Skip to main content
SpringerLink
Log in

Endophytic fungi harbored in Cannabis sativa L.: diversity and potential as biocontrol agents against host plant-specific phytopathogens

Fungal Diversity volume 60, pages 137–151 (2013)Cite this article

Abstract

The objective of the present work was isolation, phylogenetic characterization, and assessment of biocontrol potential of endophytic fungi harbored in various tissues (leaves, twigs, and apical and lateral buds) of the medicinal plant, Cannabis sativa L. A total of 30 different fungal endophytes were isolated from all the plant tissues which were authenticated by molecular identification based on rDNA ITS sequence analysis (ITS1, 5.8S and ITS2 regions). The Menhinick’s index revealed that the buds were immensely rich in fungal species, and Camargo’s index showed the highest tissue-specific fungal dominance for the twigs. The most dominant species was Penicillium copticola that could be isolated from the twigs, leaves, and apical and lateral buds. A detailed calculation of Fisher’s log series index, Shannon diversity index, Simpson’s index, Simpson’s diversity index, and Margalef’s richness revealed moderate overall biodiversity of C. sativa endophytes distributed among its tissues. The fungal endophytes were challenged by two host phytopathogens, Botrytis cinerea and Trichothecium roseum, devising a dual culture antagonistic assay on five different media. We observed 11 distinct types of pathogen inhibition encompassing a variable degree of antagonism (%) on changing the media. This revealed the potential chemodiversity of the isolated fungal endophytes not only as promising resources of biocontrol agents against the known and emerging phytopathogens of Cannabis plants, but also as sustainable resources of biologically active and defensive secondary metabolites.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  • Ahmed SA, Ross SA, Slade D, Radwan MM, Zulfiqar F, ElSohly MA (2008) Cannabinoid ester constituents from high-potency Cannabis sativa. J Nat Prod 71:536–542

    Article  PubMed  CAS  Google Scholar 

  • Aly AH, Debbab A, Kjer J, Proksch P (2010) Fungal endophytes from higher plants: a prolific source of phytochemicals and other bioactive natural products. Fungal Divers 41:1–16

    Article  Google Scholar 

  • Aly AH, Debbab A, Proksch P (2011) Fifty years of drug discovery from fungi. Fungal Divers 50:3–19

    Article  Google Scholar 

  • Arabatzis M, Kambouris M, Kyprianou M, Chrysaki A, Foustoukou M, Kanellopoulou M, Kondyli L, Kouppari G, Koutsia-Karouzou C, Lebessi E, Pangalis A, Petinaki E, Stathi A, Trikka-Graphakos E, Vartzioti E, Vogiatzi A, Vyzantiadis TA, Zerva L, Velegraki A (2011) Polyphasic identification and susceptibility to seven antifungals of 102 Aspergillus isolates recovered from immunocompromised hosts in Greece. Antimicrob Agents Chemother 55:3025–3030

    Article  PubMed  CAS  Google Scholar 

  • Arnold AE, Mejia LC, Kyllo D, Rojas EI, Maynard Z, Robbins N (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci U S A 100:15649–15654

    Article  PubMed  CAS  Google Scholar 

  • Baker D, Pryce G, Giovannoni G, Thompson AJ (2003) The therapeutic potential of cannabis. Lancet Neurol 2:291–298

    Article  PubMed  CAS  Google Scholar 

  • Barloy J, Pelhate J (1962) PremiËres observations phytopathologiques relatives aux cultures de chanvre en Anjou. Ann Epiphyties 13:117–149

    Google Scholar 

  • Berbee ML (2001) The phylogeny of plant and animal pathogens in the Ascomycota. Physiol Mol Plant Pathol 59:165–187

    Article  CAS  Google Scholar 

  • Bode HB, Bethe B, Höfs R, Zeeck A (2002) Big effects from small changes: possible ways to explore nature’s chemical diversity. ChemBioChem 3:619–627

    Article  PubMed  CAS  Google Scholar 

  • Botella L, Diez JJ (2011) Phylogenic diversity of fungal endophytes in Spanish stands of Pinus halepensis. Fungal Divers 47:9–18

    Article  Google Scholar 

  • Bush Doctor, The (1985) Damping off. Sinsemilla Tips 5:35–39

  • Bush Doctor, The (1993) How to preserve pot potency. High Times No 213: 75, 77–78

  • Camargo JA (1992) Can dominance influence stability in competitive interactions? Oikos 64:605–609

    Article  Google Scholar 

  • Chamberlain K, Crawford DL (1999) In vitro and in vivo antagonism of pathogenic turfgrass fungi by Streptomyces hygroscopicus strains YCED9 and WYE53. J Ind Microbiol Biotechnol 23:641–646

    Article  PubMed  CAS  Google Scholar 

  • Debbab A, Aly AH, Proksch P (2012) Endophytes and associated marine derived fungi-ecological and chemical perspectives. Fungal Divers 57:45–83

    Article  Google Scholar 

  • Dewey LH (1914) “Hemp.” In: U.S.D.A. yearbook 1913 United States Department of Agriculture, Washington DC, pp 283–347

  • Eaton CJ, Cox MP, Scott B (2011) What triggers grass endophytes to switch from mutualism to pathogenism? Plant Sci 180:190–195

    Article  PubMed  CAS  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acid Res 32:1792–1797

    Article  PubMed  CAS  Google Scholar 

  • ElSohly MA, Slade D (2005) Chemical constituents of marijuana: the complex mixture of natural cannabinoids. Life Sci 78:539–548

    Article  PubMed  CAS  Google Scholar 

  • ElSohly MA, Wachtel SR, de Wit H (2003) Cannabis versus THC: response to Russo and McPartland. Psychopharmacology 165:433–434

    CAS  Google Scholar 

  • Eyberger AL, Dondapati R, Porter JR (2006) Endophyte fungal isolates from Podophyllum peltatum produce podophyllotoxin. J Nat Prod 69:1121–1124

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fischedick JT, Hazekamp A, Erkelens T, Choi YH, Verpoorte R (2010) Metabolic fingerprinting of Cannabis sativa L., cannabinoids and terpenoids for chemotaxonomic and drug standardization purposes. Phytochemistry 71:2058–2073

    Article  PubMed  CAS  Google Scholar 

  • Fisher RA, Corbet AS, Williams CB (1943) The relation between the number of species and the number of individuals in a random sample of an animal population. J Anim Ecol 12:42–58

    Article  Google Scholar 

  • Gazis R, Rehner S, Chaverri P (2011) Species delimitation in fungal endophyte diversity studies and its implications in ecological and biogeographic inferences. Mol Ecol 20:3001–3013

    Article  PubMed  Google Scholar 

  • Gomes A, Fernandes E, Lima JLFC, Mira L, Corvo ML (2008) Molecular mechanisms of anti-inflammatory activity mediated by flavonoids. Curr Med Chem 15:1586–1605

    Article  PubMed  CAS  Google Scholar 

  • Grotenhermen F, Müller-Vahl K (2012) The therapeutic potential of cannabis and cannabinoids. Dtsch Arztebl Int 109:495–501

    PubMed  Google Scholar 

  • Gunatilaka AAL (2006) Natural products from plant-associated microorganisms: distribution, structural diversity, bioactivity, and implications of their occurrence. J Nat Prod 69:509–526

    Article  PubMed  CAS  Google Scholar 

  • Hamilton CE, Bauerle TL (2012) A new currency for mutualism? fungal endophytes alter antioxidant activity in hosts responding to drought. Fungal Divers 54:39–49

    Article  Google Scholar 

  • Hamilton CE, Gundel PE, Helander M, Saikkonen K (2012) Endophytic mediation of reactive oxygen species and antioxidant activity in plants: a review. Fungal Divers 54:1–10

    Article  Google Scholar 

  • Han G, Feng X, Tian X (2011) Isolation and evaluation of terrestrial fungi with algicidal ability from Zijin Mountain, Nanjing, China. Microbiology (Reading, Engl), in press

  • Hazekamp A, Choi YH, Verpoorte R (2004) Quantitative analysis of cannabinoids from Cannabis sativa using 1H-NMR. Chem Pharm Bull 52:718–721

    Article  PubMed  CAS  Google Scholar 

  • Hazekamp A, Giroud C, Peltenburg A, Verpoorte R (2005) Spectroscopic and chromatographic data of cannabinoids from Cannabis sativa. J Liq Chromatogr Relat Technol 28:2361–2382

    Article  CAS  Google Scholar 

  • Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133

    Article  PubMed  CAS  Google Scholar 

  • Hockey JF (1927) Report of the Dominion field laboratory of plant pathology, Kentville Nova Scotia. Can Dep Agric 28–36

  • Hoffman M, Gunatilaka M, Ong J, Shimabukuro M, Arnold AE (2008) Molecular analysis reveals a distinctive fungal endophyte community associated with foliage of Montane oaks in southeastern Arizona. J Ariz Nev Acad Sci 40:91–100

    Article  Google Scholar 

  • Houbraken J, Frisvad JC, Samson RA (2011) Taxonomy of Penicillium section Citrina. Stud Mycol 70:53–138

    Article  PubMed  CAS  Google Scholar 

  • Hyde KD, Soytong K (2008) The fungal endophyte dilemma. Fungal Divers 33:163–173

    Google Scholar 

  • Jang Y, Huh N, Lee J, Lee JS, Kim GH, Kim JJ (2011) Phylogenetic analysis of major molds inhabiting woods and their discoloration characteristics Part 2. Genus Penicillium. Holzforschung 65:265–270

    Article  CAS  Google Scholar 

  • Jiang HE, Li X, Zhao YX, Ferguson DK, Hueber F, Bera S, Wang YF, Zhao LC, Liu CJ, Li CS (2006) A new insight into Cannabis sativa (Cannabaceae) utilization from 2500-year-old Yanghai Tombs, Xinjiang, China. J Ethnopharmacol 108:414–422

    Article  PubMed  Google Scholar 

  • Kharwar RN, Mishra A, Gond SK, Stierle D (2011) Anticancer compounds derived from fungal endophytes: their importance and future challenges. Nat Prod Rep 28:1208–1228

    Article  PubMed  CAS  Google Scholar 

  • Ko TWK, Stephenson SL, Bahkali AH, Hyde KD (2011) From morphology to molecular biology: can we use sequence data to identify fungal endophytes? Fungal Divers 50:113–120

    Article  Google Scholar 

  • Kurup VP, Resnick A, Kagen SL, Cohen SH, Fink JN (1983) Allergenic fungi and actinomycetes in smoking materials and their health implications. Mycopathologia 82:61–64

    Article  PubMed  CAS  Google Scholar 

  • Kusari S, Spiteller M (2011) Are we ready for industrial production of bioactive plant secondary metabolites utilizing endophytes? Nat Prod Rep 28:1203–1207

    Article  PubMed  CAS  Google Scholar 

  • Kusari S, Spiteller M (2012) Metabolomics of endophytic fungi producing associated plant secondary metabolites: progress, challenges and opportunities. In: Metabolomics U. Roessner ed. (InTech ISBN 978-953-51-0046-1):241–266

  • Kusari S, Lamshöft M, Zühlke S, Spiteller M (2008) An endophytic fungus from Hypericum perforatum that produces hypericin. J Nat Prod 71:159–162

    Article  PubMed  CAS  Google Scholar 

  • Kusari S, Lamshöft M, Spiteller M (2009a) Aspergillus fumigatus Fresenius, an endophytic fungus from Juniperus communis L. Horstmann as a novel source of the anticancer pro-drug deoxypodophyllotoxin. J Appl Microbiol 107:1019–1030

    Article  PubMed  CAS  Google Scholar 

  • Kusari S, Zuehlke S, Spiteller M (2009b) An endophytic fungus from Camptotheca acuminata that produces camptothecin and analogues. J Nat Prod 72:2–7

    Article  PubMed  CAS  Google Scholar 

  • Kusari S, Zühlke S, Kosuth J, Cellarova E, Spiteller M (2009c) Light-independent metabolomics of endophytic Thielavia subthermophila provides insight into microbial hypericin biosynthesis. J Nat Prod 72:1825–1835

    Article  PubMed  CAS  Google Scholar 

  • Kusari S, Zühlke S, Spiteller M (2011) Effect of artificial reconstitution of the interaction between the plant Camptotheca acuminata and the fungal endophyte Fusarium solani on camptothecin biosynthesis. J Nat Prod 74:764–775

    Article  PubMed  CAS  Google Scholar 

  • Kusari S, Hertweck C, Spiteller M (2012a) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19:792–798

    Article  PubMed  CAS  Google Scholar 

  • Kusari S, Verma VC, Lamshöft M, Spiteller M (2012b) An endophytic fungus from Azadirachta indica A. Juss. that produces azadirachtin. World J Microbiol Biotechnol 28:1287–1294

    Article  PubMed  CAS  Google Scholar 

  • Lambshead PJD, Hodda M (1994) The impact of disturbance on measurements of variability in marine nematode populations. Vie et Milieu 44:21–27

    Google Scholar 

  • Lambshead PJD, Platt HM, Shaw KM (1983) Detection of differences among assemblages of marine benthic species based on an assessment of dominance and diversity. J Nat Hist 17:859–874

    Article  Google Scholar 

  • Levitz SM, Diamond RD (1991) Aspergillosis and marijuana. Ann Intern Med 115:578–579

    Article  PubMed  CAS  Google Scholar 

  • Li H-Y, Wei D-Q, Shen M, Zhou J-P (2012) Endophytes and their role in phytoremediation. Fungal Divers 54:11–18

    Article  Google Scholar 

  • Margalef R (1958) Information theory in ecology. Gen Syst 3:36–71

    Google Scholar 

  • Márquez LM, Redman RS, Rodriguez RJ, Roossinck MJ (2007) A virus in a fungus in a plant: three-way symbiosis required for thermal tolerance. Science 315:513–515

    Article  PubMed  CAS  Google Scholar 

  • McAleece N, Gage JDG, Lambshead PJD, Paterson GLJ (1997) BioDiversity Professional statistics analysis software Jointly developed by the Scottish Association for Marine Science and the Natural History Museum London

  • McPartland JM (1983) Fungal pathogens of Cannabis sativa in Illinois. Phytopathology 72:797

    Google Scholar 

  • McPartland JM (1991) Common names for diseases of Cannabis sativa L. Plant Dis 75:226–227

    Google Scholar 

  • McPartland JM (1994) Microbiological contaminants of marijuana. J Int Hemp Assoc 1:41–44

    Google Scholar 

  • McPartland JM (1995) Cannabis pathogens X: Phoma, Ascochyta and Didymella species. Mycologia 86:870–878

    Article  Google Scholar 

  • McPartland JM (1996) A review of Cannabis diseases. J Int Hemp Assoc 3:19–23

    Google Scholar 

  • Miles LA, Lopera CA, González S, Cepero de García MC, Franco AE, Restrepo S (2012) Exploring the biocontrol potential of fungal endophytes from an Andean Colombian Paramo ecosystem. BioControl, in press, doi:10.1007/s10526-012-9442-6

  • Mojzisova G, Mojzis J (2008) Flavonoids and their potential health benefits: relation to heart diseases and cancer. Recent Prog Med Plants 21:105–129

    CAS  Google Scholar 

  • Mueller GM, Schmit JP (2007) Fungal biodiversity: what do we know? what can we predict? Biodivers Conserv 16:1–5

    Article  Google Scholar 

  • Paranagama PA, Wijeratne EMK, Gunatilaka AAL (2007) Uncovering biosynthetic potential of plant-associated fungi: effect of culture conditions on metabolite production by Paraphaeosphaeria quadriseptata and Chaetomium chiversii. J Nat Prod 70:1939–1945

    Article  PubMed  CAS  Google Scholar 

  • Pertwee RG (2006) Cannabinoid pharmacology: the first 66 years. Br J Pharmacol 147:163–171

    Article  CAS  Google Scholar 

  • Porras-Alfaro A, Bayman P (2011) Hidden fungi, emergent properties: endophytes and microbiomes. Annu Rev Phytopathol 49:291–315

    Article  PubMed  CAS  Google Scholar 

  • Purahong W, Hyde KD (2011) Effects of fungal endophytes on grass and non-grass litter decomposition rates. Fungal Divers 47:1–7

    Article  Google Scholar 

  • Radwan MM, Ross SA, Slade D, Ahmed SA, Zulfiqar F, ElSohly MA (2008) Isolation and characterization of new cannabis constituents from a high potency variety. Planta Med 74:267–272

    Article  PubMed  CAS  Google Scholar 

  • Rajulu MBG, Thirunavukkarasu N, Suryanarayanan TS, Ravishankar JP, Gueddari NEE, Moerschbacher BM (2011) Chitinolytic enzymes from endophytic fungi. Fungal Divers 47:43–53

    Article  Google Scholar 

  • Rakeman JL, Bui U, Lafe K, Chen YC, Honeycutt RJ, Cookson BT (2005) Multilocus DNA sequence comparisons rapidly identify pathogenic molds. J Clin Microbiol 43:3324–3333

    Article  PubMed  CAS  Google Scholar 

  • Redman RS, Sheehan KB, Stout RG, Rodriguez RJ, Henson JM (2002) Thermotolerance conferred to plant host and fungal endophyte during mutualistic symbiosis. Science 298:1581

    Article  PubMed  CAS  Google Scholar 

  • Rodrigues A, Mueller UG, Ishak HD, Bacci M Jr, Pagnocca FC (2011) Ecology of microfungal communities in gardens of fungus-growing ants (Hymenoptera: Formicidae): a year-long survey of three species of attine ants in Central Texas. FEMS Microbiol Ecol 78:244–255

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez R, Redman R (2008) More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J Exp Bot 59:1109–1114

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez RJ, Redman RS, Henson JM (2004) The role of fungal symbioses in the adaptation of plants to high stress environments. Mitig Adapt Strateg Glob Chang 9:261–272

    Article  Google Scholar 

  • Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim YO, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416

    Article  PubMed  Google Scholar 

  • Russo EB, McPartland JM (2003) Cannabis is more than simply delta(9)-tetrahydrocannabinol. Psychopharmacology (Berl) 165:431–432

    CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sánchez Márquez S, Bills GF, Zabalgogeazcoa I (2007) The endophytic mycobiota of the grass Dactylis glomerata. Fungal Divers 27:171–195

    Google Scholar 

  • Scherlach K, Hertweck C (2009) Triggering cryptic natural product biosynthesis in microorganisms. Org Biomol Chem 7:1753–1760

    Article  PubMed  CAS  Google Scholar 

  • Schulz B, Guske S, Dammann U, Boyle C (1998) Endophyte-host interactions II. Defining symbiosis of the endophyte-host interaction. Symbiosis 25:213–227

    Google Scholar 

  • Schulz B, Roemmert AK, Dammann U, Aust HJ, Strack D (1999) The endophyte-host interaction: a balanced antagonism. Mycol Res 103:1275–1283

    Article  Google Scholar 

  • Schwartz IS (1985) Marijuana and fungal infection. Am J Clin Pathol 84:256

    PubMed  CAS  Google Scholar 

  • Simpson EH (1949) Measurement of diversity. Nature 163:688

    Article  Google Scholar 

  • Sirikantaramas S, Taura F, Tanaka Y, Ishikawa Y, Morimoto S, Shoyama Y (2005) Tetrahydrocannabinolic acid synthase, the enzyme controlling marijuana psychoactivity, is secreted into the storage cavity of the glandular trichomes. Plant Cell Physiol 46:1578–1582

    Article  PubMed  CAS  Google Scholar 

  • Staniek A, Woerdenbag HJ, Kayser O (2008) Endophytes: exploiting biodiversity for the improvement of natural product-based drug discovery. J Plant Interact 3:75–93

    Article  CAS  Google Scholar 

  • Stone JK, Bacon CW, White JF (2000) An overview of endophytic microbes: endophytism. In: Bacon CW, White JF (eds) Microbial endophytes. Marcel Dekker Inc, New York, pp 3–30

    Google Scholar 

  • Strobel GA, Daisy B (2003) Bioprospecting for microbial endophytes and their natural products. Microbiol Mol Biol Rev 67:491–502

    Article  PubMed  CAS  Google Scholar 

  • Strobel GA, Daisy B, Castillo U, Harper J (2004) Natural products from endophytic microorganisms. J Nat Prod 67:257–268

    Article  PubMed  CAS  Google Scholar 

  • Suryanarayanan TS, Kumaresan V (2000) Endophytic fungi of some halophytes from an estuarine mangrove forest. Mycol Res 104:1465–1467

    Article  Google Scholar 

  • Suryanarayanana TS, Thirunavukkarasub N, Govindarajulub MB, Sassec F, Jansend R, Murali TS (2009) Fungal endophytes and bioprospecting. Fungal Biol Rev 23:9–19

    Article  Google Scholar 

  • Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101:11030–11035

    Article  PubMed  CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  CAS  Google Scholar 

  • Tao G, Liu ZY, Hyde KD, Liu XZ, Yu XN (2008) Whole rDNA analysis reveals novel and endophytic fungi in Bletilla ochracea (Orchidaceae). Fungal Divers 33:101–122

    Google Scholar 

  • Taura F, Morimoto S, Shoyama Y, Mechoulam R (1995) First direct evidence for the mechanism of Δ1-tetrahydrocannabinolic acid biosynthesis. J Am Chem Soc 117:9766–9767

    Article  CAS  Google Scholar 

  • Taylor DN, Wachsmuth IK, Shangkuan YH, Schmidt EV, Barrett TJ, Schrader JS, Scherach CS, McGee HB, Feldman RA, Brenner DJ (1982) Salmonellosis associated with marijuana. N Engl J Med 306:1249–1253

    Article  PubMed  CAS  Google Scholar 

  • Trejo-Estrada SR, Sepulveda IR, Crawford DL (1998) In vitro and in vivo antagonism of Streptomyces violaceusniger YCED9 against fungal pathogens of turfgrass. World J Microbiol Biotechnol 14:865–872

    Article  Google Scholar 

  • Turner CE, Elsohly MA, Boeren EG (1980) Constituents of Cannabis sativa L. XVII a review of the natural constituents. J Nat Prod 43:169–234

    Article  PubMed  CAS  Google Scholar 

  • Ungerlerder JT, Andrysiak T, Tashkin DP, Gale RP (1982) Contamination of marijuana cigarettes with pathogenic bacteria. Cancer Treat Res 66:589–590

    Google Scholar 

  • van der Werf HMG, van Geel WCA (1994) Vezelhennep als papiergrondstof, teeltonderzoek 1987–1993 Fiber hemp as a raw material for paper, crop research 1987–1993. Report nr. 177, PAGV, Lelystad, the Netherlands, p 62

  • van der Werf HMG, van Geel WCA, Wijlhuizen M (1995) Agronomic research on hemp (Cannabis sativa L.) in the Netherlands 1987–1993. J Int Hemp Assoc 2:14–17

    Google Scholar 

  • Vesterlund S-R, Helander M, Faeth SH, Hyvönen T, Saikkonen K (2011) Environmental conditions and host plant origin override endophyte effects on invertebrate communities structure and guilds. Fungal Divers 47:109–118

    Article  Google Scholar 

  • Wachtel SR, ElSohly MA, Ross SA, Ambre J, de Wit H (2002) Comparison of the subjective effects of D9-tetrahydrocannabinol and marijuana in humans. Psychopharmacology 161:331–339

    Article  PubMed  CAS  Google Scholar 

  • Waller F, Achatz B, Baltruschat H, Fodor J, Becker K, Fischer M, Heier T, Hückelhoven R, Neumann C, von Wettstein D, Franken P, Kogel KH (2005) The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance and higher yield. Proc Natl Acad Sci U S A 102:13386–13391

    Article  PubMed  CAS  Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal rRNA genes for phylogenetics. In: Protocols: a guide to methods and applications. PCR Academic press, San Diego, pp 315–322

  • Whittaker RH (1977) Evolution of species diversity in land communities. Evol Biol 10:1–67

    Article  Google Scholar 

  • Williamson EM, Evans FJ (2000) Cannabinoids in clinical practice. Drugs 60:1303–1314

    Article  PubMed  CAS  Google Scholar 

  • Yuan ZL, Zhang CL, Lin FC, Kubicek CP (2010) Identity, diversity, and molecular phylogeny of the endophytic mycobiota in the roots of rare wild rice (Oryza granulate) from a nature reserve in Yunnan, China. Appl Environ Microbiol 76:1642–1652

    Article  PubMed  CAS  Google Scholar 

  • Zhang HW, Song YC, Tan RX (2006) Biology and chemistry of endophytes. Nat Prod Rep 23:753–771

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work was funded by the Ministry of Innovation, Science and Research of the German Federal State North Rhine-Westphalia (NRW) and TU Dortmund by scholarship to P.K. from the CLIB-Graduate Cluster Industrial Biotechnology (CLIB2021). We are grateful to the Federal Institute for Drugs and Medical Devices (Bundesinstituts für Arzneimittel und Medizinprodukte, BfArM), Bonn, Germany for granting us the necessary permissions for conducting this work (BtM number 458 49 89). We are also thankful to Bedrocan BV for kindly providing us with the Cannabis sativa L. plants.

Author information

Authors and Affiliations

  1. Department of Biochemical and Chemical Engineering, Chair of Technical Biochemistry, TU Dortmund, Emil-Figge-Str. 66, 44227, Dortmund, Germany

    Parijat Kusari & Oliver Kayser

  2. Institute of Environmental Research (INFU) of the Faculty of Chemistry, Chair of Environmental Chemistry and Analytical Chemistry, TU Dortmund, Otto-Hahn-Str. 6, 44221, Dortmund, Germany

    Souvik Kusari & Michael Spiteller

Authors
  1. Parijat Kusari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Souvik Kusari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael Spiteller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Oliver Kayser
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Oliver Kayser.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Kusari, P., Kusari, S., Spiteller, M. et al. Endophytic fungi harbored in Cannabis sativa L.: diversity and potential as biocontrol agents against host plant-specific phytopathogens. Fungal Diversity 60, 137–151 (2013). https://doi.org/10.1007/s13225-012-0216-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13225-012-0216-3

Keywords

search

Navigation