Mycobiology

The Korean Society of Mycology (한국균학회)
권호 표지
DOI QR코드

DOI QR Code

Diversity and Bioactive Potential of Culturable Fungal Endophytes of Medicinal Shrub Berberis aristata DC.: A First Report

  • Sharma, Supriya (School of Biotechnology, University of Jammu) ;
  • Gupta, Suruchi (School of Biotechnology, University of Jammu) ;
  • Dhar, Manoj K. (School of Biotechnology, University of Jammu) ;
  • Kaul, Sanjana (School of Biotechnology, University of Jammu)
  • Received : 2017.08.10
  • Accepted : 2018.02.19
  • Published : 2018.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Bioactive natural compounds, isolated from fungal endophytes, play a promising role in the search for novel drugs. They are an inspiring source for researchers due to their enormous structural diversity and complexity. During the present study fungal endophytes were isolated from a well-known medicinal shrub, Berberis aristata DC. and were explored for their antagonistic and antioxidant potential. B. aristata, an important medicinal shrub with remarkable pharmacological properties, is native to Northern Himalayan region. A total of 131 endophytic fungal isolates belonging to eighteen species and nine genera were obtained from three hundred and thirty surface sterilized segments of different tissues of B. aristata. The isolated fungi were classified on the basis of morphological and molecular analysis. Diversity and species richness was found to be higher in leaf tissues as compared to root and stem. Antibacterial activity demonstrated that the crude ethyl acetate extract of 80% isolates exhibited significant results against one or more bacterial pathogens. Ethyl acetate extract of Alternaria macrospora was found to have potential antibacterial activity. Significant antioxidant activity was also found in crude ethyl acetate extracts of Alternaria alternata and Aspergillus flavus. Similarly, antagonistic activity of the fungal endophytes revealed that all antagonists possessed inhibition potential against more than one fungal pathogen. This study is an important step towards tapping endophytic fungal diversity for bioactive metabolites which could be a step forward towards development of novel therapeutic agents.

Keywords

References

  1. Freeman EM. The seed fungus of Lolium temulentum L., the darnel. Philos Trans R Soc Lond B. 1904;196:1-28. https://doi.org/10.1098/rstb.1904.0001
  2. Sharma T, Kaul S, Dhar MK. Diversity of culturable bacterial endophytes of saffron in Kashmir, India. Springer Plus. 2015;4:661-674. https://doi.org/10.1186/s40064-015-1435-3
  3. Shahid M, Rahim T, Shahzad A, et al. Ethnobotanical studies on Berberis aristata DC. root extracts. Afr J Biotech. 2009;8:556-563.
  4. Lamichhane B, Adhikari S, Shrestha P, et al. Study of phytochemical, antioxidant, antimicrobial and anticancer activity of Berberis aristata. JTLS. 2014;4:01-07. https://doi.org/10.11594/jtls.04.01.01
  5. Kumari K, Setty OH. The protective effect of Berberis aristata against mitochondrial dysfunction induced due to co-administration of mitomycin C and cisplatin. J Cancer Sci Ther. 2002;4:199-206.
  6. Tamilselvi S, Balasubramani SP, Venkatasubramanian P, et al. A review on the pharmacognosy and pharmacology of the herbals traded as Daruharidra. Int J Pharm Bio Sci. 2014;5:556-570.
  7. Pasrija A, Singh R, Katiyar CK. Comparative study on the antimicrobial activity of Berberis aristata from different regions and berberine in vitro. Int J Life Sci Res. 2011;1:17-20.
  8. Unkeshwar P, Nasiruddin M, Fayazuddin M, et al. Evaluation of hepatoprotective activity of Berberis aristata against carbon tetrachloride induced hepatotoxicity in rats. Int J Pharm Pharm Sci. 2013;5:254-265.
  9. Ramteke AD, Aiyer RB, Gandhi SP, et al. Phytochemical study of Daruharidra and hepatoprotective efficacy in infective hepatitis. J Pharm Sci Innov. 2013;1:44-47.
  10. Singh J, Kakkar P. Anti hyperglycemic and antioxidant effect of Berberis aristata root extract and its role in regulating carbohydrate metabolism in diabetic rats. J Ethnopharmacol. 2009;123:22-26. https://doi.org/10.1016/j.jep.2009.02.038
  11. Dehar N, Walia R, Ratol S. Potentiation of thiopentone sodium induced hypnosis by Berberis aristata in rodents. Asian J Pharm Clin Res. 2013;5:131-133.
  12. Santos RMG, Rodrigues-Fo E, Rocha WC, et al. Endophytic fungi from Melia azedarach. World J Microbiol Biotechnol. 2013;19:767-770.
  13. Schulz B, Guske S, Dammann U, et al. Endophyte host interactions II. Defining symbiosis of the endophyte-host interaction. Symbiosis. 1998;25:213-227.
  14. Saghai-Maroof MA, Soliman KM, Jorgensen RA, et al. Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA. 1984;81:8014-8019. https://doi.org/10.1073/pnas.81.24.8014
  15. Li H, Qing C, Zhang Y, et al. Screening for endophytic fungi with antitumor and antifungal activities from Chinese medicinal plants. World J Microbiol Biotechnol. 2005;21:1515-1519. https://doi.org/10.1007/s11274-005-7381-4
  16. Schwalbe R, Steele-Moore L, Goodwin AC. Antimicrobial susceptibility testing protocol. Boca Raton, USA: CRC press; 2004.
  17. Orole OO, Adejumo TO. Activity of fungal endophytes against four maize wilt pathogens. Afr J Microbiol Res. 2009;3:969-973.
  18. Whipps JM. Developments in the biological control of soil borne plant pathogens. Adv Bot Res. 1997;26:1-134.
  19. Sanchez-Moreno C, Larrauri JA, Saura-Calixto F. A procedure to measure the antiradical efficiency of polyphenols. J Agric Food Chem. 1998;47:425-431.
  20. Strobel GA. Endophytes as sources of bioactive products. Microbes Infect. 2003;5:535-544. https://doi.org/10.1016/S1286-4579(03)00073-X
  21. Pandey A, Palni LMS. The rhizosphere effect in trees of the Indian Central Himalaya with special reference to altitude. App Ecol Env Res. 2007;5:93-102.
  22. Kaul S, Ahmed M, Zargar K, et al. Prospecting endophytic fungal assemblage of Digitalis lanata Ehrh. (foxglove) as a novel source of digoxin: a cardiac glycoside. 3 Biotech. 2013;3:335-340.
  23. Xu L, Wang J, Zhao J, et al. Beauvericin from the endophytic fungus, Fusarium redolens, isolated from Dioscorea zingiberensis and its antibacterial activity. Nat Prod Commun. 2010;5:811-814.
  24. Gond SK, Mishra A, Sharma VK, et al. Diversity and antimicrobial activity of endophytic fungi isolated from Nyctanthes arbor- tristis, a well-known medicinal plant of India. Mycoscience. 2012;53:113-121. https://doi.org/10.1007/S10267-011-0146-Z
  25. Qin JC, Zhang YM, Hu L, et al. Cytotoxic metabolites produced by Alternaria spp., an endophytic fungus isolated from Ginkgo biloba. Nat Prod Commun. 2009;4:1473-1476.
  26. Pillai TG, Jayaraj R. Colletotrichum gloeosporioides: a true endophyte of the endangered tree, Cynometra travancorica in the Western Ghats. J Plant Pathol Microb. 2015;6:5.
  27. Gupta S, Kaul S, Singh B, et al. Production of gentisyl alcohol from Phoma herbarum endophytic in Curcuma longa L. and its antagonistic activity towards leaf spot pathogen Colletotrichum gloeosporioides. Appl Biochem Biotechnol. 2016;180:1-17. https://doi.org/10.1007/s12010-016-2088-6
  28. De Siqueira VM, Conti R, De Araujo JM, et al. Endophytic fungi from the medicinal plant Lippia sidoides Cham. and their antimicrobial activity. Symbiosis. 2011;3:89-95.
  29. Kaur M, Aggarwal NK. First record of A. macrospora MKP1 causing leaf spot disease on Parthenium hysterophorus from India. J Crop Prot. 2015;4:719-726.
  30. Bacon CW, White JFJ. Physiological adaptations in the evolution of endophytism in the Clavicipitaceae. Microb Endophytes. 2000;7:237-263.
  31. Kharwar RN, Verma VC, Kumar A, et al. Endophytic fungi: better players of biodiversity, stress tolerance, host protection and antimicrobial production. In: Chauhan AK, Verma A (eds) A textbook of molecular biotechnology. New Delhi: IK international Publishing house; 2009; p.1033-1357.
  32. Verma VC, Kharwar RN, Gange A. Biosynthesis of antimicrobial silver nanoparticles by the endophytic fungus Aspergillus clavatus. Nanomedicine. 2010;5:33-40. https://doi.org/10.2217/nnm.09.77
  33. Bezerra JD, Nascimento CC, Barbosa R, et al. Endophytic fungi from medicinal plant Bauhinia forficata: diversity and biotechnological potential. Braz J Microbiol. 2015;46:49-57. https://doi.org/10.1590/S1517-838246120130657
  34. Patil MP, Patil RH, Maheshwari VL. Biological activities and identification of bioactive metabolite from endophytic Aspergillus flavus L7 isolated from Aegle marmelos. Curr Microbiol. 2015;71:39-48. https://doi.org/10.1007/s00284-015-0805-y
  35. Qadri M, Johri S, Shah BA, et al. Identification and bioactive potential of endophytic fungi isolated from selected plants of the Western Himalayas. Springer Plus. 2013;2:8-17. https://doi.org/10.1186/2193-1801-2-8
  36. Crozier J, Thomas SE, Aime MC, et al. Molecular characterization of fungal endophytic morphospecies isolated from stems and pods of Theobroma cacao. Plant Pathol. 2006;55:783-791. https://doi.org/10.1111/j.1365-3059.2006.01446.x
  37. Castillo UF, Strobel GA, Ford EJ, et al. Munumbicins, wide-spectrum antibiotics produced by Streptomyces NRRL 30562 endophytic on Kennedia nigriscans. Microbiology. 2002;148:2675-2685. https://doi.org/10.1099/00221287-148-9-2675
  38. Deshidi R, Devari S, Kushwaha M, et al. Isolation and quantification of alternariols from endophytic fungus, Alternaria alternata: LCESI-MS/MS analysis. Chemistry Select. 2017;2:364-368.
  39. Lawrence R, Tripathi P, Jeyakumar E. Isolation, purification and evaluation of antibacterial agents from Aloe vera. Braz J Microbiol. 2009;40:906-915. https://doi.org/10.1590/S1517-83822009000400023
  40. Biswas B, Rogers K, McLaughlin F, et al. Antimicrobial activities of leaf extracts of guava (Psidium guajava L.) on two gram-negative and gram-positive bacteria. Int J Microbiol. 2013;2013:1-7.
  41. Kumar S, Upadhyay R, Aharwal RP, et al. Antibacterial activity of some isolated endophytic fungi from Menthe viridis. Int J App Biol Pharm Technol. 2016;7:239-248.
  42. Devaraju R, Satish S. Endophytic mycoflora of Mirabilis jalapa L. and studies on antimicrobial activity of its endophytic Fusarium spp. Asian J Biol Sci. 2011;2:75-79.
  43. Darshana CN, Praveena R, Ankegowda SJ, et al. Morphological variability, mycelial compatibility and fungicidal sensitivity of Colletotrichum gloeosporioides causing leaf spot of ginger (Zingiber officinale Rosc. J Spices Arom Crops. 2014;23:211-223.
  44. Monkai J, Promputtha I, Kodsueb R, et al. Fungi on decaying leaves of Magnolia liliifera and Cinnamomum iners show litter fungi to be hyperdiverse. Mycosphere. 2013;4:292-301. https://doi.org/10.5943/mycosphere/4/2/12
  45. Toledo AV, Virla E, Humber RA, et al. First record of Clonostachys rosea (Ascomycota: Hypocreales) as an entomopathogenic fungus of Oncometopia tucumana and Sonesimia grossa (Hemiptera: Cicadellidae) in Argentina. J Invertebr Pathol. 2006;92:7-10. https://doi.org/10.1016/j.jip.2005.10.005
  46. Zhai MM, Qi FM, Li J, et al. Isolation of secondary metabolites from the soil-derived fungus Clonostachys rosea YRS-06, a biological control agent, and evaluation of antibacterial activity. J Agric Food Chem. 2016;64:2298-2306. https://doi.org/10.1021/acs.jafc.6b00556
  47. Gong LJ, Guo SX. Endophytic fungi from Dracaena combodiana and Aquilaria sinensis and their antimicrobial activity. Afr J Biotechnol. 2009;8:731-736.
  48. Motaal A, Nassar SM, Zayat SA, et al. Antifungal activity of endophytic fungi isolated from Egyptian henbane (Hyoscyamus Muticus L). Pak J Bot. 2010;42:2883-2894.
  49. Rabha AJ, Naglot A, Sharma GD, et al. In vitro evaluation of antimicrobial activity of Colletotrichum spp. against potent fungal pathogens of tea. Ind J Microbiol. 2014;54:302-309. https://doi.org/10.1007/s12088-014-0458-8
  50. Orlandelli RA, de Almeida TT, Alberto RN, et al. Antifungal and proteolytic activities of endophytic fungi isolated from Piper hispidum Sw. Braz J Microbiol. 2015;46:359-366. https://doi.org/10.1590/S1517-838246220131042
  51. Yadav M, Yadav A, Yadav JP. In vitro antioxidant activity and total phenolic content of endophytic fungi isolated from Eugenia jambolana Lam. Asian Pac J Trop Med. 2014;7:256-261. https://doi.org/10.1016/S1995-7645(14)60242-X
  52. Vasundhara M, Baranwal M, Kumar A. Fusarium tricinctum, an endophytic fungus exhibits cell growth inhibition and antioxidant activity. Ind J Microbiol. 2016;56:433-438. https://doi.org/10.1007/s12088-016-0600-x
  53. Tohidi B, Rahimmalek M, Arzani A. Essential oil composition, total phenolic, flavonoid contents, and antioxidant activity of Thymus species collected from different regions of Iran. Food Chem. 2017;220:153-161. https://doi.org/10.1016/j.foodchem.2016.09.203

Cited by

  1. A Survey of Endophytic Fungi Associated with High-Risk Plants Imported for Ornamental Purposes vol.10, pp.12, 2018, https://doi.org/10.3390/agriculture10120643
  2. Engineering Host Microbiome for Crop Improvement and Sustainable Agriculture vol.12, pp.None, 2021, https://doi.org/10.3389/fmicb.2021.635917
  3. Diversity and biological activity of fungal endophytes of Zingiber officinale Rosc. with emphasis on Aspergillus terreus as a biocontrol agent of its leaf spot vol.39, pp.None, 2022, https://doi.org/10.1016/j.bcab.2021.102234