Advertisement

Microbial Ecology

, 54:685 | Cite as

Volatile Terpenoids of Endophyte-free and Infected Peppermint (Mentha piperita L.): Chemical Partitioning of a Symbiosis

  • Marco MucciarelliEmail author
  • Wanda Camusso
  • Massimo Maffei
  • Paola Panicco
  • Carlo Bicchi
Article

Abstract

The study reports the effects on volatiles of an endophytic fungus inhabiting asymptomatically the leaves of peppermint. By means of headspace solid-phase microextraction (HS-SPME) and gaschromatography-mass spectrometry (GC-MS) terpenoids were sampled in time course from the head space of peppermint leaves and roots. After removal of the mycelium from peppermint tissues, fungal volatiles were analyzed and compared with those of pure fungal cultures. In the presence of the endophyte, the relative amount of all main compounds increased in leaves. Starting from the first 14 d of culture, (−)-menthone and (+)-neomenthol were consistently higher than in control plants. On the contrary, (+)-menthofuran increased only by 28 d of culture. Root volatiles were also dramatically altered by the presence of the fungus, with (+)-pulegone accounting for at least 44% of the total volatile emission. (+)-Pulegone was also the main compound of PGP-HSF mycelium isolated from peppermint roots. The sesquiterpenoid cuparene was found as a novel compound of peppermint leaf headspace and was a main volatile of ex planta and pure culture mycelia. The chemical spectrum of terpenoids and their distribution among peppermint roots, leaves, and mycelia are likely to account for a fine regulation of the mutualism in planta and for the acquisition by the fungus of novel metabolic competences.

Keywords

Arbuscular Mycorrhizal SPME Terpene Terpenoid Limonene 
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.

Notes

Aknowledgments

The authors wish to thank all the students and graduated students who gave technical support to this work. This research project was supported by a MURST 60% grant.

This article is dedicated to the memory of prof. Silvano Scannerini who first addressed our interest to the microbial communities of peppermint leaves and largely contributed to the critical revision of these results.

References

  1. 1.
    Ahmad, A, Alam, M, Janardhanan, KK (2001) Fungal endophyte enhances biomass production and essential oil yield of east Indian lemongrass. Symbiosis 30: 275–285Google Scholar
  2. 2.
    Akiyama, K, Hayashi, H (2002) Arbuscular mycorrhizal fungus-promoted accumulation of two new triterpenoids in cucumber roots. Biosci Biotechnol Biochem 66: 762–769PubMedCrossRefGoogle Scholar
  3. 3.
    Akiyama, K, Matsuzaki, K, Hayashi, H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435: 824–827PubMedCrossRefGoogle Scholar
  4. 4.
    Augusto, F, Valente, ALP (2002) Applications of solid-phase microextraction to chemical analysis of live biological samples. TrAC, Trends Anal Chem 21: 428–438CrossRefGoogle Scholar
  5. 5.
    Bauch, J, Puls, J, Klupsch, R, Vogel, C (2004) Biological and chemical characteristics of included sapwood of Juniperus virginiana L. Holzforschung 58: 74–81CrossRefGoogle Scholar
  6. 6.
    Bertea, CM, Maffei, M, Schalk, M, Karp, F, Croteau, R (2001) Demonstration that menthofuran synthase of mint (Mentha) is a cytochrome P450 monooxygenase: cloning, functional expression, and characterization of the responsible gene. Arch Biochem Biophys 390: 279–286PubMedCrossRefGoogle Scholar
  7. 7.
    Besserer, A, Puech-Pages, V, Kiefer, P, Gomez-Roldan, V, Jauneau, A, Roy, S, Portais, JC, Roux, C, Becard, G, Sejalon-Delmas, N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PloS Biol 4: 1239–1247CrossRefGoogle Scholar
  8. 8.
    Bicchi, C, Panero, OM, Pellegrino, GM, Vanni, AC (1997) Characterization of roasted coffee and coffee beverages by solid phase microextraction Gas chromatography and principal component analysis. J Agric Food Chem 45: 4680–4686CrossRefGoogle Scholar
  9. 9.
    Bicchi, C, D Amato, A, Rubiolo, P (1999) Cyclodextrin derivatives as chiral selectors for direct gas chromatographic separation of enantiomers in the essential oil, aroma and flavour fields. J Chromatogr A 843: 99–121PubMedCrossRefGoogle Scholar
  10. 10.
    Bicchi, C, Cordero, C, Iori, C, Rubiolo, P, Sandra, P (2000) Headspace sorptive extraction (HSSE) in the headspace analysis of aromatic and medicinal plants. HRC, J High Resolut Chromatogr 23: 539–546CrossRefGoogle Scholar
  11. 11.
    Bicchi, C, Iori, C, Rubiolo, P, Sandra, P (2002) Headspace sorptive extraction (HSSE), stir bar sorptive extraction (SBSE), and solid phase microextraction (SPME) applied to the analysis of roasted arabica coffee and coffee brew. J Agric Food Chem 50: 449–459PubMedCrossRefGoogle Scholar
  12. 12.
    Bicchi, C, Cordero, C, Liberto, E, Rubiolo, P, Sgorbini, B (2004) Automated head-space solid-phase dynamic extraction to analyse the volatile fraction of food matrices. J Chromatogr 1024: 217–226CrossRefGoogle Scholar
  13. 13.
    Copetta, A, Lingua, G, Berta, G (2006) Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. var. Genovese. Mychorriza 16: 485–494Google Scholar
  14. 14.
    Davis, EM, Ringer, KL, McConkey, ME, Croteau, R (2005) Monoterpene metabolism. Cloning, expression, and characterization of menthone reductases from peppermint. Plant Physiol 137: 873–881PubMedCrossRefGoogle Scholar
  15. 15.
    Demyttenaere, JCR, De Kimpe, N (2001) Biotransformation of terpenes by fungi study of the pathways involved. J Mol Catal B Enzym 11: 265–270CrossRefGoogle Scholar
  16. 16.
    Demyttenaere, JCR, Morina RM, Sandra, P (2003) Monitoring and fast detection of mycotoxin-producing fungi based on headspace solid-phase microextraction and headspace sorptive extraction of the volatile metabolites. J Chromatogr A 985: 127–135PubMedCrossRefGoogle Scholar
  17. 17.
    Demyttenaere, JCR, Vanoverschelde, J, De Kimpel, N (2004) Biotransformation of (R)-(+)- and (S)-(−)-citronellol by Aspergillus. J Chromatogr A 1027: 137–146PubMedCrossRefGoogle Scholar
  18. 18.
    Espinosa-Garcia, FJ, Langenheim, JH (1991a) Effect of some leaf essential oil phenotypes in coastal redwood on the growth of several fungi with endophytic stages. Biochem Syst Ecol 19: 629–642CrossRefGoogle Scholar
  19. 19.
    Espinosa-Garcia, FJ, Langenheim, JH (1991b) Effect of some leaf essential oil phenotypes from coastal redwood on growth of its predominant endophytic fungus, Pleuroplaconema sp. J Chem Ecol 17: 1837–1857CrossRefGoogle Scholar
  20. 20.
    Fiedler, K, Schütz, E, Geh, S (2001) Detection of microbial organic compounds (MVOCs) produced by moulds on various materials. Int J Hyg Environ Health 201: 111–121CrossRefGoogle Scholar
  21. 21.
    Gatenby, WA, Munday-Finch, SC, Wilkins, AL, Miles, CO (1999) Terpendole M, a novel indole-diterpenoid isolated from Lolium perenne infected with the endophytic fungus Neotyphodium lolii. J Agric Food Chem 47: 1092–1097PubMedCrossRefGoogle Scholar
  22. 22.
    Giamperi, L, Fraternale, D, Ricci, D (2002) The in vitro action of essential oils on different organisms. J Essent Oil Res 14: 312–318Google Scholar
  23. 23.
    Gupta, ML, Prasad, A, Ram, M, Kumar, S (2002) Effect of the vesicular-arbuscular mycorrhizal (VAM) fungus Glomus fasciculatum on the essential oil yield related characters and nutrient acquisition in the crops of different cultivars of menthol mint (Mentha arvensis) under field conditions. Bioresour Technol 81: 77–79PubMedCrossRefGoogle Scholar
  24. 24.
    Hans, J, Hause, B, Strack, D, Walter, MH (2004) Cloning, characterization, and immunolocalization of a mycorrhiza-inducible 1-deoxy-d-xylulose 5-phosphate reductoisomerase in arbuscule-containing cells of maize. Plant Physiol 134: 614–624PubMedCrossRefGoogle Scholar
  25. 25.
    Harborne, JB (1991) Recent advances in the ecological chemistry of plant terpenoids. In: Harborne, JB, Tomas-Barberan, FA (Eds.) Ecological Chemistry and Biochemistry of Plant Terpenoids, Clarendon Press, Oxford, pp 399–426Google Scholar
  26. 26.
    Ishikawa, NK, Yamaji, K, Tahara, S, Fukushi, Y, Takahashi, K (2000) Highly oxidized cuparene-type sesquiterpenes from a mycelial culture of Flammulina velutipes. Phytochemistry 54: 777–782PubMedCrossRefGoogle Scholar
  27. 27.
    Ishikawa, NK, Fukushi, Y, Yamaji, K, Tahara, S, Takahashi, K (2001) Antimicrobial cuparene-type sesquiterpenes, enokipodins C and D, from a mycelial culture of Flammulina velutipes. J Nat Products 64: 932–934CrossRefGoogle Scholar
  28. 28.
    Ismailialaoui, M, Benjilali, B, Buisson, D, Azerad, R (1992) Biotransformation of terpenic compounds by fungi. 1. Metabolism of R-(+)-pulegone. Tetrahedron Lett 33: 2349–2352CrossRefGoogle Scholar
  29. 29.
    Jurc, D, Bojovic, S, Jurc, M (1999) Influence of endogenous terpenes on growth of three endophytic fungi from the needles of Pinus nigra Arnold. Phyton Ann Rei Bot 39: 225–229Google Scholar
  30. 30.
    Kapoor, R, Giri, B, Mukerji, KG (2002a) Mycorrhization of coriander (Coriandrum sativum L) to enhance the concentration and quality of essential oil. J Sci Food Agric 82: 339–342CrossRefGoogle Scholar
  31. 31.
    Kapoor, R, Giri, B, Mukerji, KG (2002b) Glomus macrocarpum: a potential bioinoculant to improve essential oil quality and concentration in Dill (Anethum graveolens L.) and Carum (Trachyspermum ammi Linn.) Sprague. World J Microbiol Biotechnol 18: 459–463CrossRefGoogle Scholar
  32. 32.
    Langenheim, JH (1994) Higher plant terpenoids—a phytocentric overview of their ecological roles. J Chem Ecol 20: 1223–1280CrossRefGoogle Scholar
  33. 33.
    Madyastha, KM, Thulasiram, HV (1999) Transformation of a monoterpene ketone, (R)-(+)-pulegone, a potent hepatotoxin, in Mucor piriformis. J Agric Food Chem 47: 1203–1207PubMedCrossRefGoogle Scholar
  34. 34.
    Maffei, M (1990) Plasticity and genotypic variation in some Mentha x verticillata hybrids. Biochem Syst Ecol 18: 493–502CrossRefGoogle Scholar
  35. 35.
    Maffei, M, Mucciarelli, M, Scannerini, S (1994) Are leaf area index (LAI) and flowering related to oil productivity in peppermint? Flavour Fragr J 9: 119–124CrossRefGoogle Scholar
  36. 36.
    Maffei, M, Scannerini, S (2000) UV-B effect on photomorphogenesis and essential oil composition in peppermint (Mentha piperita L.). J Essent Oil Res 12: 523–529Google Scholar
  37. 37.
    Maffei, M, Camusso, W, Sacco, S (2001) Effect of Mentha x piperita essential oil and monoterpenes on cucumber root membrane potential. Phytochemistry 58: 703–707PubMedCrossRefGoogle Scholar
  38. 38.
    Mahmoud, SS, Croteau, RB (2003) Menthofuran regulates essential oil biosynthesis in peppermint by controlling a downstream monoterpene reductase. Proc Natl Acad Sci USA 100: 14481–14486PubMedCrossRefGoogle Scholar
  39. 39.
    Maier, W, Hammer, K, Dammann, U, Schulz, B, Strack, D (1997) Accumulation of sesquiterpenoid cyclohexenone derivatives induced by an arbuscular mycorrhizal fungus in members of the Poaceae. Planta 202: 36–42CrossRefGoogle Scholar
  40. 40.
    McGarvey, DJ, Croteau, R (1995) Terpenoid metabolism. Plant Cell 7: 1015–1026PubMedCrossRefGoogle Scholar
  41. 41.
    Miyazawa, M, Kawazoe, H, Hyakumachi, M (2002) Biotransformation of l-menthol by soil-borne plant pathogenic fungi (Rhizoctonia solani). J Chem Technol Biotechnol 77: 21–24CrossRefGoogle Scholar
  42. 42.
    Mucciarelli, M, Camusso, W, Bertea, CM, Bossi, S, Maffei, M (2001) Effect of (+)-pulegone and other oil components of Mentha x piperita on cucumber respiration. Phytochemistry 57: 91–98PubMedCrossRefGoogle Scholar
  43. 43.
    Mucciarelli, M, Scannerini, S, Bertea, CM, Maffei, M (2002) An ascomycetous endophyte isolated from Mentha piperita L.: biological features and molecular studies. Mycologia 94: 28–39CrossRefGoogle Scholar
  44. 44.
    Mucciarelli, M, Scannerini, S, Bertea, CM, Maffei, M (2003) In vitro and in vivo peppermint (Mentha piperita) growth promotion by nonmycorrhizal fungal colonization. New Phytol 158: 579–591CrossRefGoogle Scholar
  45. 45.
    Murashige, T, Skoog, F (1962) A revised medium for rapid growth and byoassays with tobacco tissue cultures. Physiol Plant 15: 473–497CrossRefGoogle Scholar
  46. 46.
    Nabeta, K, Kawakita, K, Yada, Y, Okuyama, H (1993) Biosynthesis of sesquiterpenes from deuterated mevalonates in Perilla callus. Biosci Biotechnol Biochem 57: 792–798CrossRefGoogle Scholar
  47. 47.
    Napierala-Filipiak, A, Werner, A, Mardarowicz, M, Gawdzik, J (2002) The effects of heavy metals, content of nutrients and inoculation with mycorrhizal fungi on the level of terpenoids in roots of Pinus sylvestris seedlings. Acta Physiol Plant 24: 137–143CrossRefGoogle Scholar
  48. 48.
    Oumzil, H, Ghoulami, S, Rhajaoui, M, Ilidrissi, A, Fkih-Tetouani, S, Faid, M, Benjouad, A (2002) Antibacterial and antifungal activity of essential oils of Mentha suaveolens. Phytotherapy Res 16: 727–731CrossRefGoogle Scholar
  49. 49.
    Packiyasothy, EV, Kyle, S (2002) Antimicrobial properties of some herb essential oils. Food Aust 54: 384–387Google Scholar
  50. 50.
    Pandey, RR, Arora, DK, Dubey, RC (1993) Antagonistic interactions between fungal pathogens and phylloplane fungi of guava. Mycopathologia 124: 31–39CrossRefGoogle Scholar
  51. 51.
    Pichersky, E, Gershenzon, J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5: 237–243PubMedCrossRefGoogle Scholar
  52. 52.
    Raffa, KF, Smalley, EB (1995) Interaction of pre-attack and induced monoterpene concentrations in host conifer defense against bark beetle fungal complexes. Oecologia 102: 285–295CrossRefGoogle Scholar
  53. 53.
    Riu-Aumatell, M, Castellari, M, Lopez-Tamames, E, Galassi, S, Buxaderas, S (2004) Characterisation of volatile compounds of fruit juices and nectars by HS/SPME and GUMS. Food Chem 87: 627–637CrossRefGoogle Scholar
  54. 54.
    Sassa, T, Kenmoku, H, Sato, M, Murayama, T, Kato, N (2003) (+)-Menthol and its hydroxy derivatives, novel fungal monoterpenols from the fusicoccin-producing fungi, Phomopsis amygdali F6A and Niigata 2. Biosci Biotechnol Biochem 67: 475–479PubMedCrossRefGoogle Scholar
  55. 55.
    Sati, S, Mathela, CS (2005) Essential oil composition of Valeriana hardwickii var. arnottiana from the Himalayas. Flavour Fragr J 20: 299–301CrossRefGoogle Scholar
  56. 56.
    Scannerini, S, Fusconi, A, Mucciarelli, M (2001) The effect of endophytic fungi on host plant morphogenesis. In: Seckbach, J (Ed.) Symbiosis, Cellular Origin and Life in Extreme Habitats, Kluwer Academic Publishers, Dordrecht, pp 427–447Google Scholar
  57. 57.
    Schardl, CL (1996) Interactions of grasses with endophytic Epichloë species and hybrids. In: Stacey, G, Keen, NT (Eds.) Plant Microbe Interactions, Chapman Hall, New York, pp 107–140Google Scholar
  58. 58.
    Schulz, B, Rommert, AK, Dammann, U, Aust, HJ, Strack, D (1999) The endophyte–host interaction: a balanced antagonism? Mycol Res 103: 1275–1283CrossRefGoogle Scholar
  59. 59.
    Schulz, B, Boyle, C, Draeger, S, Rommert, AK, Krohn, K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106: 996–1004CrossRefGoogle Scholar
  60. 60.
    Stinson, M, Ezra, D, Hess, WM, Sears, J, Strobel, G (2003) An endophytic Gliocladium sp. of Eucryphia cordifolia producing selective volatile antimicrobial compounds. Plant Sci 165: 913–922CrossRefGoogle Scholar
  61. 61.
    Strobel, GA, Dirkse, E, Sears, J, Markworth, C (2001) Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiology 7: 2943–2950Google Scholar
  62. 62.
    Takahashi, H, Noma, Y, Toyota, M, Asakawa, Y (1994) Biotransformation of (−)- and (+)-neomenthols and isomenthol by Aspergillus niger. Phytochemistry 35: 1465–1467CrossRefGoogle Scholar
  63. 63.
    Tamasloukht, M, Sejalon-Delmas, N, Kluever, A, Jauneau, A, Roux, C, Becard, G, Franken, P (2003) Root factors induce mitochondrial-related gene expression and fungal respiration during the developmental switch from asymbiosis to presymbiosis in the arbuscular mycorrhizal fungus Gigaspora rosea. Plant Physiol 131: 1468–1478PubMedCrossRefGoogle Scholar
  64. 64.
    Toyota, M, Koyama, H, Asakawa, Y (1997) Sesquiterpenoids from the three Japanese liverworts Lejeunea aquatica, L. flava and L. japonica. Phytochemistry 46: 145–150CrossRefGoogle Scholar
  65. 65.
    van Dyk, MS, van Rensburg, E, Rensburg, IPB, Moleleki, N (1998) Biotransformation of monoterpenoid ketones by yeasts and yeast-like fungi. J Mol Catal B Enzym 5: 149–154CrossRefGoogle Scholar
  66. 66.
    Viiri, H, Annila, E, Kitunen, V, Niemela, P (2001) Induced responses in stilbenes and terpenes in fertilized Norway spruce after inoculation with blue-stain fungus, Ceratocystis polonica. Trees 15: 112–122CrossRefGoogle Scholar
  67. 67.
    Werner, A, Napierala-Filipiak, A, Mardarowicz, M, Gawdzik, J (2004) The effect of two substrates differing in the amount of toxic metals and nutrients on the content of volatile organic compounds in roots of Pinus sylvestris. Acta Physiol Plant 26: 187–196CrossRefGoogle Scholar
  68. 68.
    Yue, Q, Miller, CJ, White, JF Jr, Richardson, MD (2000) Isolation and characterization of fungal inhibitors from Epichloë festucae. J Agric Food Chem 48: 4687–4962PubMedCrossRefGoogle Scholar
  69. 69.
    Yue, Q, Wang, C, Gianfagna, TJ, Meyer, WA (2001) Volatile compounds of endophyte-free and infected tall fescue (Festuca arundinacea Schreb.). Phytochemistry 58: 935–941PubMedCrossRefGoogle Scholar
  70. 70.
    Zhang, Z, Pawliszyn, J (1993) Headspace solid-phase microextraction. Anal Chem 65: 1843–1852CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Marco Mucciarelli
    • 1
    Email author
  • Wanda Camusso
    • 1
  • Massimo Maffei
    • 2
  • Paola Panicco
    • 3
  • Carlo Bicchi
    • 3
  1. 1.Department of Veterinary MorphophysiologyUniversity of TorinoGrugliascoItaly
  2. 2.Department of Plant Biology and Centre of Excellence—CebiovemUniversity of TorinoTurinItaly
  3. 3.Dipartimento di Scienza e Tecnologia del FarmacoUniversità di TorinoTurinItaly

Personalised recommendations