, and modern medicine such as novel antibiotics, antimycotics, immunosuppressant and anticancer compounds. In addition, the studies of endophytic fungi and their relationships with host plants will shed light on the ecology and evolution of both the endophytes and their hosts: the evolution of endophyte plant symbioses; the ecological factors that influence the direction and strength of the endophyte host plant interaction. Since, natural products are likely adapted to a specific function in nature, searching for novel secondary metabolites should concentrate on organisms that inhabit novel biotopes 12.
TABLE 1: INFLUENCES OF HOST MEDICINAL PLANTS ON THE POPULATION STRUCTURE OF ENDOPHYTIC FUNGI 13-15
Family of host plants (represent species) | Isolation part | Habitat | Factor affecting the population structure |
Cactaceae (Cactus sp.) | Stem | Desert of tropical savanna | Environment: moisture and temperature |
Rosaceae (Malus
domestica) |
Leaf, flower, fruit | Tropical rainy region | Environment: cultivation style |
Leguminosae (Glycyrrhiza inflat) | Root | Salinized sandy land in warm temperate region | Environment: moisture and temperature |
Eucommiaceae (Eucommia ulmoides) | Leaf, branch, bark | Subtropical mountain and warm temperate semi-humid region | Environment: latitude and temperature
Tissue |
Orchidaceae (Gastrodia
elata) |
Tuber, flower | Hillside forests, wetland in
temperate plateau |
Enviroment: latitude
Tissue |
Euphorbiaceae (Sapium
sebiferum) |
Leaf, twig | Mountain in subtropics | Genetic background
Tissue |
Smilacaceae (Heterosmilax
japonica) |
Stem | Subtropical monsoon region | Season |
Pinaceae (Pinus
tabulaeformis) |
Bark, needle, xylem | Forests in warm temperate
semi-humid monsoon region |
Season
Tissue age |
Teaceae (Camellia japonica) | Leaf | Temperate secondary forest | Season
Tissue age |
Zingiberaceae (Amomum
siamense) |
Leaf, pseudostem, rhizome | Tropical monsoon forest | Tissue |
Compositae (Atractylodes
lancea) |
Rhizome | Mountain in subtropics | Tissue and age of tissue |
Asclepiadaceae (Calotropis
procera) |
Leaf | Garden bed | Tissue |
Classification of Endophytic Fungi: Schaechter (2011) 16 stated that endophytic fungi have frequently been divided into two groups based on differences in taxonomy, host range, colonization transmission patterns, tissue specificity and ecological function. Group one is the Clavicipitaceous endophytes (C-endophytes) which infect some grasses. Group two is the Nonclavicipitaceous endophytes (N Cendophytes). While Rodriguez et al., (2009) 17.
Clavicipitaceous Endophytes (Class I): The Clavicipitaceae is a family of fungi (Hypocreales; ascomycota) including free living and symbiotic species associated with insects and fungi or grasses, rushes and sedges 18.
Many of its members produce alkaloids that are toxic to animals and humans. European investigators first noted clavicipitaceous endophytes of grasses in the late 19th century in seeds of Lolium temulentum, L. arvense, L. linicolum and L. remotum 18.
Nonclavicipitaceous Endophytes (Class II): Traditionally NC-endophytes treated as a single functional group, while Rodriguez et al., (2009), 19, showed that NC-endophytes represent three distinct functional groups. Class II endophytes include the hyper diverse endophytic fungi associated with leaves of tropical trees as well as the highly diverse associates of above-ground tissues of nonvascular plants, seedless vascular plants, conifers and woody and herbaceous angiosperms in biomes ranging from tropical forests to boreal and Arctic/Antarctic communities 20.
FIG. 1: BIOTECHNOLOGY APPLICATION OF SECONDARY METABOLITES AND EXTRACELLULAR ENZYMES PRODUCED FROM ENDOPHYTIC FUNGI
TABLE 2: LIST OF SOME BIOACTIVE COMPOUNDS PRODUCED BY ENDOPHYTIC FUNGI POSSESSING BIOLOGICAL ACTIVITIES 21-26
Endophytic Fungi | Host Plant | Bioactive Compounds | Biological Properties | Activity Level |
Phomopsis sp. CFS42 | Cephalotaxus fortunei | Polyketides | Antifungal activity | MIC = 2.5 µg/mL |
Chaetomium globosum | Ginkgo biloba | Azaphilone alkaloids | Anticancer activity | IC50 = 53.4 µM |
Alternariaal ternata AE1 | Azadirachta indica | Phenolics and flavonoids | Antioxidant properties | IC50 = 38 µg/mL |
Mycosphaerella nawae ZJLQ129 | Smilax china | Amide derivative | Immunosuppressant activity | 30 and 300 nM |
Phomopsis sp. CGMCC No. 5416 | Achyranthes bidentata | Chromanones | Antiviral activity | IC50 =32.5 µg/ ml |
Gliocladium sp. MR41 | Culture collection | Polyols | Antitubercular properties | MIC = 3.13 µg/mL |
Penicillium roqueforti and
Trichoderma reesei |
Solanum surattense | Ferulic acid, cinnamic acid, quercetin, and rutin | Antibacterial activity | MBC = 2.5 µg/mL |
Trichoderma asperellum T1 | Culture collection | 6-pentyl-2H-pyran-2-one (6-PP) | Antifungal and plant | 61.31% Inhibition |
Cladosporium cladosporioides | Zygophyllum mandavillei | 3-phenylpropionic acid, 5j-hydroxyasperentin | Antifungal activity | MIC = 15.62 µg/mL |
Diaporthe phaseolorum 92C | Combretum lanceolatum | 18-Des-hydroxy Cytochalasin | Antiparasitic activity | IC50 = 50 µg/mL |
Phyllosticta capitalensi | Tibouchina granulosa | Brefeldin and heptelidic acid | Antiparasitic activity | IC50 = 50.13 µg/mL, |
Fusarium solani | Glycyrrhiza glabra | Fusarubin, 3-O-methylfusarubin, and javanicin | Antitubercular activity | MIC = 8 µg/mL |
Identification of Fungal Endophytes: Morphological identification of endophytic fungi by mycologists is a critical step 27.
TABLE 3: FUNGAL ENDOPHYTES ISOLATED FROM VARIOUS PLANTS 28-32
Host plant | Identified Endophytic fungus |
Oryza sativa | Alternaria alternata, Cladosporium tenuissimum, Epicoccum purpurescens, Fusarium equiseti, F. oxysporum, Hymenula cerealis, Phoma sorghina, Pleospora herbarum, Pythium sp., Trematosphaeria sp., Fusarium sp. Penicillium sp. Aspergillus sp. Paecilomyces sp. Pyricularia Sacc, Helminthos porium
sp. Yeast, Sterile mycelium |
Manilkara bidentata | Xylaria sp., Colletotrichumcras sipes, Pestalotiopsis
versicolor |
Lycopersicon esculentum | Alternaria alternata, Colletotrichum gloeosporioides, Cladosporium sp., Penicillium sp., Arthrinium sp., Chaetomium globosum, Colletotrichum coccodes, Nigrospora sphaerica, Phomopsis sp., Ulocladium
alternariae, Stemphyliumbotryosum |
Taxus cuspidate | Alternaria sp. |
Nothapodyt esfoetida | Neurospora sp. |
Camellia sinensis (Tea) | Fusarium sp., Penicillium sp., Diporthe sp.,
Schizophillum sp. |
Coffee | Aspergillus, Bipolaris, Cladosporium, Clonostachys, Colletotrichum, Epicoccum, Fusarium,Guignardia, Mycospharella, Phomopsis, Rosellinia, Talaromyces,
Trichoderma, Xylaria |
Quercus variabilis | Aspergillus sp., Penicillium sp., Alternaria sp.,
Cladosporium sp., Fusarium sp., Rhizoctonia sp. |
Azadira chtaindica | Phomopsisoblonga, Cladosporiumcladorsporioides, Pestalotiopsissp, Trochoderma sp., Aspergillus sp.,
Periconia, Stenella, Drechslera |
Huperzia serrata | Acremonium sp. |
Ananas ananassoides | Muscodorcrispans |
Jatrophacurcas | Leptosphaeria sp. |
Paris polyphylla var. Yunnanensis | Fusarium, Gliocladiopsisirregularis, Gliomastixmurorum var. murorum, Aspergillusfumigatus, Cylindrocarpon, Podospora sp., Plectosphaerellacucumerina, Pichiaguilliermondii, Neonectria
radicicola |
Foeniculum vulgare | Acremonium, Alternaria, Fusarium, Plectosporium |
Antiaris toxicaria | Trichothecium, acremonium, Rhizoctonia |
Iris germanica | Rhizopusoryzae |
Saussurea involucrate | Cylindrocarpan sp. Phoma sp., Fusarium sp. |
Dendrobium devonianum | Fusarium sp., Phoma sp., Epicoccumnigrum |
Podocarpus species | Aspergillus fumigates |
Hemionitisariflora | Several endophytic fungi |
Oryza granulate | Dothideomycetes, Arthrinium sp., Magnaporthe sp., Muscador sp. |
Actinidia macrosperma | Acremoniumfurcatum, Cylindrocarponpauciseptatum, Trichodermacitrinoviride, Paecilomycesmarquandii,
Chaetomiumglobosum |
Solanum cernuum Vell. | Arthrobotrysfoliicola, Colletotrichumgloeosporioides, Coprinellus radians, Glomerellaacutata, Diatrypellafrostii, Phomaglomerata, Mucor sp., Phlebiasubserialis, Phomamoricola, Phanerochaetesordida,
Colletotrichum sp. |
Methods for Isolation of Fungal Endophytes: Isolation by cutting of selected plant parts.
Isolation by Blender shaft. Isolation by Mortar and Pestle
TABLE 4: MEDIA USED FOR ISOLATION OF FUNGAL ENDOPHYTES 33
Media Name | Composition (g/L) |
Wickerham medium | Malt extract 3, Peptone 5, Yeast extract 3, Glucose 10 pH- 7.2 |
SAB | Peptone 10, Dextrose 20, agar 15 |
YM agar | Malt extract 10, Yeast extract 2, Agar 20. |
CYA | Czapek 10, Yeast extract 5, Sucrose 30, K2HPO4, Agar 15 |
YES | Sucrose 150, Yeast extract 20, MgSO4.7H2O 0.5, CuSO4.5H2O 0.005, ZnSO4. 7H2O 0.01. |
MEA | Malt extract 30, Peptone 5, agar 15, Chloramphenicol 0.1 |
PDA | Potato 200, Dextrose 20, agar 15 |
Production and Optimization of Endophyte-Derived Bioactive Compounds 34:
Production of Bioactive Compounds from Fungal Endophytes: The symbiotic relationship among endophytic fungi and plants gives the powerful ability to produce new bioactive compounds. However, there are two main substrate-based methods for producing bioactive compounds: solid-state fermentation and submerged-state fermentation 34.
Solid state Fermentation (SSF): Solid State fermentation is widely used for the production of the bioactive compound from the fungal endophytes 34. These biomolecules are mostly metabolites generated by endophytic fungi grown on solid support selected for this purpose. In this fermentation process, different solid substrates such as Wheat bran, Rice bran, coconut oil cake, vegetable waste, gram husk, orange peel, sugarcane bagasse etc, were used with pure cultures of endophytic fungi 34.
SSF enables the optimal growth of endophytic fungi, permitting the mycelium to spread on the surface of solid compounds through which air can flow 34. SSF uses culture substratum with low water levels. The solid medium contains both the substrates and solid support. After fermentation, fermented media are mixed with effective solvent and further used for purification and analysis 34.
Submerged Fermentation: In submerged fermentation, enzymes and other reactive compounds are submerged in a liquid such as alcohol, oil, or nutrient broth. Endophytic fungi are sited in a small closed flask containing the rich nutrient broth with a high volume of oxygen. The in situ production of enzymes results in the production of bioactive molecules. Batch Fed fermentation method is commonly used, which utilizes the sterilized nutrients under optimized conditions along with fungal endophytes, increasing density. The addition of nutrients maintains the growth rate of fungal endophytes, also reduces risk of an overflow of metabolism 34.
Optimization of Production of Bioactive Compounds from Fungal Endophytes 35: Optimization of both fermentation processes depends on considerations of carbon homes and nitrogen homes, inoculums, phosphorus, organic acids, surfactants, incubation period, temperature, moisture level, and pH level under optimized conditions to achieve the greatest production of bioactive compounds from fungal endophytes.
- Effect of different medium
- Effect of carbon sources
- Effect of nitrogen sources
- Effect of inoculum amount
- Effect of inoculum time
- Effect of pH and temperature 35
TABLE 5: MEDIA USED FOR THE PRODUCTION OF BIOACTIVE COMPOUNDS BY FUNGAL ENDOPHYTES 36
Sr. no. | Medium | Conditions |
1 | Liquid Wickerhammedium | 26°C, 21days |
2 | S7medium | 26°C, 21days |
3 | Minimalmedium | 28°C,10-14days |
4 | Lactose & Starch Caseinbroth | 37°C, 120rpm, 18 days |
5 | M2medium | 28°C, 124rpm, 7days |
6 | C2broth, Sabourauds broth, PDB, MEB | 28°C, 10days |
7 | Nutrient Broth | 30°C,120rpm, 5days |
8 | Liquid fermentation | 37°C,120rpm, 18 days |
9 | Nutrient Broth | 30°C, 124rpm, 24 hrs |
10 | Cornmeal medium | 26°C, 21days |
Novel fungal Endophytes Verses Novel Bioactive Compounds 37-42: Discovering novel bioactive compounds from undiscovered endophytes is the current trend. Not all endophytes are culturable, and these may produce useful bioactive metabolites. Metabolomics of endophyte-infected and endophyte-free plant hosts could reveal intersections in secondary metabolite paths that may be pushed into synthesizing novel chemical species or lead compounds, another possibility of manipulating these chemo-diverse organisms 37.
In fungal endophytes, genes coding for enzymes of secondary metabolic pathways usually occurs as gene clusters being positioned in the same locus and co-expressed. These gene clusters are known to evolve swiftly through multiple rearrangements, duplication, and losses and are capable of interspecific feast through horizontal gene transfer. It is important to screen fungal species for their secondary metabolite assortment under different growing conditions; culture parameters such as composition of growth medium, aeration, pH and the presence of certain enzyme inhibitors change vividly the secondary metabolite profile and even induce the synthesis of several new metabolites 38 is because the synthetic capability of endophytes, like in other organisms, has been fine tuned by natural selection over millions of years. Smith et al. (2008) united sequence analysis with bioassay procedures to explore the endophyte diversity of the tropics. Their results suggest that tropical plants harbour a substantial portion of undiscovered endophytes that may be vested with novel biochemical diversity. Hence, including fungal endophytes in natural product discovery programs is necessary. Testing endophytes isolated from different tissues of plant hosts and plants growing in unusual and less studied habitats will be more productive 39-42.
CONCLUSION: Isolation of fungal endophytes from medicinal and other plants may result in methods to produce biologically active agents for biological exploitation on a large commercial scale, as they are easily cultured in a laboratory and fermenter instead of harvesting plants and affecting the eco-friendly biodiversity.
ACKNOWLEDGEMENT: NIL
CONFLICTS OF INTEREST: The authors declare no conflict of interest exists.
REFERENCES:
- Sumathi R, Saravanakumar A, Rajeswari R and Pavani S: Isolation, Purification, Partial Characterization and Antibacterial Activities of Compound Produced by some Actinomycetes from Sedimented Waters. Research J. Pharm and Tech 2009; 2(3): 521-526.
- Sumathi R, Saravanakumar A, Rajeswari R and Pavani S: Isolation, purification, partial characterization and antibacterial activities of compound produced by some actinomycetes from sedimented waters. Research J Pharm and Tech 2009; 2(4): 783-788.
- Nadeem Siddiqui, Waquar Ahsan, M. Shamsher Alam, Andalip, Bishmillah Azad and M. Jawaid Akhtar: Newer Biologically Active Pyridines: A Potential Review. Research J. Pharm. and Tech 2011; 4(12): 1918-1932.
- Kaura A, Lalit Sharma and Dhar VJ: Spectral and Antimicrobial Study of Some Novel Schiff Bases and Beta-Lactam Derivatives. Research J Pharm and Tech 2012; 5(1): 129-132.
- Chinedu Fredrick Anowi, Nnabuife Chinedu Cardinal, Onyegbule AF and Anowi LN: Antimicrobial Properties of the Ethylacetate Extract of the Leaves of Nauclea latifolia. Research J Pharm and Tech 2012; 5(5): 645-651.
- Manjunath Sangappa and Padma Thiagarajan: Isolation and Screening of Soil Penicilliumsp VIT-2012 Metabolites against Methicillin Resistant Staphylococcus aureus. Research J Pharm and Tech 2013; 6(12): 1340-1349.
- Girija K, Seethalakshmi P, Hemalatha K N and Arumugam N: Research J Pharm and Tech 2014; 7(4): 460-462
- Patel LS and Patel RS: Preliminary Phytochemical Analysis and Antimicrobial Activity of In-vitro Condition Asparagus racemosus leaf. Research J Pharm and Tech 2013; 6(12): 1387-1390.
- Mankar SD, Sahil B. Shaikh and Avesh A. Tamboli: Formulation of Herbal Tablet with the help of Tulsi and Turmeric Extract which Showing Antimicrobial Activity. Research J. Science and Tech 2020; 12(1): 69-73.
- Govindasamy Vinodhini, Madhava Anil Kumar, Saptharishi Balamanikandan and Muthulingam Seenuvasan: Assessment of Antimicrobial Property of a Secondary Metabolite Produced by an Enriched Bacterial Culture Isolated from Soil. Research J Pharm and Tech 2015; 8(1): 51-53.
- Priyanka Sahu, Sayanti Gupta, Monideepa Banerjee, Charles Lekhya Priya and Kokati Venkata Bhaskara Rao: Phytochemical Composition, Antimicrobial, Hemolytic activity and HPLC analysis of Ethanolic Extract of Cleome viscosa Stems. Research J Pharm and Tech 2014; 7(10): 1140-1144.
- Petrini O: Fungal endophytes in tree leaves. In: Microbial Ecology of Leaves. Andrews JH, Hirano SS, eds., Springer, New York 1991; 179-197.
- Cabral D, Stone J and Carroll GC: The internal mycoflora of Juncus spp., microscopic and cultural observation of infection patterns. Mycol Res 1993; 97: 367-376.
- Wilson AD: Endophyte-the evolution of the term, a clarification of its use and definition. Oikos 1995; 73: 274-276.
- Sampson K: Further observations on the systemic infection of Lolium. Transactions of the British Mycological Society 1938; 21: 84-97.
- Latch GCM, Christensen MJ and Gaynor DL: Aphid detection of endophyte infection in tall fescue. New Zealand J Agri Res 1985; 28: 129-132.
- Latch GCM, Hunt WF and Musgrave DR: Endophytic fungi affect growth of perennial ryegrass. New Zealand J Agri Res 1985; 28: 165-168.
- Saha DC, Johnson-Cicalese JM, Halisky PM, Heemstra MI and Funk CR: Occurrence and significance of endophytic fungi in the fine fescues. Plant Disease 1987; 71: 1021-1024.
- Clay K and Leuchtmann A: Infection of woodland grasses by fungal endophytes. Mycologia 1989; 81: 805-811.
- Carroll GC and Carroll FE: Studies on the incidence of coniferous needle endophytes in the Pacific Northwest. Canadian J Bot 1978; 56: 3034-3043.
- Carroll GC and Petrini O: Patterns of substrate utilization of fungal endophytes from coniferous foliage. Mycologia 1983; 75: 53-63.
- Rodrigues KF and Samuels GJ: Preliminary study of endophytic fungi in a tropical palm. Mycol Res 1990; 94: 827-830.
- Rodrigues KF and Samuels GJ: Idriella species endophytic in palms. Mycotaxon 1992; 43: 271-276.
- Rodrigues KF and Samuels GJ: Letendraeposis palmarum, a new genus and species of loculascomycetes. Mycologia. 1994; 86: 254-258.
- Rodrigues KF and Samuels GJ: Fungal endophytes of Spondiasmombin leaves in Brazil. J Basic Microbiol 1999; 39: 131-135.
- Redlin SC and Carris LM: Endophytic fungi in grasses and woody plants. The American Phytopathological Society Press, St Paul 1996; 223.
- Rodrigues KF and Dias MB: Fungal endophytes in the tropical grasses Brachiariabrizantha cv. Manrandú and Brachiariahumidicola. Pesquisa. Agropecuária. Brasileira. 1996; 31: 904-909.
- Taylor JE, Hyde KD and Jones EBG: Endophytic fungi associated with the temperate palm Trachycarpus fortunei within and outside its natural geographic Range. New Phytologist 1999; 142: 335-346.
- Frohlich J, Hyde KD and Petrini O: Endophytic fungi associated with palms. Mycol Res 2000; 104: 1202- 1212.
- Frohlich J and Hyde KD: Biodiversity of palm fungi in the tropics: are global fungal diversity estimates realistic? Biodiversity and Conservation 1999; 8: 977-1004.
- Petrini O and Fisher PJ: Ocurrence of fungal endophytes in twigs of Salix fragilis and Quercusrobur. Mycol Res 1990; 94: 1077-1080.
- Pereira JO, Carneiro-Vieira ML and Azevedo JL: Endophytic fungi from Musa acuminate and their reintroduction into axenic plants. World. J. Microbiol. Biotechnol 1999; 15: 37-40.
- Fisher PJ, Petrini O and Webster J: Aquatic hyphomycetes and other fungi in living aquatic and terrestrial roots of Alnus glutinosa. Mycol Res 1991; 95: 543-547.
- Fisher PJ, Petrini O and Lappin-Scott HM: The distribution of some fungal and bacterial endophytes in maize (Zea mays). New Phytologist 1992; 122: 299-05.
- Fisher PJ, Petrini LE and Sutton BC: A study of fungal endophytes from leaves, stem and roots of Gynoxisoleifolia, Muchler (Compositae) from Ecuador. Nova. Hedwigia 1995; 60: 589-594.
- Fisher PJ and Petrini O: A comparative study of fungal endophytes of xylem and bark of Alnus species in England and Switzerland. Mycol Res 1990; 94: 313.
- Schulz B, Guske S, Dammann U and Boyle C: Endophyte-host interactions II. Defining symbiosis of the endophyte-host interaction. Symbiosis 1998; 25: 213-227.
- Arnold AE, Maynard Z, Gilbert GS, Coley PD and Kursar TA: Are tropical fungal endophyteshyperdiverse. Ecol Lett 2000; 3: 267-274.
- Arnold AE, Maynard Z and Gilbert GS: Fungal endophytes in dicotyledonous neotropical trees, patterns of abundance and diversity. Mycol Res 2001; 105: 1502-1507.
- Arnold AE: Understanding the diversity of foliar endophytic fungi, progress, challenges and frontiers. Fungal Biol Rev 2007; 21: 51- 66.
- Bettucci L, Simeto S, Alonso R and Lupo S: Endophytic fungi of twigs and leaves of three native species of Myrtaceae in Uruguay. Sydowia 2004; 56: 8-23.
- Gallery RE, Dalling JW and Arnold AE: Diversity, host affinity, and distribution of seed infecting fungi, A case study with Cecropia Ecol 2007; 88: 582-588.
How to cite this article:
Azharuddin M, Saad M and Kharat AR: A review on mutualistic relationship of endophytic fungi for the production of bioactive metabolites. Int J Pharm Sci & Res 2023; 14(6): 2651-57. doi: 10.13040/IJPSR.0975-8232.14(6).2651-57.
All © 2023 are reserved by International Journal of Pharmaceutical Sciences and Research. This Journal licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 3.0 Unported License.
Article Information
4
2651-2657
717 KB
331
English
IJPSR
Mohd Azharuddin *, Mohammad Saad and Amol R. Kharat
Department of Pharmacognosy, Government College of Pharmacy, Aurangabad, Maharashtra, India.
quaziazharpharma@gmail.com
09 September 2022
20 October 2022
18 November 2022
10.13040/IJPSR.0975-8232.14(6).2651-57
01 June 2023