International Journal of Plant Biology 2018; volume 9:7810

Secrets of plants: endophytic grows asymptomatically in aerial plant tissues and is vertically trans- Correspondence: Asiya Nazir, Department of mitted from the plant to its offspring via Applied Science and Mathematics, College of Asiya Nazir, Habeeb Abdul Rahman seeds and tillers. Endophytes are thought to Arts and Sciences, Abu Dhabi University, Abu Department of Applied Science and interact mutualistically with their host Dhabi, United Arab Emirates. Mathematics, College of Arts and plants mainly by increasing host resistance Tel.: +97125015447. Sciences, Abu Dhabi University, Abu to herbivores1 and have been termed E-mail: [email protected] Dhabi, United Arab Emirates acquired plant defenses.5 In return, plants Key words: Endophytic fungi; bioactive com- provide spatial structure and protection pounds; secondary metabolite. from desiccation, nutrients, and photosyn- thate and, in the case of vertical-transmis- Contributions: the authors contributed equally. Abstract sion, dissemination to the next generation of Endophytic fungi are an important com- hosts. Endophytic fungi represent an impor- Conflict of interest: the authors declare no ponent that colonizes in healthy tissues of tant and quantifiable component of fungal potential conflict of interest. living plants and can be readily isolated biodiversity in plants that impinge on plant from any microbial or plant growth medi- community diversity and structure. Received for publication: 5 August 2018. um. They act as reservoirs of novel bioac- They produce a wide range of com- Revision received: 5 September 2018. tive secondary metabolites, such as alka- pounds useful for plants for their growth, Accepted for publication: 6 September 2018. loids, phenolic acids, quinones, steroids, protection to environmental conditions, and This work is licensed under a Creative sustainability, in favor of a good dwelling saponins, tannins, and terpenoids that serve Commons Attribution-NonCommercial 4.0 as a potential candidate for antimicrobial, place within the hosts. Due to its ability of International License (CC BY-NC 4.0). anti-insect, anticancer and many more prop- producing bioactive secondary metabolites erties. Their huge diversity and particular similar or same compounds as their host ©Copyright A. Nazir and H.A. Rahman, 2018 habituation, they can provide a good area plant, promoting growth, good yield, induc- Licensee PAGEPress srl, Italy for research in the field of making new ing host plants to tolerate both biotic and International Journal of Plant Biology 2018; 9:7810 medicines and novel drug-like molecules. abiotic stresses and disease resistance, onlydoi:10.4081/pb.2018.7810 Because of the impact of endophytes on endophytes is currently attracting a lot of host plant by enhancing their growth or research interest and therefore, can be used transmission, in plant biodiversity and fit- increasing their fitness, also making them as a potential source of novel natural prod- ness benefits conferred to hosts while the C ucts for food, industrial, medicinal anduse agri- tolerant to abiotic and biotic stresses and group has just one class. Class 2 endophytes cultural industries. holding the secondary metabolites, endo- have been the most extensively researched phytes are gaining attention as a subject for and has been shown to enhance fitness ben- research. This review aims to comprehend efits of their plant host as a result of habitat- the contribution and uses of endophytes and Classification of endophytes specific stresses such as pH, temperature, relationships between endophytic fungi and There are mainly two classes in which and salinity. Class 3 endophytes are restrict- their host medicinal plants. endophytic fungi are classified as Class I ed to growth in belowground plant tissues Clavicipitaceae and Class II and form in localized areas of plant tissue. Nonclavicipitaceous. The Class 1 endo- Class 4 endophytes are also restricted to Introduction phytes are the clavicipitaceous endophytes plant tissues below ground but can colonize Endophytes are microorganisms that associated with warm- and cool-season much more of the plant tissue.10 NC-endo- reside within study plant tissues intercellu- grasses. They are host specific, mainly in phytes have been recovered from every larly and/or intracellularly but usually the grass family poaceae and rarely in major lineage of land plants, and from all remain asymptomatic and does not show cyperaceae, and are often vertically trans- terrestrial ecosystems, including both agro- any noticeable damage to the host. mitted through seeds. Transmission of Class ecosystems and biomes ranging from the Endophytic fungi inhabit plant tissues with- 1 endophytes is primarily vertical, with tropics to the tundra.11 out destroying or producing substancesNon-commercial that maternal plants passing fungi on to off- The scale of their diversity, their eco- 6 cause an infection in the host cell. They spring via seed infections. Class 1 endo- logical roles, the insights they provide into exhibit complex interactions with their phytes frequently increase plant biomass, the evolution of various ecological modes hosts, which involves mutualism and antag- confer drought tolerance, and produce in fungi, their potential applications, and the onism.1,2 Plants strictly limit the growth of chemicals that are toxic to animals and 5 ability of many fungi to switch between endophytes, and these endophytes use many decrease herbivory. However, the benefits endophytic and freeliving lifestyles12,13 mechanisms to gradually adapt to their liv- conferred by these fungi appear to depend are becoming more apparent, engendering ing environments.3 Unlike mycorrhizal on the host species, host genotype and envi- 7,8 growing enthusiasm from mycologists, fungi that colonize plant roots and grow ronmental conditions. ecologists, physiologists and applied scien- into the rhizosphere, endophytes reside Compared with Class 1 endophytes, tists. entirely within plant tissues and may grow Class 2 endophytes are highly diverse and within roots, stems and/or leaves, emerging comprised of species from to sporulate at plant or hosttissue senes- () to agaricomycotina and puc- cence.1,4 Symbioses have been responsible ciniomycotina (basidiomycota).9 They col- for the origin of major ecological and evo- onize roots, stems, leaves, or the whole Isolation and identification lutionary transitions in the history of life. plant. They can be vertically or horizontally Endophytic fungi are any fungi that Plants are hosts to complex communities of transmitted. However, NC-endophytes rep- grow all or part of their life cycles symp- endophytes that colonize the interior of both resent three distinct functional classes class tomlessly in the intercellular spaces of liv- below- and above-ground tissues. The 2, 3 and 4, based on host colonization and ing and apparently healthy host plant tis-

[International Journal of Plant Biology 2018; 9:7810] [page 43] Review sues, while the inhabited host tissues remain insects.19 Reports of molecular studies on wide variety of structurally unique bioac- intact and functional. The diversity and endophytic bacterial diversity have revealed tive natural products, such as alkaloids, numbers of fungal endophytes vary consid- a large richness of species. Endophytes pro- benzopyranones, chinones, flavonoids, phe- erably and their detection depends on biotic, mote plant growth and yield, suppress nolic acids, quinones, steroids, terpenoids, abiotic and experimental factors. Detection pathogens, may help to remove contami- tetralones, xanthones, and others.23 and recovery of endophytic fungi have nants, solubilize phosphate, or contribute relied heavily on dissection of plant organs assimilable nitrogen to plants.20 The endo- into small fragments followed by their sur- phyte-host relationship is believed to be face sterilization and subsequent plating of complex and probably varies from host to Antioxidants and phenolic con- fragments onto a nutrient-rich agar medi- host and microorganism to the microorgan- tent of endophytes um.4,14 ism.21 Many experiments have been con- Traditionally, endophytic fungi inside ducted to compare how -infected Antioxidants are thought to be highly plant tissues can be recognized by two basic plants and non-infected plants behave in effective in the management of ROS-medi- techniques, i.e. direct observation and culti- relation to environmental stress, and attack ated tissue impairments. Many antioxidant vation-dependent methods. In the direct by insect and animal predators.22 Therefore, compounds possess anti-inflammatory, observation method, endophytic fungal search for interesting biological activities anti-atherosclerotic, antitumor, antimuta- structures within living plant tissues are within the natural biodiversity has been the genic, anticarcinogenic, antibacterial, and antiviral activities to a greater or lesser directly examined under a light and electron basis for the development of various appli- extent. Afra et al., in 2015, revealed that microscope, which can show all endophytic cations in biotechnology, agriculture, pro- endophytic fungus Aspergillus sp. from mycobiota within the plant tissue.15 In con- duction of pharmaceuticals compounds and Trigonella foenum-graecum seeds demon- trast, cultivation-dependent techniques have other fields. strated the highest both total phenolic con- been routinely employed in endophyte tent in term of gallic acid equivalent and diversity studies.1 It is important to isolate antioxidant activity for free radical scav- endophytic fungi for further detailed studies Application of endophytes enging assay.24 The antioxidant activity and into their characterization, population Medicinal plants and their endophytes totalonly phenolic content (TPC) of ethyl dynamics, species diversity, or as inoculate are important resources for the discovery of acetate extracts of endophytic fungi isolated to improve plant growth and health, or natural products. Since endophytes residing from Eugenia jambolana were studied by screening for novel biologically active sec- inside healthy plant tissues without any dis- Manila et al., in 2014.25 The study showed ondary metabolites (Figure 1). cernible infectious symptom and exhibit that 36% endophytic extracts of Endophytes can also be isolated by cul- use mutualism and antagonism with the host, Chaetomium sp., Aspergillus sp., turing from ground tissue extract16 or by they could be a potential source of novel Aspergillus peyronelii and Aspergillus direct culturing of plant tissues17 on media natural products for medicinal, agricultural, Niger was having high phenolic content suitable for bacteria or fungi or actino- and industrial uses. Endophytes provide a exhibited potent antioxidant activity. The mycetes. Conventionally, identification of endophytes is based on morphological char- acteristics for bacteria, fungi, and actino- mycetes and with the help of biochemical tests for bacteria and actinomycetes. With the development of molecular biology, ribo- somal DNA Internal Transcribed Spacer (ITS) sequence analysis is widely used for the identification of microorganisms. Ribosomal DNA (rDNA) ITS was proved to be a valuable source of evidence to resolve phylogenetic relationships at lower levels, such as among genera or species.18 Non-commercial Microorganisms are important media- tors of plant-herbivore interactions. The role of endophytic microorganisms in plant associations has been extensively dis- cussed. Endophytes are considered plant mutualists. They receive nutrition and pro- tection from the host plant while the host plant may benefit from enhanced competi- tive abilities and increased resistance to her- bivores, pathogens, and various abiotic stresses.7 As endophytes colonize ecologi- cal niches similar to those colonized by phytopathogens, interactions between these two groups are possible, and in fact, many studies have shown that endophytic microorganisms isolated from surface disin- fected plant tissues exhibit potential as bio- Figure 1. The interaction between endophytes and plant host. control agents against phytopathogens and

[page 44] [International Journal of Plant Biology 2018; 9:7810] Review free radical scavenging ability of phenols is Saccharomyces cerevisiae, Geotrichum sp. in U-87 cell line.46 The production of attributed to the occurrence of hydroxyl and Penicillium canadensis.36 podophyllotoxin from endophytic groups. Phenols and alkaloids were the Antimicrobial activity was exhibited by Alternaria tenuissima isolated from major phytochemical constituents of endo- some endophytic fungal isolates from Sinopodophyllum emodi (Wall) was also phytes and were reported by Huang et al. Cinnamomum. burmani, C. camphora, and reported by Liang et al.47 Cephalosporium sp., an endophytic fungus C. insularimontanum and C. zeylanicum.37 isolated from the root of Trachelospermum Beauvericin, isolated from Fusarium oxys- jasminoides (Apocynaceae) produce a phe- porum, which is associated with cinnamo- nolic compound (graphislactone A) with mum kanihirai, was reported toxic against Conclusions strong free radical scavenging and antioxi- methicillin-resistant S. aureus and B. sub- Endophytic fungi comprise a diverse dant activity.26 Cui et al., in 2015 isolated tilis.38 The endophyte of Magnolia x group of species existing in various ecosys- 315 endophytes from Rhodiola crenulata, soulangeana, Fusarium dimerum, was the tems and are capable of synthesizing bioac- R. angusta, and R. sachalinensis and report- source of enniatins which exhibited effec- tive compounds, which have proven to be ed that antioxidant assay by showing that tiveness against Bacillus subtilis, Candida useful for novel drug discovery. This group, the DPPH radical-scavenging rates of 114 albicans, Trychosporom cutaneum and which causes no apparent effects on plant isolates (63.33%) were >50%, and those of Cryptococcus neoformans.39 performance but lives on the metabolites five isolates (Rct45, Rct63, Rct64, Rac76, 27 produced by the host, is presumably the and Rsc57) were >90%. The culture fil- most dominant functional group among trate of Pestalotiopsis microspora, which Anticancer activities of endo- endophytes by quantity. Since many was isolated from combretaceaous plant phytes microorganisms have developed resistance Terminalia morobensis, showed promising against the current drugs so it is necessary antioxidant activity.28 There is some evidence that bioactive compounds produced by endophytes could to search for new drugs. Much more work is be substitute approaches for innovation of essential to understand endophytes physiol- ogy, biochemical pathways, defensive role, Antimicrobial activities of endo- new drugs, as various natural products of plants, microorganisms, and marine sources secondaryonly metabolite production, motiva- phytes were identified as anticancer agents. tion and encouragement of researcher from Many endophytic fungi have the ability Firakova et al., in 2007 reported diterpenoid life sciences to contribute research related to produce antimicrobial substances. An that taxol also known as paclitaxel as a to endophytes. It is vital importance to increasing number of compounds with anti- novel drug since it’s due to the use mode of review and highlight the previous success- bacterial activity are being isolated from action compared to other anticancer es, on-going research and latest develop- endophytic fungi, including fumitremorgins agents.40 Taxol is beneficial for the cure of ments in research associated with endophyt- B isolated from Phomopsis sp., and peri- advanced breast cancer, lungs cancer, and ic microorganisms to draw the attention of conicins A and B from Periconia sp.29 refractory ovarian cancer. Taxol was from the research community toward this emerg- Research has shown that the compound the bark of tree belonging to taxus family ing field and possible exploitation of the ophiopogon japonicus pill has displayed (Taxus brevifolia), its main general available sources for their therapeutic uses effective inhibition of Staphylococcus resource. Another significant anticancer in various fields, such as the medical, phar- aureus and an extract from O. japonicus compound is the alkaloid Camptothecin maceutical, food and cosmetics. 30 showed strong inhibition of malic mildew. (C20H16N2O4), a powerful antineoplastic 8.3% of the strains isolated from Dracaena agent which was firstly isolated from the cambodiana and Aquilaria sinensis showed wood of Camptotheca acuminate Decaisne antimicrobial activity,31 whereas 27.6% of (Nyssaceae) in China.41 Ergoflavin References strains isolated from Camptotheca acumi- (C30H26O14), a dimeric xanthene linked in 1. Carroll GC. Fungal endophytes in stems nata displayed antimicrobial activity position 2, belongs to the compound class and leaves: from latent pathogen to mutu- against some pathogens.32 Antimicrobial called ergochromes and was described as a alistic symbiont. Ecol 1988;69:2-9. activity of endophytic fungiNon-commercial from new anticancer agent isolated from an endo- 2. Parker MA. Mutualism in metapopula- Lippiasidoides Cham. showed antimicro- phytic fungus rising on the Mimuscop elen- tions of legumes and Rhizobia. Am bial activity in an assay on a solid medi- gi (Sapotaceae) plant leaves42 Wu et al., in Natural 1999;153:S48-60. um.33 The steroid ergosta-7,9(14),22-triene- 2015 also reported leaf endophytes from 3. Dudeja SS, Giri R, Saini R, et al. 3β-ol, produced by the endophytic fungus Morinda citrifolia inhibited the growth of Interaction of endophytic microbes with sphaerica isolated from leaves human carcinoma cell lines of lungs, legumes. J Basic Microb 2012;52:248-60. of Vinca rosea, showed antifungal activity prostate, and breast.43 Bioactive compound 4. Stone JK, Polishook JD, White JF. against Cryptococcus neoformans with an sclerotiorin has been isolated from an endo- Endophytic fungi. In: G.M. Mueller, G.F. IC50 value of 14.81 μg/mL.34 Maryam et al. phytic fungus Cephalotheca faveolata.44 Bills and M.S. Foster (Eds.), Biodiversity reported Sixteen out of 23 bacterial isolates Sclerotiorin was found to be potent anti- of fungi: inventory and monitoring meth- (69%) exhibited antimicrobial activity proliferative against different cancer cells. ods. New York: Elsevier Academic Press; against the selected pathogenic bacteria, An endophytic fungus Colletotrichum 2004. pp. 241-270. such as Bacillus cereus, Staphylococcus gloeosporioides (strain JGC-9) was isolated 5. Cheplick GP, Clay K. Acquired chemical aureus, Bacillus subtilis, Klebsiella pneu- from Justicia gendarussa, a medicinal plant defenses of grasses: the role of fungal moniae, Citrobacter freundii, Proteus and screened for taxol production.45 endophytes. Oikos 1988;52:309-18. mirabilis, Shigella flexneri and Escherichia Podophyllum hexandrum, which produced 6. Saikkonen K, Ion D, Gyllenberg M. The coli.35 Rodrigues et al., in 2000 have report- podophyllotoxin, podophyllotoxin glyco- persistence of vertically transmitted fungi ed that Guignardia sp. from Spondias mom- side and demethoxypodophyllotoxin. The in grass metapopulations. Proc R Soc B bin inhibited E. coli, S. aureus, isolated metabolites exhibited cytotoxicity Biol Sci 2002;269:397-1403.

[International Journal of Plant Biology 2018; 9:7810] [page 45] Review

7. Saikkonen K, Faeth SH, Helander M, chemical synthesizers inside plants. Sci 2017;9:11-8. Sullivan TJ. Fungal endophytes: a contin- Progr 2004;87. 36. Rodrigues KF, Hesse M, Werner C. uum of interactions with host plants. Annu 23. Tan RX, Zou WX. Endophytes: a rich Antimicrobial activities of secondary Rev Ecol Evol Syst 1998;29:319-43. source of functional metabolites. Nat Prod metabolites produced by endophytic fungi 8. Faeth SH, Sullivan TJ. Mutualistic, asexu- Rep 2001;18:448-59. from Spondias mombin. J Basic Microbiol al endophytes in a native grass are usually 24. Afra K, Ietidal M, Justinne T, et al. A pilot 2000;40:261-7. parasitic. Am Nat 2003;161: 310-25. study of the antioxidant potential of endo- 37. Praptiwi, Ilyas M, Fathoni A, et al. 9. Rodriguez RJ, White JF, Arnold AE, phytic fungi from some Sudanese medici- Antibacterial screening of the culture of Redman RS. Fungal endophytes: diversity nal plants. Asian Pac J Trop Dis and functional roles. New Phytol 2015;8:701-4. endophytic fungal extracts isolated from 2009;182:314-30. 25. Yadav M, Yadav A, Yadav JP. In vitro cinnamon stick. Teknol Indones 10. Wani ZA, Ashraf N, Mohiuddin T, Riyaz- antioxidant activity and total phenolic con- 2015;38:33-41. Ul-Hassan S. Plant-endophyte symbiosis, tent of endophytic fungi isolated from 38. Wang QX, Li SF, Zhao F, et al. Chemical an ecological perspective. Appl Microbiol Eugenia jambolana Lam. Asian Pac J Trop constituents from endophytic fungus Biotechnol 2015;99: 2955-65. Med 2014;7S1:S256-61. Fusarium oxysporum. Fitoterapia 11. Arnold AE, Lutzoni F. Diversity and host 26. Song YC, Huang WY, Sun C, et al. 2011;82:777-81. range of foliar fungal endophytes: are Characterization of graphislactone A as the 39. Firakova S, Sturdikoca M, Liptaj T, tropical leaves biodiversity hotspots? antioxidant and free radical scavenging Bezakova L, Proksa B. Enniatins pro- Ecology 2007;88:541-9. substance from the culture of duced by Fusarium dimerum, an endo- 12. Vasiliauskas R, Menkis A, Finlay RD, Cephalosporium sp. IFB-E001, an endo- phytic fungal strain. Pharmazie 2008; Stenlid J. Wooddecay fungi in fine living phytic fungus in Trachelospermum jasmi- roots of conifer seedlings. N Phytol noides. Biol Pharm Bull 2005;28: 506-9. 63:539-41. 2007;174:441-6. 27. Cui JL, Guo TT, Ren ZX, et al. Diversity 40. Firakova S, Sturdikoca M, M´uˇckov´a. 13. Selosse MA, Vohník M, Chauvet E. Out of and Antioxidant Activity of Culturable Bioactive secondary metabolites produced the rivers: are some aquatic Endophytic Fungi from Alpine Plants of byonly microorganisms associated with plants. plant endophytes? N Phytol 2008;178:3-7. Rhodiola crenulata, R. angusta, and R. Biologia 2007;62:251-7. 14. Gamboa MA, Laureano S, Bayman P. sachalinensis. PLoS One 2015;10:3. 41. Cremasco MA, Hritzko BJ, Linda WNH. Measuring diversity of endophytic fungi 28. Harper JKEJ, Ford GA, Strobel A, et al. Experimental purification of paclitaxel in leaf fragments: Does size matter? Pestacin: A 1,3-dihydro isobenzofuranuse from a complex mixture of taxanes using a Mycopathologia 2003;156:41-5. from Pestalotiopsis microspora possessing simulated moving bed. Braz J Chem Eng 15. Lucero ME, Unc A, Cooke P, et al. antioxidant and antimycotic activities. 2009;26:207-18. Endophyte microbiome diversity in Tetrahedron 2003;59: 2471-6. 42. Deshmukh S, Mishra PD, Kulkarni- micropropagated Atriplex canescens and 29. Ni ZW, Li GH, Zhao PJ, Shen YM. Almeida S, et al. Anti-inflammatory and Atriplex torreyi var. griffithsii. PLoS One Antimicrobial components of the endo- 2011 [Epub ahead of print]. phytic fungal strain chaetomium globo- anticancer activity of Ergoflavin isolated 16. Rai R, Dash PK, Prasanna BM, et al. sum Ly50′ from maytenus hookeri. Nat from an endophytic fungus. Chem Endophytic bacterial flora in the stem tis- Prod Rev 2008;20:33-6 [in Chinese]. Biodivers 2009;6:784-9. sue of a tropical maize (Zea mays L.) 30. Rao Y, Chen C, Zhao B. Study on the 43. Wu Y, Girmay S, da Silva VM, et al. The genotype: isolation, identification and eliminating phlegm effect and bacteriosta- Role of Endophytic Fungi in the enumeration. World J Microbiol tic action of compound Maidong pills. Anticancer Activity of Morinda citrifolia Biotechnol 2007;23:853-8. Chin Hosp Pharm J 2008;28:615-7. Linn. (Noni). Evid Based Complement 17. Hata K, Sone K. Isolation of endophytes 31. Gong LJ, Guo SH. Endophytic fungi from Alternat Med 2015;2015: 393960. from leaves of Neolitsea sericea in Dracaena cambodiana and Aquilaria 44. Periyasamy G, Shilpa AV, Amit K, et al. broadleaf and conifer stands. Mycoscience sinensis and their antimicrobial activity. Anticancer activity of sclerotiorin, isolated 2008;49:229-32. Afr J Biotechnol 2009;8: 731-6. from an endophytic fungus Cephalotheca 18. Youngbae S, Kim S, Park CW. A phyloge-Non-commercial32. Lin X, Lu C, Huang Y, et al. Endophytic netic study of polygonum sect. tovara fungi from a pharmaceutical plant, faveolata. Indian J Exper Biol 2012;50: (polygonaceae) based on ITS sequences of Camptotheca acuminata: isolation, identi- 464-8. nuclear ribosomal DNA. Plant Biol fication and bioactivity. World J Microbiol 45. Gangadevi V, Muthumary J. Isolation of 1997;40:47-52. 2007;23:1037-40. Colletotrichum gloeosporioides, a novel 19. Azevedo JL, Araujo WL. Genetically 33. Siqueira VM, Conti R, Araújo JM, Souza- endophytic taxol producing fungus from modified crops: environmental and human Motta CM. Endophytic fungi from the the leaves of a medicinal plant, Justicia health concerns. Mutat Res 2003;544:223- medicinal plant Lippia sidoides Cham. gendarussa. Mycol Balcan 2008;5:1-4. 33. and their antimicrobial activity. Symbiosis 46. Puri S, Nazir Asiya N, Chawla R, et al. 20. Rosenblueth M, Martínez-Romero E. 2011;53:89-95. The endophytic fungus Trametes hirsuta Bacterial endophytes and their interactions 34. Metwaly AM, Kadry HA, El-Hela AA, et as a novel alternative source of podophyl- with hosts. Am Phytopathol Soc al. Nigrosphaerin A a new isochromene lotoxin and related aryl tetralin lignans. J 2006;827-37. derivative from the endophytic fungus Biotechnol 2006;122:494-510. 21. Bing LA, Lewis LC. Suppression of Nigrospora sphaerica. Phytochem Lett Ostrinia nubilalis (Hu¨bner) (Lepidoptera: 2014;7:1-5. 47. Liang Z, Zhang JX, Zhang X, et al. Pyralidae) by endophytic Beauveria 35. Maryam B, Mansour A, Abdolrazag H, et Endophytic Fungus from bassiana (Balsamo) Vuillemin. Environ al. Antimicrobial activity of endophytic Sinopodophyllum emodi (Wall.) Ying that Entomol 1991;20:1207-11. bacterial populations isolated from med- Produces Podophyllotoxin. J Chromatogr 22. Noel O, Nicholas H. Endophytes - the ical plants of Iran. Iran J Microbiol Sci 2016;54:175-8.

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