Secondary Metabolites in Soil Ecology pp 141-165

Part of the Soil Biology book series (SOILBIOL, volume 14) | Cite as

Biological Significance of Truffle Secondary Metabolites

  • Richard Splivallo

Fungal primary and secondary metabolites have an important impact on our society. Best known as mycotoxins, phytotoxins, antibiotics and natural aromas; they represent industries worth billions of dollars. Fungi are also of major importance in terms of biomass: they rank first with an estimated dry weight of 450 kg/ha, which represents 91% of the total soil biomass (microflora and microfauna) (Müller and Loeffler 1976). Yet our knowledge of the ecological significance of fungal metabolites is limited. Despite the pioneer work of Dick and Hutchinson (1966) and Hutchinson (1973) on the effect of volatile fungal metabolites on fungi and plants, this argument seems to have raised little interest in the scientific community. Since then, most studies have focused on parasitic interactions with plants (phytopathogens), while much less attention has been given to the ecological role of the metabolites of symbiotic fungi. An important group of the latter is represented by mycorrhizal fungi. Mycorrhizas are one of the oldest associations between plants and fungi. Dating back to the early colonization of the terrestrial environment (Brundrett 2002), they are classified as endomycorrhizas (arbuscular, ericoid, orchid mycorrhizas) or ectomycorrhizas depending on their ability to penetrate the host-plant root. Truffles fall in the last category of the ectomycorrhizal fungi. Best known for the complex aroma of their hypogeous fruitbodies, truffles were already known to the Greeks and the Romans, but only reached their luxury standing in the last 20 years owing to decreasing production (Fauconnet and Delher 1998; Hall and Yun 2001) and an ever-increasing demand. Despite their high commercial value, very little is known about their biology. Indeed, the unique features of mycorrhizal fungi, from their formation to signal exchange with the surrounding environment (the rhizosphere), are still poorly understood. In addition to the compounds involved in nutritional exchanges between the host plant and the fungus, various micromolecules and macromolecules are secreted into the rhizosphere. These exudates and volatile organic compounds (VOCs) play an active role in the regulation of symbiosis and interactions with other organisms, including nonhost plants.

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References

  1. Abraham BG, Berger RG (1994) Higher fungi for generating aroma components through novel biotechnologies. J Agric Food Chem 42:2344–2348CrossRefGoogle Scholar
  2. Aharoni A, Giri AP, Verstappen FWA, Bertea CM, Sevenier R, Zhongkui S, Jongsma MA, Schwab W, Bouwmeestera HJ (2004) Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell 16:3110–3131PubMedCrossRefGoogle Scholar
  3. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefGoogle Scholar
  4. Amaranthus M, Luoma D, Eberhart JL, Trappe JM (1999). Truffle dominance and diversity in natural vegetative communities. In: Actes du Vème congrès international, science et culture de la truffe. Fédération Française des Trufficulteurs, Aix-en-Provence, pp 4.183–4.187Google Scholar
  5. Arfi K, Tâche R, Spinnler HE, Bonnarme P (2003) Dual influence of the carbon source and L-methionine on the synthesis of sulfur compounds in the cheese-ripening yeast Geotrichum candidum. Appl Microbiol Biotechnol 61:359–365PubMedGoogle Scholar
  6. Assaf S, Hadar Y, Dosoretz CG (1997) 1-Octen-3-ol and 13-hydroperoxylinoleate are products of distinct pathways in the oxidative breakdown of linoleic acid by Pleurotus pulmonarius. Enzyme Microb Technol 21:484–490CrossRefGoogle Scholar
  7. Barbieri E, Bertini L, Rossi I, Ceccaroli P, Saltarelli R, Guidi C, Zambonelli A, Stocchi V (2005) New evidence for bacterial diversity in the ascoma of the ectomycorrhizal fungus Tuber borchii Vittad. FEMS Microbiol Lett 247:23–35PubMedCrossRefGoogle Scholar
  8. Barney JN, Hay AG, Weston LA (2005) Isolation and characterization of allelopathic volatiles from mugwort (Artemisia vulgaris). J Chem Ecol 31(2):247–265PubMedCrossRefGoogle Scholar
  9. Barry D, Staunton S, Callot G (1994) Mode of absorption of water and nutrients by ascocarps of Tuber melanosporum and Tuber aestivum: a radioactive tracer technique. Can J Bot 72:317–322CrossRefGoogle Scholar
  10. Bellesia F, Pinetti A, Bianchi A, Tirillini B (1996) I composti solforati dell’aroma del tartufo: loro evoluzione durante la conzervatione. Atti Soc Nat Mat Modena 127:177–187Google Scholar
  11. Bellesia F, Pinetti A, Bianchi A, Tirillini B (1998a) The volatile organic compounds of black truffle (Tuber melanosporum Vitt.) from middle Italy. Flavour Fragr J 13:56–58.CrossRefGoogle Scholar
  12. Bellesia F, Pinetti A, Bianchi A, Tirillini B (1998b) Volatile compounds of white truffle (Tuber magnatum Pico.) from middle Italy. Flavour Fragr J 11:239–243CrossRefGoogle Scholar
  13. Bellesia F, Pinetti A, Tirillini B, Bianchi A (2001) Temperature-dependant evolution of volatiles organic compounds in Tuber borchii from Italy. Flavour Fragr J 16:1–6CrossRefGoogle Scholar
  14. Bellesia F, Pinetti A, Tirillini B, Paolocci F, Rubina A. Arcioni S, Bianchi A (2002) The headspace volatiles of the Asian truffle Tuber indicum Cooke et Mass. J Essent Oil Res 14:3–5Google Scholar
  15. Bending GD, Lincoln SD (1999) Characterization of volatile sulphur-containing compounds produced during decomposition of Brassica juncea tissues in soil. Soil Biol Biochem 31:695–703CrossRefGoogle Scholar
  16. Berger C, Khan JA, Molimard P, Martin N, Spinnler HE (1999) Production of sulfur flavors by ten strains of Geotrichum candidum. Appl Environ Microbiol 65:5510–5514PubMedGoogle Scholar
  17. Bidartondo MI, Burghardt B, Gebauer G, Bruns TD, Read DJ (2004) Changing partners in the dark: isotopic and molecular evidence of ectomycorrhizal liaisons between forest orchids and trees. Proc R Soc Lond Ser B 271:1799–1806CrossRefGoogle Scholar
  18. Bode HB, Bethe B, Hofs R, Zeeck A (2002) Big effects from small changes: possible ways to explore nature’s chemical diversity. Chembiochem 3:619–627PubMedCrossRefGoogle Scholar
  19. Bonnarme P, Arfi K, Dury C, Helinck S, Yvon M, Spinnler HE (2001a) Sulfur compounds production by Geotrichum candidum from L-methionine: importance of the transaminase step. FEMS Microbiol Lett 205:247–252PubMedGoogle Scholar
  20. Bonnarme P, Lapadatescu C, Yvon M, Spinnler HE (2001b) L-Methionine: degradation potentiality of cheese-ripening microorganisms. J Dairy Res 68:663–674PubMedCrossRefGoogle Scholar
  21. Borowicz VA (2001) Do arbuscular mycorrhizal fungi alter plant-pathogen relations? Ecology 82(11):3057–3068Google Scholar
  22. Bratek Z, Albert L, Gagi I, Pálfy B, Takács T, Rudnóy S, Alász K (1999) New and rare hypogenus fungi of Carpathian Basin. In: Actes du Vème congrès international, science et culture de la truffe. Fédération Française des Trufficulteurs, Aix-en-Provence, pp 2.55–2.56Google Scholar
  23. Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytol 154(2):275–304CrossRefGoogle Scholar
  24. Buscot F, Munch JC, Charcosset JY, Gardes M, Nehls U, Hampp R (2000) Recent advances in exploring physiology and biodiversity of ectomycorrhizas highlight the functioning of these symbioses in the ecosystem. FEMS Microbiol Rev 24:601–614PubMedCrossRefGoogle Scholar
  25. Buzzini P, Gasparetti C, Turchetti B, Cramarossa MR, Vaughan-Martini A, Martini A, Pagnoni UM, Forti L (2005) Production of volatile organic compounds (VOCs) by yeasts isolated from the ascocarps of black (Tuber melanosporum Vitt.) and white (Tuber magnatum Pico) truffles. Arch Microbiol 184:187–193PubMedCrossRefGoogle Scholar
  26. Ceccaroli P, Saltarelli R, Cesari P, Zambonelli A, Stocchi V (2001) Effects of different carbohydrates sources on the growth of Tuber borchii Vitta. Mycelium strains in pure culture. Mol Cell Biochem 218:65–70PubMedCrossRefGoogle Scholar
  27. Ceruti A, Fontana A, Nosenzo C (2003) Le specie europee del genere Tuber. Una revisione storica. Monografie XXXVII. Museo Regionale di Scienze Naturali, TurinGoogle Scholar
  28. Chiron N, Michelot D (2005) Mushrooms odors, chemistry and role in the biotic interactions–a review (in French). Cryptogam Mycol 26(4):299–364Google Scholar
  29. Chitarra GS, Abee T, Rombouts FM, Posthumus MA, Dijksterhuis J (2004) Germination of Penicillium paneum conidia is regulated by 1-octen-3-ol, a volatile self-inhibitor. Appl Environ Microbiol 70:2823–2829PubMedCrossRefGoogle Scholar
  30. Ciccarello A (1564) Opusculum de tuberibus. PaduaGoogle Scholar
  31. Claus R, Hoppe HO, Karg H (1981) The secret of truffle: a steroidal pheromone? Experientia 37:1178–1179CrossRefGoogle Scholar
  32. Combet E, Henderson J, Eastwood DC, Burton KS (2006) Eight-carbon volatiles in mushrooms and fungi: properties, analysis, and biosynthesis. Mycoscience 47:317–326CrossRefGoogle Scholar
  33. De Angelis F, Arcadi A, Marinelli F, Paci M, Botti D, Pacioni G, Miranda M (1996) Partial structures of truffle melanins. Phytochemistry 43(5):1103–1106CrossRefGoogle Scholar
  34. Delmas J (1983) La truffe et sa culture, 2nd edn. INRA, ParisGoogle Scholar
  35. Dénarié J, Cullimore J (1993) Lipo-oligosaccharide nudulation factors: a new class of signalling molecules mediating recognition and morphogenesis. Cell 74:951–954PubMedCrossRefGoogle Scholar
  36. Diaz P, Ibanez E, Senorans FJ, Reglero G (2003) Truffle aroma characterization by headspace solid-phase microextarction. J Chromatogr A 1017:207–214PubMedCrossRefGoogle Scholar
  37. Dick CM, Hutchinson SA (1966) Biological activity of volatile fungal metabolites. Nature 211:868PubMedCrossRefGoogle Scholar
  38. Douet JP, Castroviejo M, Mabru D, Chevalier G, Dupre C, Bergougnoux F, Ricard JM, Medina B (2004) Rapid molecular typing of Tuber melanosporum, T. brumale and T. indicum for tree seedlings and canned truffles. Anal Bioanal Chem 379(4):668–673PubMedCrossRefGoogle Scholar
  39. Falasconi M, Pardo M, Sberveglieri G, Battistutta F, Piloni M, Zironi R (2005) Study of white truffle aging with SPME-GC-MS and the Pico2-electronic nose. Sens Actuators B 106:88–94CrossRefGoogle Scholar
  40. Fasolo-Bonfante P, Fontana A, Montacchini F (1971) Studi sull’ecologia del Tuber melanosporum. Domonstrazione di un effetto fitotossico. Allionia 17:47–54Google Scholar
  41. Fassi B, Fontana A (1969) Sintesi micorrhizica tra Pinus strobus e Tuber maculatum. Allionia 15:115–120Google Scholar
  42. Fauconnet C, Delher G (1998) Influence des facteurs climatiques sur la production des truffes en Quercy. Trufficult Fr 24(3):19–21Google Scholar
  43. Fitter AH (1991) Costs and benefits of mycorrhizas—implications for functioning under natural conditions. Experientia 47:350–354CrossRefGoogle Scholar
  44. Flament I, Chevalier G, Debonneville C (1990) Analysis of the volatile flavor constituents of Périgord black truffle (Tuber melanosporum Vitt.). Riv Ital EPPOS 9:280–299Google Scholar
  45. Francis R, Read DJ (1995) Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to impacts on plant community structure. Can J Bot 73:S1301–S1309CrossRefGoogle Scholar
  46. Gallet C, Pellissier F (1997) Phenolic compounds in natural solutions of a coniferous forest. J Chem Ecol. 23(10):2401–2412CrossRefGoogle Scholar
  47. Gandeboeuf D (1997) Caractérisation et identification moléculaire de différentes espèces de genre Tuber. PhD thesis, Université Blaise Pascal, Clermont-FerrandGoogle Scholar
  48. Gioacchini AM, Menotta M, Polidori E, Giomaro G, Stocchi V (2002) Solid-phase microextraction gas chromatography/ion trap mass spectrometry and multistage mass spectrometry experiments in the characterization of germacrene D. J Mass Spectrom 37:1229–1235PubMedCrossRefGoogle Scholar
  49. Giomaro G, Sisti D, Zambonelli A, Amicucci A, Cecchini M, Comandini O, Stocchi V (2002) Comparative study and molecular characterization of ectomycorrhizas in Tilia americana and Quercus pubescens with Tuber brumale. FEMS Microbiol Lett 216(1):9–14PubMedCrossRefGoogle Scholar
  50. Girlanda M, Selosse MA, Cafasso D, Brilli F, Delfine S, Fabbian R, Ghignone S, Pinelli P, Segreto R, Loreto F, Cozzolino S, Perotto S (2006) Inefficient photosythesis in the mediterrean orchid Limodorum abortivum is mirrored by specific association to ectomycorrhizal Russulaceae. Mol Ecol 15(2):491–504PubMedCrossRefGoogle Scholar
  51. Guidi C, Zeppa S, Annibalini G, Pierleoni R, Guescini M, Buffalini M, Zambonelli A, Stocchi V (2006) The isoprenoid pathway in the ectomycorrhizal fungus Tuber borchii Vittad.: cloning and characterization of the tbhmgr, tbfpps and tbsqs genes. Curr Genet 50:393–404PubMedCrossRefGoogle Scholar
  52. Hall I, Yun W (2001) Truffles and other edible mycorrhizal mushrooms—some new crops for the Southern Hemisphere. In: Hall I, Yun W, Danell E, Zambonelli A (eds) Edible mycorrhizal mushrooms and their cultivation. Proceedings of the 2nd international conference on edible mycorrhizal mushrooms, New Zealand, pp 1–7Google Scholar
  53. Harley FRSJL, Smith SE (1983) Mycorrhizal symbiosis. Academic. LondonGoogle Scholar
  54. Harrison MJ (2005) Signaling in the arbuscular mycorrhizal symbiosis. Annu Rev Microbiol 59:19–42PubMedCrossRefGoogle Scholar
  55. Heidstra R, Bisseling T (1996) Nod factor induced hosts responses and mechanisms of Nod factor perception. New Phytol 133:25–43CrossRefGoogle Scholar
  56. Hibbett DS, Gilbert LB, Donoghue MJ (2000) Evolutionary instability of ectomycorrhizal symbioses in basidiomycetes. Nature 407:506–510PubMedCrossRefGoogle Scholar
  57. Hutchinson SA (1973) Biological activities of volatile fungal metabolites. Annu Rev Phytopathol 11:223–246CrossRefGoogle Scholar
  58. Ingvarsdóttir A, Birkett MA, Duce I, Genna RL, Mordue W, Pickett JA, Wadhams LJ, Mordue LAJ (2002) Semiochemical strategies for sea louse control: host location cues. Pest Manag Sci 58:537–545PubMedCrossRefGoogle Scholar
  59. Iotti M, Amicucci A, Stocchi V, Zambonelli A (2002) Morphological and molecular characterization of mycelia of some Tuber species in pure culture. New Phytol 155:499–505CrossRefGoogle Scholar
  60. Jin-Ming G, Wei-Ming Z, She-Qi Z, Xing Z, An-Ling Z, Hui C, Yue-Ying S, Ming T (2004) Sphingolipids from the edible fungus Tuber indicum. Eur J Lipid Sci Technol 106:815–821CrossRefGoogle Scholar
  61. Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2005) Volatile C6-aldehyde and allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol 46(7):1093–1102PubMedCrossRefGoogle Scholar
  62. Lanfranco L, Arlorio M, Matteucci A, Bonfante (1995) Truffles: their life cycle and molecular characterization. In: Stocchi V, Bonfante P, Nuti M (eds) Biotechnology of ectomycorrhizae. Molecular approaches. Plenum, New York, pp 139–150Google Scholar
  63. Lanza B, Owezarek M, De Marco A, Raglione M (2004) Evaluation of phytotoxicity and genotoxicity of substances produced by Tuber asetivum and distributed in the soil using Vicia faba root micronucleus test. Fresenius Environ Bull 13:1410–1414Google Scholar
  64. LePage BA, Currah RS, Stockey RA, Rothwell GW (1997) Fossil ectomycorrhizae from the middle Eocene. Am J Bot 84:410–412CrossRefGoogle Scholar
  65. Luppi Mosca AM, Fontana A (1977) Studi sull’ecologia del Tuber melanosporum. Analisi micologiche di terreni tartufieri dell’italia centrale. Allionia 22:105–113Google Scholar
  66. Mamoun M, Olivier JM (1997) Mycorrhizal inoculation of cloned hazels by Tuber melanosporum: effect of soil disinfestation and co-culture with Festuca ovina. Plant Soil 188:221–226CrossRefGoogle Scholar
  67. Mannina L, Cristinzio M, Sobolev AP, Ragni P, Serge A (2004) High-field nuclear magnetic resonance (NMR) study of truffles (Tuber aestivum vittadini). J Agric Food Chem 52:7988–7996PubMedCrossRefGoogle Scholar
  68. Martin F, Dupleissis S, Ditengou F, Lagrange H, Voiblet C, Lapeyrie F (2001) Developmental cross talking in the ectomycorrhizal symbiosis: signals and communication genes. New Phytol 151:145–154CrossRefGoogle Scholar
  69. Mauriello G, Marino R, D’Auria M, Cerone G, Rana GL (2004) Determination of volatile organic compounds from truffles via SPME-GC-MS. J Chromatogr Sci 42:299–305PubMedGoogle Scholar
  70. Menotta M, Gioacchini AM, Amicucci A, Buffalini M, Sisti D, Stocchi V (2004a) Headspace solid-phase microextraction with gas chromatography and mass spectrometry in the investigation of volatile organic compounds in an ectomycorrhizae synthesis system. Rapid Commun Mass Spectrom 18:206–210PubMedCrossRefGoogle Scholar
  71. Menotta M, Amicucci A, Sisti D, Gioacchini AM, Stocchi V (2004b) Differential gene expression during pre-symbiotic interaction between Tuber borchii Vittad. and Tilia Americana L. Curr Genet 46:158–165PubMedCrossRefGoogle Scholar
  72. Meruva NK, Penn JM, Farthing DE (2004) Rapid identification of microbial VOCs from tobacco molds using closed-loop stripping and gas chromatography/time-of-flight mass spectrometry. J Ind Microbiol Biotechnol 31482–488Google Scholar
  73. Miozzi L, Balestrini R, Bolchi A, Novero M, Ottonello S, Bonfante P (2005) Phospholipase A(2) up-regulation during mycorrhiza formation in Tuber borchii. New Phytol 167(1):229–238PubMedCrossRefGoogle Scholar
  74. Montacchini F, Caramiello Lomango R (1977) Studi sull’ecologia del Tuber melanosporum. Azione inibitrice su specie erbacee della flora spontanea. Allionia 22:81–85Google Scholar
  75. Müller E, Loeffler W (1976) Mycology. An outline for science and medical students. Translated by B Kendrick and F Bärlocher. Thieme, Stuttgart, p 15Google Scholar
  76. Murat C, Diez J, Luis P, Delaruelle C, Dupre C, Chevalier G, Bonfante P, Martin F (2004) Polymorphism at the ribosomal DNA ITS and its relation to postglacial re-colonization routes of the Perigord truffle Tuber melanosporum. New Phytol 164:401–411CrossRefGoogle Scholar
  77. Murat C, Vizzini A, Bonfante P, Mello A (2005) Morphological and molecular typing of the below-ground fungal community in a natural Tuber magnatum truffle-ground. FEMS Microbiol Lett 245(2):307–313PubMedCrossRefGoogle Scholar
  78. Ney KH, Freytag WG (1980) Trüffel-aroma. Gordian 9:214Google Scholar
  79. O’Donnell K, Cigelnik E, Weber NS, Trappe JM (1997) Philogenetic relationships among ascomycetous truffles and the true and false morels inferred from 18S and 28S ribosomal DNA sequence analysis. Mycologia 89(1):48–65CrossRefGoogle Scholar
  80. Papa G (1978–1979) Studi sull’ecologial del Tuber melanosporum. Analisi spettrofotometriche di estratti di terreni tartufigeni ed azione inibente la germinazione. Allionia 23:95–102Google Scholar
  81. Papa G (1980) Purification attempts of the plant inhibitory principle of Tuber melanosporum Vitt Phytopathol Mediterr 19:177Google Scholar
  82. Pacioni G (1991) Effects of Tuber metabolites on the rhizospheric environment. Mycol Res 95:1355–1358CrossRefGoogle Scholar
  83. Paolocci F, Rubini A, Riccioni C, Arcioni S (2006) Reevaluation of the life cycle of Tuber magnatum. Appl Environ Microbiol 72:2390–2393PubMedCrossRefGoogle Scholar
  84. Pelusio F, Nillsson T, Montanarella L, Tilio R, Larsen B, Facchetti S, Madsen JØ (1995) Headspace solid-phase microextraction analysis of volatile organic sulfur compounds in black and white truffle aroma. J Agric Food Chem 34:2138–2143CrossRefGoogle Scholar
  85. Plattner I, Hall IR (1995) Parasitism of non-host plants by the mycorrhizal fungus Tuber melanosporum. Mycol Res 99(11):1367–1370CrossRefGoogle Scholar
  86. Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–390CrossRefGoogle Scholar
  87. Saltarelli R, Ceccaroli P, Vallorani L, Zambonelli A, Citterio B, Malatesta M, Stocchi V (1998) Biochemical and morphological modifications during the growth of Tuber borchii mycelium. Mycol Res 102(4):403–409CrossRefGoogle Scholar
  88. Schulz B, Boyle C, Draeger S, Rommert AK, Krohn K (2002) Endophytic fungi: a source of novel biologically active secondary metabolites. Mycol Res 106(9): 996–1004CrossRefGoogle Scholar
  89. Schnitzler I, Boland W, Hay ME (1998) Organic sulfur compounds from Dictyopteris spp. deter feeding by an herbivorous amphipod (Ampithoe longimana) but not by an herbivorous sea urchin (Arbacia punctulata) J Chem Ecol 24(10):1715–1732CrossRefGoogle Scholar
  90. Selosse MA, Faccio A, Scappaticci G, Bonfante P (2004) Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal septomycetes, including truffles. Microbiol Ecol 47(4):416–442CrossRefGoogle Scholar
  91. Sisti D, Zambonelli A, Giomaro G, Rossi I, Ceccaroli P, Citterio B, Benedetti PA, Stocchi V (1998) In vitro mycorrhizal synthesis of micropropagated Tilia platyphyllos Scop. plantlets with Tuber borchii Vittad. mycelium in pure culture. Acta Hortic 457:379–387Google Scholar
  92. Soragni E, Bolchi A, Balestrini R, Gambaretto C, Percudani R, Bonfante P, Ottonello S (2001) A nutrient-regulated, dual localization phospholipase A2 in the symbiotic fungus Tuber borchii. EMBO J 20(18):5079–5090PubMedCrossRefGoogle Scholar
  93. Sourzat P (1997) Guide pratique de trufficulture. Station d’experimentation sur la truffe. Lycee Professionnel Agricole de Cahors, Le MontatGoogle Scholar
  94. Spinnler HE, Berger C, Lapadatescu C, Bonnarme P (2001) Production of sulfur compounds by several yeasts of technological interest for cheese ripening. Int Dairy J 11:245–252CrossRefGoogle Scholar
  95. Splivallo R, Bossi S, Maffei M, Bonfante P (2007a) Discrimination of truffle fruiting body versus mycelial aromas by stir bar sorptive extraction. Phytochemistry 68:2584–2598. doi:10.1016/j.phytochem.2007.03.030PubMedCrossRefGoogle Scholar
  96. Splivallo R, Novero M, Bertea CM, Bossi S, Bonfante P (2007b) Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana. New Phytol 175:417–424PubMedCrossRefGoogle Scholar
  97. Talou T, Delmas M, Gaset A (1987a) Identification of the principal constituents of black truffle aroma. In: Frontiers of flavor. Proceedings of the 5th international flavor conference, Porto Karras, Chalkidiki, Greece, pp 367–371Google Scholar
  98. Talou T, Delmas M, Gaset A (1987b) Principal constituents of black truffle (Tuber melanosporum) aroma. J Agric Food Chem 35:774–777CrossRefGoogle Scholar
  99. Talou T, Delmas M, Gaset A (1989a) Analysis of headspace volatiles from entire black truffle (Tuber melanosporum). J Sci Food Agric 48:57–62CrossRefGoogle Scholar
  100. Talou T, Delmas M, Gaset A (1989b) Direct capture of volatiles emitted from entire black Perigord truffle. J Essent Oil Res 1:281–286Google Scholar
  101. Talou T, Delmas M, Gaset A (1989c) Black Perigord truffle: from aroma analysis to aromatizer formulation. In: Flavors and off-flavors, Proceedings of the 6th international flavor conference, Rethymnon, Crete, Greece, pp 715–728Google Scholar
  102. Talou T, Delmas M, Gaset A (1989d) New trends in black truffle aroma analysis. ACS Symp Ser 388:202–212CrossRefGoogle Scholar
  103. Tibbett M, Sanders FE (2002) Ectomycorrhizal symbiosis can enhance plant nutrition through improved access to discrete organic nutrient patches of high resource quality. Ann Bot 89:783–789PubMedCrossRefGoogle Scholar
  104. Tirillini B, Verdelli G, Paolocci F, Ciccioli P, Frattoni M (2000) The volatile organic compounds from the mycelium of Tuber borchii Vitt. Phytochemistry 55:983–985PubMedCrossRefGoogle Scholar
  105. Trappe JM (1962) Fungus associates of ectotrophic mycorrhizae. Bot Rev 28:538–606CrossRefGoogle Scholar
  106. Trappe JM (1979) The orders, families and genera of hypogeous ascomycotina (truffles and their relatives). Mycotaxon 9:297–340Google Scholar
  107. Venkateshwarlu G, Chandravadana MV, Tewari RP (1999) Volatile flavor components of some edible mushrooms (Basidiomycetes). Flavour Fragr J 14:191–194CrossRefGoogle Scholar
  108. Weden C, Danell E, Camacho FJ, Backlund A (2004) The population of the hypogeous fungus Tuber aestivum syn. Tuber uncinatum on the island of Gotland. Mycorrhiza 14(1):19–23PubMedCrossRefGoogle Scholar
  109. Wnouk S, Kinastowski S, Kaminski E (1983) Synthesis and analysis of 1-octen-3-ol, the main flavor component of mushrooms. Nahrung 27:479–486CrossRefGoogle Scholar
  110. Yang Mei C (1999) Truffles in southwest China. In: Actes du Vème congrès international, science et culture de la truffe. Fédération Française des Trufficulteurs, Aix-en-Provence, pp 4.248–4.249Google Scholar
  111. Zacchi L, Vaughan-Martini A, Angelini P (2003) Yeast distribution in a truffle field ecosystem. Ann Microbiol 53(3):275–282Google Scholar
  112. Zambonelli A, Branzanti MB (1989) Mycorrhizal synthesis of Tuber albidum Pico with Castanea sativa Mill. and Alnus cordata Loisel. Agric Ecosyst Environ 28:563–568CrossRefGoogle Scholar
  113. Zambonelli A, Branzanti MB (1990) Competizione fra Tuber albidum e alcuni basidiomiceti nella formazione di ectomycorrize su semenzali di Pinus pinea. In: Bencivenga M, Granetti B (eds) Atti del secondo congresso internazionale sul tartufo, Spoleto, pp 443–449Google Scholar
  114. Zeppa S, Gioacchini AM, Guidi C, Guescini M, Pierleoni R, Zambonelli A, Stocchi V (2004) Determination of specific volatile organic compounds synthesized during Tuber borchii Fruit body development by solid-phase microextraction and gas chromatography/mass spectrometry. Rapid Commun Mass Spectrom 18:199–205PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Richard Splivallo
    • 1
  1. 1.Department of Plant Biology, IPP-CNRUniversity of TorinoTorinoItaly

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