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Cannabis Endophytes and Their Application in Breeding and Physiological Fitness

Abstract

Plant-associated endophytes live in mutualistic association with their hosts wherein a plethora of physiological, chemical, and molecular interactions are responsible maintaining their association. In this chapter, we explore the multifaceted potential of endophytes harbored in Cannabis sativa L. plants in interacting not only with the host plants, but also with invading pathogens and associated endophytic microflora, resulting in diverse functional traits. These traits range from production of bioactive natural products, attenuation of virulence factors of invading phytopathogens, to providing host plant fitness and maintaining ecological interactions. We further elaborate the ecological relevance of endophytes harbored in the liverwort, Radula marginata that produces secondary metabolites structurally similar to those found in Cannabis plants. Until now, research on endophytic microflora of C. sativa prospected from different ecosystems has yielded interesting fundamental insights into plant-microbe and microbe-microbe interactions, which have direct or indirect biotechnological implications. Therefore, we discuss the possible benefits of using Cannabis and Radula endophytes in the pharmaceutical and agricultural sectors, and the biotechnological approaches required to commercialize selected endophytes.

Keywords

  • Endophytic Bacterium
  • Fungal Endophyte
  • Bacterial Endophyte
  • Bioactive Secondary Metabolite
  • Quorum Quenching

These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  • Afzal I, Shinwari ZK, Iqrar I (2015) Selective isolation and characterization of agriculturally beneficial endophytic bacteria from wild hemp using canola. Pak J Bot 47:1999–2008

    CAS  Google Scholar 

  • 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

    CrossRef  CAS  PubMed  PubMed Central  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

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Asakawa Y, Hashimoto T, Takikawa K, Tori M, Ogawa S (1991a) Prenyl bibenzyls from the liverworts Radula perrottetti and Radula complanata. Phytochemistry 30:235–251

    CrossRef  CAS  Google Scholar 

  • Asakawa Y, Hashimoto T, Takikawa K, Tori M, Ogawa S (1991b) Prenyl bibenzyls from the liverwort Radula kojana. Phytochemistry 30:219–234

    CrossRef  CAS  Google Scholar 

  • Bacon CW, White JF (2000) Microbial endophytes. Marcel Deker Inc, New York

    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

    CrossRef  CAS  Google Scholar 

  • Blakeslee JJ, Murphy AS (2016) Microscopic and biochemical visualization of auxins in plant tissues. In: Duque Paula (ed) Environmental responses in plants, methods and protocols, methods in molecular biology. Springer, New York, pp 37–53

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    CrossRef  Google Scholar 

  • Carchman RA, Harris LS, Munson AE (1976) The inhibition of DNA synthesis by cannabinoids. Cancer Res 36:95–100

    CAS  PubMed  Google Scholar 

  • Cegelski L, Marshall GR, Eldridge GR, Hultgren SJ (2008) The biology and future prospects of antivirulence therapies. Nat Rev Microbiol 6:17–27

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Chandra S, Lata H, Khan IA, ElSohly MA (2013) The role of biotechnology in Cannabis sativa propagation for the production of phytocannabinoids. In: Chandra S et al (eds) Biotechnology for medical plants. Springer-Verlag, Berlin Heidelberg, pp 123–148

    CrossRef  Google Scholar 

  • Chaohua C, Gonggu Z, Lining Z, Chunsheng G, Qing T, Jianhua C, Xinbo G, Dingxiang P, Jianguang S (2016) A rapid shoot regeneration protocol from the cotyledons of hemp (Cannabis sativa L.). Ind Crop Prod 83:61–65

    CrossRef  Google Scholar 

  • Claessen D, Rozen DE, Kuipers OP, Søgaard-Andersen L, vanWezel GP (2014) Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat Rev Microbiol 12:115–124

    CrossRef  CAS  PubMed  Google Scholar 

  • Clatworthy AE, Pierson E, Hung DT (2007) Targeting virulence: a new paradigm for antimicrobial therapy. Nat Chem Biol 3:541–548

    CrossRef  CAS  PubMed  Google Scholar 

  • Cornforth DM, Popat R, McNally L, Gurney J, Scott-Phillips TC, Ivens A, Diggle SP, Brown SP (2014) Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. Proc Natl Acad Sci U S A 111:4280–4284

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Cullmann F, Becker H (1999) Prenylated bibenzyls from the liverwort Radula laxiramea. Z Naturforsch J Biosci 54:147–150

    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

    CrossRef  Google Scholar 

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

    CrossRef  CAS  PubMed  Google Scholar 

  • Ezra D, Hess WH, Strobel GA (2004) New endophytic isolates of M. albus, a volatile antibiotic-producing fungus. Microbiology 150:4023–4031

    CrossRef  CAS  PubMed  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

    CrossRef  CAS  PubMed  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

    CrossRef  Google Scholar 

  • Flemming T, Muntendam R, Steup C, Kayser O (2007) Chemistry and biological activity of tetrahydrocannabinol and its derivatives. In: Khan MTH (ed) Topics in heterocyclic chemistry, vol 10. Springer-Verlag, Berlin/Heidelberg, pp 1–42

    Google Scholar 

  • Flores-Sanchez IJ, Pec J, Fei J, Choi YH, Dusek J, Verpoorte R (2009) Elicitation studies in cell suspension cultures of Cannabis sativa L. J Biotechnol 143:157–168

    CrossRef  CAS  PubMed  Google Scholar 

  • Gautam AK, Kant M, Thakur Y (2013) Isolation of endophytic fungi from Cannabis sativa and study their antifungal potential. Archives Phytopathol Plant Protect 46:627–635

    CrossRef  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

    CrossRef  CAS  PubMed  Google Scholar 

  • Grotenhermen F, Müller-Vahl K (2012) The therapeutic potential of Cannabis and cannabinoids. Medicine 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

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Hallmann J, Berg G, Schulz B (2007) Isolation procedures for endophytic microorganisms. Springer, Berlin, Heidelberg, New York (NY)

    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

    CrossRef  Google Scholar 

  • Hartmann A, Rothballer M, Hense BA, Schröder P (2014) Bacterial quorum sensing compounds are important modulators of microbe-plant interactions. Front Plant Sci 5:131

    CrossRef  PubMed  PubMed Central  Google Scholar 

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

    CrossRef  CAS  PubMed  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

    CrossRef  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

    CrossRef  CAS  PubMed  Google Scholar 

  • Hong K-W, Koh C-L, Sam C-K, Yin Y-F, Chan K-G (2012) Quorum quenching revisited—from signal decays to signaling confusion. Sensors 12:4661–4696

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Hosni T, Moretti C, Devescovi G, Suarez-Moreno ZR, Fatmi MB, Guarnaccia C, Pongor S, Onofri A, Buonaurio R, Venturi V (2011) Sharing of quorum-sensing signals and role of interspecies communities in a bacterial plant disease. ISME J 5:1857–1870

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

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

    CrossRef  CAS  PubMed  Google Scholar 

  • Kunzmann MH, Bach NC, Bauer B, Sieber SA (2014) α-Methylene-γ-butyrolactones attenuate Staphylococcus aureus virulence by inhibition of transcriptional regulation. Chem Sci 5:1158–1167

    CrossRef  CAS  Google Scholar 

  • Kusari P, Kusari S, Eckelmann D, Zuelhke S, Kayser O, Spiteller M (2016) Cross-species biosynthesis of maytansine in Maytenus serrata. RSC Advances 6:10011–10016

    CrossRef  CAS  Google Scholar 

  • Kusari P, Kusari S, Lamshoeft M, Sezgin S, Spiteller M, Kayser O (2014a) Quorum quenching is an antivirulence strategy employed by endophytic bacteria. Appl Microbiol Biotechnol 98:7173–7183

    CrossRef  CAS  PubMed  Google Scholar 

  • Kusari P, Kusari S, Spiteller M, Kayser O (2013) Endophytic fungi harbored in Cannabis sativa L.: diversity and potential as biocontrol agents against host plant-specific phytopathogens. Fungal Divers 60:137–151

    CrossRef  Google Scholar 

  • Kusari P, Kusari S, Spiteller M, Kayser O (2014b) Biocontrol potential of endophytes harbored in Radula marginata (liverwort) from the New Zealand ecosystem. Antonie Van Leeuwenhoek 106:771–788

    CrossRef  CAS  PubMed  Google Scholar 

  • Kusari P, Kusari S, Spiteller M, Kayser O (2015) Implications of endophyte-plant crosstalk in light of quorum responses for plant biotechnology. Appl Microbiol Biotechnol 99:5383–5390

    CrossRef  CAS  PubMed  Google Scholar 

  • Kusari P, Spiteller M, Kayser O, Kusari S (2014c) Recent advances in research on Cannabis sativa L. endophytes and their prospect for the pharmaceutical industry. In: Kharwar RN et al (eds) Microbial diversity and biotechnology in food security. Springer, New Delhi, pp 3–15

    Google Scholar 

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

    CrossRef  CAS  PubMed  Google Scholar 

  • Kusari S, Lamshoeft M, Kusari P, Gottfried S, Zuehlke S, Louven K, Hentschel U, Kayser O, Spiteller M (2014d) Endophytes are hidden producers of maytansine in Putterlickia roots. J Nat Prod 77:2577–2584

    CrossRef  CAS  PubMed  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

    CrossRef  CAS  PubMed  Google Scholar 

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

    CrossRef  CAS  PubMed  Google Scholar 

  • Kusari S, Singh S, Jayabaskaran C (2014e) Biotechnological potential of plant-associated endophytic fungi: hope versus hype. Trends Biotechnol 32:297–303

    CrossRef  CAS  PubMed  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, pp 241-266

    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

    CrossRef  CAS  PubMed  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

    CrossRef  CAS  PubMed  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

    CrossRef  CAS  PubMed  Google Scholar 

  • LaSarre B, Federle MJ (2013) Exploiting quorum sensing to confuse bacterial pathogens. Microbiol Mol Biol Rev 77:73–111

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Leekha S, Terrel CL, Edson RS (2011) General principles of antimicrobial therapy. Mayo Clin Proc 86:156–167

    CrossRef  PubMed  PubMed Central  Google Scholar 

  • Li G, Kusari S, Kusari P, Kayser O, Spiteller M (2015) Endophytic Diaporthe sp. LG23 produces a potent antibacterial tetracyclic triterpenoid. J Nat Prod 78:2128–2132

    CrossRef  CAS  PubMed  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

    CrossRef  Google Scholar 

  • Liu F, Bian Z, Jia Z, Zhao Q, Song S (2012) The GCR1 and GPA1 participate in promotion of Arabidopsis primary root elongation induced by N-acyl-homoserine lactones, the bacterial quorumsensing system. Mol Plant Microbe Interact 25:677–683

    CrossRef  CAS  PubMed  Google Scholar 

  • Ludwiczuk A, Asakawa Y (2008) Distribution of terpenoids and aromatic compounds in selected southern hemispheric liverworts. In: Fieldiana Botany Number 47. Field Museum of Natural History, Chicago, pp 37–58

    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

    CrossRef  PubMed  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

    CrossRef  Google Scholar 

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

    CrossRef  Google Scholar 

  • Mustafa NR, de Winter W, van Iren F, Verpoorte R (2011) Initiation, growth and cryopreservation of plant cell suspension cultures. Nat Protoc 6:715–742

    CrossRef  CAS  PubMed  Google Scholar 

  • Newman DJ, Cragg GM (2015) Endophytic and epiphytic microbes as “sources” of bioactive agents. Front Chem. doi:10.3389/fchem.2015.00034

    PubMed  PubMed Central  Google Scholar 

  • Pandotra VR, Sastry KSM (1967) Wilt: a new disease of hemp in India. Indian J Agr Sci 37:520

    Google Scholar 

  • Park BH, Lee YR (2010) Concise synthesis of (±)-perrottetinene with bibenzyl cannabinoid. Bull Korean Chem Soc 31:2712–2714

    CrossRef  CAS  Google Scholar 

  • Partida MLP, Hertweck C (2005) Pathogenic fungus harbors endosymbiotic bacteria for toxin production. Nature 437:884–888

    CrossRef  Google Scholar 

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

    CrossRef  Google Scholar 

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

    CrossRef  CAS  PubMed  Google Scholar 

  • Qadri M, Johri S, Shah BA, Khajuria A, Sidiq T, Lattoo SK, Abdin MZ, Riyaz-Ul-Hassan S (2013) Identification and bioactive potential of endophytic fungi isolated from selected plants of the Western Himalayas. SpringerPlus 2:8

    CrossRef  PubMed  PubMed Central  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

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Raharjo TJ, Eucharia O, Chang W-T, Verpoorte R (2006) Callus induction and phytochemical characterization of Cannabis sativa cell suspension cultures. Indo J Chem 6:70–74

    Google Scholar 

  • Rajesh PS, Rai VR (2014) Quorumquenching activity in cell-free lysate of endophytic bacteria isolated from Pterocarpus santalinus Linn., and its effect on quorum sensing regulated biofilm in Pseudomonas aeruginosa PAO1. Microbiol Res 169:561–569

    CrossRef  CAS  PubMed  Google Scholar 

  • Rashid S, Charles TC, Glick BR (2012) Isolation and characterization of new plant growth-promoting bacterial endophytes. Appl Soil Ecol 61:217–224

    CrossRef  Google Scholar 

  • Rasko DA, Sperandio V (2010) Anti-virulence strategies to combat bacteria-mediated disease. Nat Rev Drug Discov 9:117–128

    CrossRef  CAS  PubMed  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

    CrossRef  CAS  PubMed  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

    CrossRef  CAS  PubMed  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

    CrossRef  PubMed  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

    CrossRef  Google Scholar 

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

    CrossRef  CAS  PubMed  Google Scholar 

  • Safari M, Amache R, Esmaeilishirazifard E, Keshavarz T (2014) Microbial metabolism of quorum-sensing molecules acylhomoserine lactones, γ-heptalactone and other lactones. Appl Microbiol Biotechnol 98:3401–3412

    CrossRef  CAS  PubMed  Google Scholar 

  • Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449

    CrossRef  CAS  PubMed  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

    CrossRef  CAS  PubMed  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 

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

    CrossRef  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

    CrossRef  CAS  PubMed  Google Scholar 

  • Smits THM, Rezzonico F, Kamber T, Blom J, Goesmann A, Ishimaru CA, Frey CE, Stockwell VO, Duffy B (2011) Metabolic versatility and antibacterial metabolite biosynthesis are distinguishing genomic features of the fire blight antagonist Pantoeavagans C9-1. PLoS ONE 6:e22247

    CrossRef  CAS  PubMed  PubMed Central  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

    CrossRef  CAS  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

    CrossRef  CAS  Google Scholar 

  • Taura F, Sirikantaramas S, Shoyamaa Y, Shoyamaa Y, Morimotoa S (2007) Phytocannabinoids in Cannabis sativa: Recent Studies on Biosynthetic Enzymes. Chem Biodivers 4:1649–1663

    CrossRef  CAS  PubMed  Google Scholar 

  • Teplitski M, Mathesius U, Rumbaugh KP (2011) Perception and degradation of N-acyl homoserine lactone quorum sensing signals by mammalian and plant cells. Chem Rev 111:100–116

    CrossRef  CAS  PubMed  Google Scholar 

  • Toyota M, Kinugawa T, Asakawa Y (1994) Bibenzyl cannabinoid and bisbibenzyl derivative from the liverwort Radula perrottetti. Phytochemistry 37:859–862

    CrossRef  CAS  Google Scholar 

  • Toyota M, Shimamura T, Ishii H, Renner M, Braggins J, Asakawa Y (2002) New bibenzyl cannabinoid from the New Zealand liverwort Radula marginata. Chem Pharm Bull 50:1390–1392

    CrossRef  CAS  PubMed  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

    CrossRef  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang WX, Kusari S, Laatsch H, Golz C, Kusari P, Strohmann C, Kayser O, Spiteller M (2016) Antibacterial Azaphilones from an Endophytic Fungus, Colletotrichum sp. BS4. J Nat Prod doi:10.1021/acs.jnatprod.5b00436

  • Wang WX, Kusari S, Sezgin S, Lamshöft M, Kusari P, Kayser O, Spiteller M (2015) Hexacyclopeptides secreted by an endophytic fungus Fusarium solani N06 act as crosstalk molecules in Narcissus tazetta. Appl Microbiol Biotechnol 99:7651–7662

    CrossRef  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Williamson EM, Evans FJ (2000) Cannabinoids in clinical practice. Drugs 60: 1303–131

    Google Scholar 

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Acknowledgements

We gratefully acknowledge the Ministry of Innovation, Science, Research, and Technology of the State of North Rhine-Westphalia (CLIB), Germany and TU Dortmund for funding.

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Kusari, P., Kusari, S., Spiteller, M., Kayser, O. (2017). Cannabis Endophytes and Their Application in Breeding and Physiological Fitness. In: Chandra, S., Lata, H., ElSohly, M. (eds) Cannabis sativa L. - Botany and Biotechnology. Springer, Cham. https://doi.org/10.1007/978-3-319-54564-6_20

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