Biotechnology Letters

, Volume 37, Issue 7, pp 1325–1334 | Cite as

Plants and endophytes: equal partners in secondary metabolite production?

Review

Abstract

Well known plant production systems should be re-evaluated due to findings that the interesting metabolite might actually be produced by microbes intimately associated with the plant, so-called endophytes. Endophytes can be bacteria or fungi and they are characterized usually by the feature that they do not cause any harm to the host. Indeed, in some cases, such as mycorrhizal fungi or other growth promoting endophytes, they can be beneficial for the plant. Here some examples are reviewed where the host plant and/or endophyte metabolism can be induced by the other partner. Also, partial or complete biosynthesis pathways for plant secondary metabolites can be attributed to such endophytes. In other cases the host plant is able to metabolize substances from fungal origin. The question of the natural role of such metabolic changes for the endophyte will be briefly touched. Finally, the consequences for the use of plant cultures for secondary metabolite production is discussed.

Keywords

Antimicrobial activity Bioactive metabolites Biocontrol Endophyte In vitro conversion Secondary metabolites 

Notes

Acknowledgments

Work in the author’s laboratory on secondary metabolites is funded by the European Union, The German Ministry for Education and Science and the State of Saxony.

References

  1. Abrahão MRE, Molina G, Pastore GM (2013) Endophytes: recent developments in biotechnology and the potential for flavor production. Food Res Int 52:367–372CrossRefGoogle Scholar
  2. Agusta A, Maehara S, Ohashi K, Simanjuntak P, Shibuya H (2005) Stereoselective oxidation at C-4 of flavans by the endophytic fungus Diaporthe sp. isolated from a tea plant. Chem Pharm Bull 53:1565–1569PubMedCrossRefGoogle Scholar
  3. Agusta A, Wulansari D, Praptiwi Nurkanto A, Fathoni A (2014) Biotransformation of protoberberine alkaloids by the endophytic fungus Coelomycetes AFKR-3 isolated from yellow moonsheed plant (Archangelisia flava (L.) Merr.). Proced Chem 13:38–43CrossRefGoogle Scholar
  4. Aly AH, Debbab A, Proksch P (2013) Fungal endophytes—secret producers of bioactive plant metabolites. Pharmazie 68:499–505PubMedGoogle Scholar
  5. Arnold AE, Mejía LC, Kyllo D, Rojas EI, Maynard Z, Robbins N, Herre EA (2003) Fungal endophytes limit pathogen damage in a tropical tree. Proc Natl Acad Sci USA 26:15649–15654CrossRefGoogle Scholar
  6. Bertrand S, Bohni N, Schnee S, Schumpp O, Gindro K, Wolfender J-L (2014) Metabolite induction via microorganism co-culture: a potential way to enhance chemical diversity for drug discovery. Biotechnol Adv 32:1180–1204PubMedCrossRefGoogle Scholar
  7. Bicas JL, Dionisio AP, Pastore GM (2009) Bio-oxidation of terpenes: an approach for the flavor industry. Chem Rev 109:4518–4531PubMedCrossRefGoogle Scholar
  8. Borges KB, Borges WdS, Pupo MT, Bonato PS (2008) Stereoselective analysis of thioridazine-2-sulfoxide and thioridazine-5-sulfoxide: an investigation of rac- thioridazine biotransformation by some endophytic fungi. J Pharm Biomed Anal 46:945–952PubMedCrossRefGoogle Scholar
  9. Borges KB, Borges WdS, Durán-Patrón R, Pupo MT, Bonato PS, Collado IG (2009) Stereoselective biotransformations using fungi as biocatalysts. Tetrahedron Asymmetry 20:385–397CrossRefGoogle Scholar
  10. Casella TM, Eparvier V, Mandavid H, Bendelac A, Odonne G, Dayan L, Duplais C, Espindola LS, Stien D (2013) Antimicrobial and cytotoxic secondary metabolites from tropical leaf endophytes: isolation of antibacterial agent pyrrocidine C from Lewia infectoria SNB-GTC2402. Phytochemistry 96:370–377PubMedCrossRefGoogle Scholar
  11. Chandra S, Chandra R (2011) Engineering secondary metabolite production in hairy roots. Phytochem Rev 10:371–395CrossRefGoogle Scholar
  12. Cusido RM, Onrubia M, Sabater-Jara AB, Moyano E, Bonfill M, Goossens A, Pedreño MA, Palazon J (2014) A rational approach to improving the biotechnological production of taxanes in plant cell cultures of Taxus spp. Biotechnol Adv 32:1157–1167PubMedCrossRefGoogle Scholar
  13. Estrada C, Wcislo WT, Van Bael SA (2013) Symbiotic fungi alter plant chemistry that discourages leaf-cutting ants. New Phytol 198:241–251PubMedCrossRefGoogle Scholar
  14. Eyberger AL, Dondapati R, Porter JR (2006) Endophyte fungal isolates from Podophyllum peltatum produce podophyllotoxin. J Nat Prod 69:1121–1124PubMedCrossRefGoogle Scholar
  15. Gandhi SG, Mahajan V, Bedi YS (2015) Changing trends in biotechnology of secondary metabolism in medicinal and aromatic plants. Planta 241:303–317PubMedCrossRefGoogle Scholar
  16. Georgiev M, Agostini E, Ludwig-Müller J, Xu J (2012) Genetically transformed roots: from plant disease to biotechnology. Trends Biotechnol 30:528–537PubMedCrossRefGoogle Scholar
  17. Hansson D, Wubshet S, Olson Å, Karlsson M, Staerk D, Broberg A (2014) Secondary metabolite comparison of the species within the Heterobasidion annosum s.l. complex. Phytochemistry 108:243–251PubMedCrossRefGoogle Scholar
  18. Hwang K-S, Kim HU, Charusanti P, Palsson BØ, Lee SY (2014) Systems biology and biotechnology of Streptomyces species for the production of secondary metabolites. Biotechnol Adv 32:255–268PubMedCrossRefGoogle Scholar
  19. Jaber LR, Vidal S (2009) Interactions between an endophytic fungus, aphids, and extrafloral nectaries: do endophytes induce extrafloral-mediated defences in Vicia faba? Funct Ecol 23:707–714CrossRefGoogle Scholar
  20. Jäschke D, Dugassa-Gobena D, Karlovsky P, Vidal S, Ludwig-Müller J (2010) Suppression of clubroot development in Arabidopsis thaliana by the endophytic fungus Acremonium alternatum. Plant Pathol 59:100–111CrossRefGoogle Scholar
  21. Joost RE (1995) Acremonium in fescue and ryegrass: boon or bane? A review. J Anim Sci 73:881–888PubMedGoogle Scholar
  22. Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105:7100–7105PubMedCentralPubMedCrossRefGoogle Scholar
  23. Kusari S, Lamshöft M, Zühlke S, Spiteller M (2008) An endophytic fungus from Hypericum perforatum that produces hypericin. J Nat Prod 71:159–162PubMedCrossRefGoogle Scholar
  24. Kusari S, Zühlke S, Spiteller M (2009) An endophytic fungus from Camptotheca acuminata that produces camptothecin and analogues. J Nat Prod 72:2–7PubMedCrossRefGoogle Scholar
  25. Kusari S, Hertweck C, Spiteller M (2012a) Chemical ecology of endophytic fungi: origins of secondary metabolites. Chem Biol 19:792–798PubMedCrossRefGoogle Scholar
  26. Kusari S, Verma VC, Lamshoeft M, Spiteller M (2012b) An endophytic fungus from Azadirachta indica A. Juss. that produces azadirachtin. World J Microbiol Biotechnol 28:1287–1294PubMedCrossRefGoogle Scholar
  27. Kusari S, Pandey SP, Spiteller M (2013) Untapped mutualistic paradigms linking host plant and endophytic fungal production of similar bioactive secondary metabolites. Phytochemistry 91:81–87PubMedCrossRefGoogle Scholar
  28. Lahlali R, Peng G, Gossen BD, McGregor L, Yu FQ, Hynes RK, Hwang SF, McDonald MR, Boyetchko SM (2013) Evidence that the biofungicide Serenade (Bacillus subtilis) suppresses clubroot on canola via antibiosis and induced host resistance. Phytopathology 103:245–254PubMedCrossRefGoogle Scholar
  29. Lee JC, Strobel GA, Lobkovsky E, Clardy J (1996) Torreyanic acid: a selectively cytotoxic quinone dimer from the endophytic fungus Pestalotiopsis microspora. J Org Chem 61:3232–3233CrossRefGoogle Scholar
  30. Leifert C, Cassells AC (2001) Microbial hazards in plant tissue and cell cultures. In Vitro Cell Dev Biol Plant 37:133–138CrossRefGoogle Scholar
  31. Liu CH, Zou WX, Lu H, Tan RX (2001) Antifungal activity of Artemisia annua endophyte cultures against phytopathogenic fungi. J Biotechnol 88:277–282PubMedCrossRefGoogle Scholar
  32. Lu H, Zou WX, Meng JC, Hu J, Tan RX (2000) New bioactive metabolites produced by Colletotrichum sp., an endophytic fungus in Artemisia annua. Plant Sci 151:67–73CrossRefGoogle Scholar
  33. Ludwig-Müller J, Jahn L, Lippert A, Püschel J, Walter A (2014) Improvement of hairy root cultures and plants by changing biosynthetic pathways leading to pharmaceutical metabolites: strategies and applications. Biotechnol Adv 32:1168–1179PubMedCrossRefGoogle Scholar
  34. Malik S, Cusidó RM, Mirjalili MH, Moyano E, Palazón J, Bonfill M (2011) Production of the anticancer drug taxol in Taxus baccata suspension cultures: a review. Proc Biochem 46:23–34CrossRefGoogle Scholar
  35. Mohana Kumara P, Zuehlke S, Priti V, Ramesha BT, Shweta S, Ravikanth G, Vasudeva R, Santhoshkumar TR, Spiteller M, Uma Shaanker R (2012) Fusarium proliferatum, an endophytic fungus from Dysoxylum binectariferum Hook.f, produces rohitukine, a chromane alkaloid possessing anti-cancer activity. Antonie Van Leeuwenhoek 101:323–329PubMedCrossRefGoogle Scholar
  36. Narisawa K, Ohki T, Hashiba T (2000) Suppression of clubroot and Verticillium yellows in Chinese cabbage in the field by the root endophytic fungus, Heteroconium chaetospira. Plant Pathol 49:141–146CrossRefGoogle Scholar
  37. Nitzsche A, Tokalov SV, Gutzeit HO, Ludwig-Müller J (2004) Chemical and biological characterization of cinnamic acid derivatives from cell cultures of lavender (Lavandula officinalis) induced by stress and jasmonic acid. J Agric Food Chem 52:2915–2923PubMedCrossRefGoogle Scholar
  38. Onrubia M, Moyano E, Bonfill M, Cusidó RM, Goossens A, Palazón J (2011) Coronatine, a more powerful elicitor for inducing taxane biosynthesis in Taxus media cell cultures than methyl jasmonate. J Plant Physiol 170:211–219CrossRefGoogle Scholar
  39. Partida-Martinez LP, Hertweck C (2005) Pathogenic fungus harbours endosymbiotic bacteria for toxin production. Nature 437:884–888PubMedCrossRefGoogle Scholar
  40. Poling SM, Wicklow DT, Rogers KD, Gloer JB (2008) Acremonium zeae, a protective endophyte of maize produces dihydroresorcylide and 7-hydroxydihydroresorcylides. J Agric Food Chem 56:3006–3009PubMedCrossRefGoogle Scholar
  41. Prado S, Buisson D, Ndoye I, Vallet M, Nay B (2013) One-step enantioselective synthesis of (4S)-isosclerone through biotransformation of juglone by an endophytic fungus. Tetrahedron Lett 54:1189–1191CrossRefGoogle Scholar
  42. Prana TK, Srikandace J, Sumitro E, Wulandari D (2010) The potency of endophytic fungi of turmeric (Curcuma longa L.) in biotransformation of curcumic compounds in various media. Res J Microbiol 5:1189–1198CrossRefGoogle Scholar
  43. Pu X, Qu X, Chen F, Bao J, Zhang G, Luo Y (2013) Camptothecin-producing endophytic fungus Trichoderma atroviride LY357: isolation, identification, and fermentation conditions optimization for camptothecin production. Appl Microbiol Biotechnol 97:9365–9375PubMedCrossRefGoogle Scholar
  44. Puri SC, Nazir A, Chawla R, Arora R, Riyaz-ul-Hasan S, Amnaa T, Ahmeda B, Verma V, Singh S, Sagar R, Sharma A, Kumar R, Sharma RK, Qazi GN (2006) The endophytic fungus Trametes hirsuta as a novel alternative source of podophyllotoxin and related aryl tetralin lignans. J Biotechnol 122:494–510PubMedCrossRefGoogle Scholar
  45. Qawasmeh A, Obied HK, Raman A, Wheatley W (2012) Influence of fungal endophyte infection on phenolic content and antioxidant activity in grasses: interaction between Lolium perenne and different strains of Neotyphodium lolii. J Agric Food Chem 60:3381–3388PubMedCrossRefGoogle Scholar
  46. Rodriguez RJ, White JF Jr, Arnold AE, Redman RS (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330PubMedCrossRefGoogle Scholar
  47. Sakai K, Kinoshita H, Nihira T (2012) Heterologous expression system in Aspergillus oryzae for fungal biosynthetic gene clusters of secondary metabolites. Appl Microbiol Biotechnol 93:2011–2022PubMedCrossRefGoogle Scholar
  48. Saunders M, Kohn LM (2008) Host-synthesized secondary compounds influence the in vitro interactions between fungal endophytes of maize. Appl Env Microbiol 74:136–142CrossRefGoogle Scholar
  49. Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686PubMedCrossRefGoogle Scholar
  50. Schulz B, Rommert AK, Dammann U, Aust HJ, Strack D (1999) The endophyte host interaction: a balanced antagonism? Mycol Res 103:1275–1283CrossRefGoogle Scholar
  51. Schulz B, Boyle C, Draeger S, Rommert A-K, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106:996–1004CrossRefGoogle Scholar
  52. Schwarzer D, Finking R, Marahiel MA (2003) Nonribosomal peptides: from genes to products. Nat Prod Rep 20:275–287PubMedCrossRefGoogle Scholar
  53. Shibuya H, Agusta A, Ohashi K, Maehara S, Simanjuntak P (2005) Biooxidation of (+)- catechin and (−)- epicatechin into 3,4-dihydroxyflavan derivatives by the endophytic fungus Diaporthe sp. isolated from a tea plant. Chem Pharm Bull 53:866–867PubMedCrossRefGoogle Scholar
  54. Strobel GA (2003) Endophytes as sources of bioactive products. Microbes Infect 5:535–544PubMedCrossRefGoogle Scholar
  55. Strobel GA, Hess WM (1997) Glucosylation of the peptide leucinostatin A, produced by an endophytic fungus of European yew, may protect the host from leucinostatin toxicity. Chem Biol 4:529–536PubMedCrossRefGoogle Scholar
  56. Strobel G, Stierle A, Stierle D, Hess WM (1993) Taxomyces andreanae, a proposed new taxon for a bulbilliferous hyphomycete associated with Pacific yew (Taxus brevifolia). Mycotaxon 47:71–80Google Scholar
  57. Strobel G, Yang X, Sears J, Kramer R, Sidhu RS, Hess WM (1996) Taxol from Pestalotiopsis microspora, an endophytic fungus of Taxus wallachiana. Microbiol 142:435–440CrossRefGoogle Scholar
  58. Strobel GA, Li JY, Sugawara F, Koshino H, Harper J, Hess WM (1999) Oocydin A, a chlorinated macrocyclic lactone with potent antioomycete activity from Serratia marcescens. Microbiol 145:3557–3564CrossRefGoogle Scholar
  59. Suryanarayanan TS, Thirunavukkarasu N, Govindarajulu MB, Sasse F, Jansen R, Murali TS (2009) Fungal endophytes and bioprospecting. Fungal Biol Rev 23:9–19CrossRefGoogle Scholar
  60. Tan R, Zou WX (2001) Endophytes: a rich source of functional metabolites. Nat Prod Rep 18:448–459PubMedCrossRefGoogle Scholar
  61. Tian Y, Amand S, Buisson D, Kunz C, Hachette F, Dupont J, Nay B, Prado S (2014) The fungal leaf endophyte Paraconiothyrium variabile specifically metabolizes the host- plant metabolome for its own benefit. Phytochemistry 108:95–101PubMedCrossRefGoogle Scholar
  62. Trapp MA, Kai M, Mithöfer A, Rodrigues-Filho E (2015) Antibiotic oxylipins from Alternanthera brasiliana and its endophytic bacteria. Phytochemistry 110:72–82PubMedCrossRefGoogle Scholar
  63. Tuntiwachwuttikul P, Taechowisan T, Wanbanjob A, Thadaniti S, Taylor WC, Lansai A-D (2008) Secondary metabolites from Streptomyces sp. SUC1. Tetrahedron 64:7583–7586CrossRefGoogle Scholar
  64. Verma VC, Gond SK, Mishra A, Kumar A, Kharwar RN, Gange AC (2009) Endophytic actinomycetes from Azadirachta indica A. Juss.: isolation, diversity and anti-microbial activity. Microbial Ecol 57:749–756CrossRefGoogle Scholar
  65. Verma P, Khan SA, Mathur AK, Shanker K, Kalra A (2014) Fungal endophytes enhanced the growth and production kinetics of Vinca minor hairy roots and cell suspensions grown in bioreactor. Plant Cell Tiss Org Cult 118:257–268CrossRefGoogle Scholar
  66. Yu H, Zhang L, Li L, Zheng C, Guo L, Li W, Sun P, Qin L (2010) Recent developments and future prospects of antimicrobial metabolites produced by endophytes. Microbial Res 165:437–449CrossRefGoogle Scholar
  67. Zhang J, Zhang L, Wang X, Qiu D, Sun D, Gu J, Fang Q (1998) Microbial transformation of 10-deacetyl-7-epitaxol and 1β-hydroxybaccatin I by fungi from the inner bark of Taxus yunnanensis. J Nat Prod 61:497–500CrossRefGoogle Scholar
  68. Zhang P, Zhou P-P, Yu L-J (2009) An endophytic taxol-producing fungus from Taxus media, Cladosporium cladosporioides MD2. Curr Microbiol 59:227–232PubMedCrossRefGoogle Scholar
  69. Zhang XX, Li CJ, Nan ZB, Matthew C (2011) Neotyphodium endophyte increases Achnatherum inebrians (drunken horse grass) resistance to herbivores and seed predators. Weed Res 52:70–78CrossRefGoogle Scholar
  70. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333PubMedCrossRefGoogle Scholar
  71. Zikmundová M, Drandarov K, Bigler L, Hesse M, Werner C (2002) Biotransformation of 2-benzoxazolinone and 2-hydroxy-1,4-benzoxazin-3-one by endophytic fungi isolated from Aphelandra tetragona. Appl Env Microbiol 68:4863–4870CrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Institute of BotanyTechnische Universität DresdenDresdenGermany

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