Truffle volatiles: From chemical ecology to aroma biosynthesis

New Phytologist

Volumn 189, Issue 3, 2011, Pages 688-699

  Splivallo, Richard ^a   Ottonello, Simone ^b   Mello, Antonietta ^c   Karlovsky, Petr ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b UNIVERSITY OF PARMA   (Italy)

^c UNIVERSITY OF TURIN   (Italy)

Author keywords

Aroma biosynthesis; Chemical ecology; Ectomycorrhiza; Plant microbe interactions; Truffles; Tuber borchii; Tuber melanosporum; Volatile organic compounds

Indexed keywords

VOLATILE ORGANIC COMPOUND;

CHEMICAL ECOLOGY; DEVELOPMENTAL BIOLOGY; ECTOMYCORRHIZA; FUNGUS; GENOMICS; INSECT; MAMMAL; MICROORGANISM; MOLECULAR ANALYSIS; RESEARCH WORK; SPORE; VOLATILE ORGANIC COMPOUND;

ASCOMYCETES; ECOLOGY; METABOLISM; ODOR; REVIEW;

ASCOMYCOTA; ECOLOGY; ODORS; VOLATILE ORGANIC COMPOUNDS;

BACTERIA (MICROORGANISMS); FUNGI; HEXAPODA; MAMMALIA; TUBER (TRUFFLE); TUBER BORCHII; TUBER MELANOSPORUM;

EID: 78651272561     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2010.03523.x     Document Type: Review

References (60)

1. Arfi K, Landaud S, Bonnarme P. 2006. Evidence for distinct L-methionine catabolic pathways in the east Geotrichum candidum and the bacterium Brevibacterium linens. Applied and Environmental Microbiology 72: 2155-2162.
2. van Asten A. 2002. The importance of GC and GC-MS in perfume analysis. Trends in Analytical Chemistry: TRAC 21: 698-708.
3. Baldwin IT, Halitschke R, Paschold A, von Dahl CC, Preston CA. 2006. Volatile signaling in plant-plant interactions: "talking trees" in the genomics era. Science 311: 812-815.
4. Barbieri E, Bertini L, Rossi I, Ceccaroli P, Saltarelli R, Guidi C, Zambonelli A, Stocchi V. 2005a. New evidence for bacterial diversity in the ascoma of the ectomycorrhizal fungus Tuber borchii Vittad. FEMS Microbiology Letters 247: 23-35.
5. Barbieri E, Gioacchini AM, Zambonelli A, Bertini L, Stocchi V. 2005b. Determination of microbial volatile organic compounds from Staphylococcus pasteuri against Tuber borchii using solid-phase microextraction and gas chromatography/ion trap mass spectrometry. Rapid Communications in Mass Spectrometry 19: 3411-3415.
6. Barbieri E, Guidi C, Bertaux J, Frey-Klett P, Garbaye J, Ceccaroli P, Saltarelli R, Zambonelli A, Stocchi V. 2007. Occurrence and diversity of bacterial communities in Tuber magnatum during truffle maturation. Environmental Microbiology 9: 2234-2246.
7. Barbieri E, Potenza L, Rossi I, Sisti D, Giomaro G, Rossetti S, Beimfohr C, Stocchi V. 2000. Phylogenetic characterization and in situ detection of a Cytophaga-Flexibacter-Bacteroides phylogroup bacterium in Tuber borchii Vittad. ectomycorrhizal mycelium. Applied and Environmental Microbiology 66: 5035-5042.
8. Bellesia F, Pinetti A, Bianchi A, Tirillini B. 1996. I composti solforati dell'aroma del tartufo: loro evoluzione durante la conservazione (in italian). Atti Soc Nat e Mat Di Modena 127: 177-187.
9. Bellesia F, Pinetti A, Tirillini B, Bianchi A. 2001. Temperature-dependent evolution of volatile organic compounds in Tuber borchii from Italy. Flavour and Fragrance Journal 16: 1-6.
10. Bonnarme P, Psoni L, Spinnler HE. 2000. Diversity of L-methionine catabolism pathways in cheese-ripening bacteria. Applied and Environmental Microbiology 66: 5514-5517.
11. 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. Archives of Microbiology 184: 187-193.
12. Claus R, Hoppen HO, Karg H. 1981. The secret of truffles: a steroidal pheromone? Cellular and Molecular Life Sciences 37: 1178-1179.
13. Culleré L, Ferreira V, Chevret B, Venturini ME, Sánchez-Gimeno AC, Blanco D. 2010. Characterisation of aroma active compounds in black truffles (Tuber melanosporum) and summer truffles (Tuber aestivum) by gas chromatography-olfactometry. Food Chemistry 122: 300-306.
14. Dick CM, Hutchinson SA. 1966. Biological activity of volatile fungal metabolites. Nature 211: 868.
15. 1. FEMS Microbiology Letters 182: 249-254.
16. 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. Sensors and Actuators B: Chemical 106: 88-94.
17. Fernández M, van Doesburg W, Rutten GAM, Marugg JD, Alting AC, van Kranenburg R, Kuipers OP. 2000. Molecular and functional analyses of the metC gene of Lactococcus lactis, encoding cystathionine β-Lyase. Applied and Environmental Microbiology 66: 42-48.
18. Fiecchi A, Kienle MG, Scala A, Cabella P. 1967. Bis-methylthiomethane, an odorous substance from white truffle, pico. Tetrahedron Letters 8: 1681-1682.
19. Gioacchini AM, Menotta M, Bertini L, Rossi I, Zeppa S, Zambonelli A, Piccoli G, Stocchi V. 2005. Solid-phase microextraction gas chromatography/mass spectrometry: a new method for species identification of truffles. Rapid Communications in Mass Spectrometry 19: 2365-2370.
20. Gioacchini AM, Menotta M, Guescini M, Saltarelli R, Ceccaroli P, Amicucci A, Barbieri E, Giomaro G, Stocchi V. 2008. Geographical traceability of Italian white truffle (Tuber magnatum Pico) by the analysis of volatile organic compounds. Rapid Communications in Mass Spectrometry: RCM 22: 3147-3153.
21. Gohlke RS, McLafferty FW. 1993. Early gas chromatography/mass spectrometry. Journal of the American Society for Mass Spectrometry 4: 367-371.
22. Grimaldi B, de Raaf MA, Filetici P, Ottonello S, Ballario P. 2005. Agrobacterium-mediated gene transfer and enhanced green fluorescent protein visualization in the mycorrhizal ascomycete Tuber borchii: a first step towards truffle genetics. Current Genetics 48: 69-74.
23. Grossmann K. 2003. Mediation of herbicide effects by hormone interactions. Journal of Plant Growth Regulation 22: 109-122.
24. Guadagni DG, Buttery RG, Okano S. 1963. Odour threshold of some organic compounds associated with food flavors. Journal of the Science of Food and Agriculture 14: 761-765.
25. 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 characterisation of the tbhmgr, tbfpps and tbsqs genes. Current Genetics 50: 393-404.
26. Hanniffy S, Peláez C, Martínez-Bartolomé M, Requena T, Martínez-Cuesta M. 2009. Key enzymes involved in methionine catabolism by cheese lactic acid bacteria. International Journal of Food Microbiology 135: 223-230.
27. Hansen H, Grossmann K. 2000. Auxin-induced ethylene triggers abscisic acid biosynthesis and growth inhibition. Plant Physiology 124: 1437-1448.
28. Harki E, Bouya D, Dargent R. 2006. Maturation-associated alterations of the biochemical characteristics of the black truffle Tuber melanosporum Vitt. Food Chemistry 99: 394-400.
29. Hazelwood LA, Daran J, van Maris AJA, Pronk JT, Dickinson JR. 2008. The Ehrlich pathway for fusel alcohol production: a century of research on Saccharomyces cerevisiae metabolism. Applied and Environmental Microbiology 74: 3920.
30. Hochberg ME, Bertault G, Poitrineau K, Janssen A. 2003. Olfactory orientation of the truffle beetle, Leiodes cinnamomea. Entomologia Experimentalis et Applicata 109: 147-153.
31. Kishimoto K, Matsui K, Ozawa R, Takabayashi J. 2007. Volatile 1-octen-3-ol induces a defensive response in Arabidopsis thaliana. Journal of General Plant Pathology 73: 35-37.
32. Kuzuyama T, Seto H. 2003. Diversity of the biosynthesis of the isoprene units. Natural Product Reports 20: 171-183.
33. Liu M, Nauta A, Francke C, Siezen RJ. 2008. Comparative genomics of enzymes in flavor-forming pathways from amino acids in lactic acid bacteria. Applied and Environmental Microbiology 74: 4590-4600.
34. Liu QN, Liu RS, Wang YH, Mi ZY, Li DS, Zhong JJ, Tang YJ. 2009. Fed-batch fermentation of Tuber melanosporum for the hyperproduction of mycelia and bioactive Tuber polysaccharides. Bioresource Technology 100: 3644-3649.
35. Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R et al. 2010. Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464: 1033-1038.
36. Martínez-Cuesta MC, Peláez C, Eagles J, Gasson MJ, Requena T, Hanniffy SB. 2006. YtjE from Lactococcus lactis IL1403 Is a C-S lyase with α, γ-elimination activity toward methionine. Applied and Environmental Microbiology 72: 4878-4884.
37. Maser C, Claridge AW, Trappe JM. 2008. Trees, truffles, and beasts: how forests function. Piscataway, New Jersey, USA: Rutgers University Press.
38. Mauriello G, Marino R, D'Auria M, Cerone G, Rana GL. 2004. Determination of volatile organic compounds from truffles via SPME GC- MS. Journal of Chromatographic Science 42: 299-305.
39. Mello A, Murat C, Bonfante P. 2006. Truffles: much more than a prized and local fungal delicacy. FEMS Microbiology Letters 260: 1-8.
40. Menotta M, Gioacchini AM, Amicucci A, Buffalini M, Sisti D, Stocchi V. 2004. Headspace solid-phase microextraction with gas chromatography and mass spectrometry in the investigation of volatile organic compounds in an ectomycorrhizae synthesis system. Rapid Communications in Mass Spectrometry 18: 206-210.
41. Napoli C, Mello A, Borra A, Vizzini A, Sourzat P, Bonfante P. 2010. Tuber melanosporum, when dominant, affects fungal dynamics in truffle grounds. New Phytologist 185: 237-247.
42. Pacioni G, Bologna MA, Laurenzi M. 1991. Insect attraction by Tuber: a chemical explanation. Mycological Research 95: 1359-1363.
43. Pacioni G, Leonardi M, Aimola P, Ragnelli AM, Rubini A, Paolocci F. 2007. Isolation and characterization of some mycelia inhabiting Tuber ascomata. Mycological Research 111: 1450-1460.
44. Pelusio F, Nilsson T, Montanarella L, Tilio R, Larsen B, Facchetti S, Madsen J. 1995. Headspace solid-phase microextraction analysis of volatile organic sulfur compounds in black and white truffle aroma. Journal of Agricultural and Food Chemistry 43: 2138-2143.
45. Senger T, Wichard T, Kunze S, Göbel C, Lerchl J, Pohnert G, Feussner I. 2005. A multifunctional lipoxygenase with fatty acid hydroperoxide cleaving activity from the moss Physcomitrella patens. The Journal of Biological Chemistry 280: 7588-7596.
46. 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.
47. Splivallo R, Fischer U, Gobel C, Feussner I, Karlovsky P. 2009. Truffles regulate plant root morphogenesis via the production of auxin and ethylene. Plant Physiology 150: 2018-2029.
48. Splivallo R, Novero M, Bertea CM, Bossi S, Bonfante P. 2007b. Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana. New Phytologist 175: 417-424.
49. Suz LM, Martín MP, Oliach D, Fischer CR, Colinas C. 2008. Mycelial abundance and other factors related to truffle productivity in Tuber melanosporum-Quercus ilex orchards. FEMS Microbiology Letters 285: 72-78.
50. Talou T, Delmas M, Gaset A. 1989. Black Perigord truffle: from aroma analysis to aromatizer formulation. Flavors and Off-flavors, Proceedings of the 6th International Flavor Conference. Rethymnon, Crete, Greece, 715-728.
51. Talou T, Gaset A, Delmas M, Kulifaj M, Montant C. 1990. Dimethyl sulphide: the secret for black truffle hunting by animals? Mycological Research 94: 277-278.
52. Tang YJ, Wang G, Li YY, Zhong JJ. 2009. Fermentation condition outweighed truffle species in affecting volatile organic compounds analyzed by chromatographic fingerprint system. Analytica Chimica Acta 647: 40-45.
53. Tang YJ, Zhu LL, Li DS, Mi ZY, Li HM. 2008a. Significance of inoculation density and carbon source on the mycelial growth and Tuber polysaccharides production by submerged fermentation of Chinese truffle Tuber sinense. Process Biochemistry 43: 576-586.
54. Tang YJ, Zhu LL, Liu RS, Li HM, Li DS, Mi ZY. 2008b. Quantitative response of cell growth and Tuber polysaccharides biosynthesis by medicinal mushroom Chinese truffle Tuber sinense to metal ion in culture medium. Bioresource Technology 99: 7606-7615.
55. Tirillini B, Verdelli G, Paolocci F, Ciccioli P, Frattoni M. 2000. The volatile organic compounds from the mycelium of Tuber borchii Vitt. Phytochemistry 55: 983-985.
56. Trappe JM, Claridge AW. 2010. The hidden life of truffles. Scientific American 302: 78-84.
57. Wenke K, Kai M, Piechulla B. 2010. Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231: 499-506.
58. Yuan JS, Himanen SJ, Holopainen JK, Chen F, Stewart CN Jr. 2009. Smelling global climate change: mitigation of function for plant volatile organic compounds. Trends in Ecology and Evolution 24: 323-331.
59. Zawirska-Wojtasiak R. 2004. Optical purity of (R)-(-)-1-octen-3-ol in the aroma of various species of edible mushrooms. Food Chemistry 86: 113-118.
60. Zeppa S, Gioacchini AM, Guidi C, Guescini M, Pierleoni R, Zambonelli A, Stocchi V. 2004. Determination of specific volatile organic compounds synthesised during Tuber borchii fruit body development by solid-phase microextraction and gas chromatography/mass spectrometry. Rapid Communications in Mass Spectrometry 18: 199-205.