Browse > Article
http://dx.doi.org/10.1080/12298093.2021.1936766

Tour of Truffles: Aromas, Aphrodisiacs, Adaptogens, and More  

Allen, Kirsten (Department of Plant Biology, Rutgers, New Use Agriculture and Natural Plant Products Program, The State University of New Jersey)
Bennett, Joan W. (Department of Plant Biology, Rutgers, The State University of New Jersey)
Publication Information
Mycobiology / v.49, no.3, 2021 , pp. 201-212 More about this Journal
Abstract
Truffles are the fruiting bodies of ascomycete fungi that form underground. Truffles are globally valued, culturally celebrated as aphrodisiacs, and highly sought-after delicacies in the culinary world. For centuries, naturalists have speculated about their mode of formation, and in cultures surrounding the Mediterranean Sea, many species have been prized as a delectable food source. Truffle fruiting bodies form underground and emit a variety of volatile organic compounds (VOCs). Truffle volatiles are believed to have evolved to attract animals that disperse their spores. The main VOCs identified from truffles include sulfur compounds, such as dimethyl sulfide (DMS) and dimethyl disulfide (DMDS); in addition, 1-octen-3-ol and 2-methyl-1-propanol have been found in most truffle species. Humans use pigs and dogs trained to detect truffle VOCs in order to find these prized subterranean macrofungi. Truffles have pharmacological potential, but until more reliable cultivation methods become available their high price means they are unlikely to see widespread use as medicinals.
Keywords
Truffles; VOCs; ascomycetes; gourmet fungi; aromas;
Citations & Related Records
연도 인용수 순위
  • Reference
1 FX Cuisine.com. Cocaine is cheaper than truffles this year. 2021. Available from: http://fxcuisine.com/default.asp?language=2&Display=19&resolution=high
2 Fu SF, Wei JY, Chen HW, et al. Indole-3-acetic acid: a widespread physiological code in interactions of fungi with other organisms. Plant Signaling Behav. 2015;8:e1048052..
3 Trappe JM, Claridge AW. The hidden life of truffles. Sci Am. 2010;302(4):78-85.   DOI
4 Claus R, Hoppen HO, Karg H. The secret of truffles: a steroidal pheromone? Experientia. 1981;37(11):1178-1179.   DOI
5 Savic I, Berglund H. Androstenol-a steroid derived odor activates the hypothalamus in women. PLoS One. 2010;5(2):e8651.   DOI
6 Torben S, von Wuthenau K, Neitzke G, et al. Food authentication: species and origin determination of truffles (Tuber spp.) by inductively coupled plasma mass spectrometry and chemometrics. J Agric Food Chem. 2020;68(49):14374-14385.   DOI
7 Splivallo R, Novero M, Bertea CM, et al. Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana. New Phytol. 2007;175(3):417-424.   DOI
8 Pelusio F, Nilsson T, Montanarella L, et al. Headspace solid-phase microextraction analysis of volatile organic sulfur compounds in black and white truffle aroma. J Agric Food Chem. 1995;43(8):2138-2143.   DOI
9 Vahdatzadeh M, Deveau A, Splivallo R. The role of the microbiome of truffles in aroma formation: a meta-analysis approach. Appl Environ Microbiol. 2015;81(20):6946-6952.   DOI
10 Splivallo R, Ottonello S, Mello A, et al. Truffle volatiles: from chemical ecology to aroma biosynthesis. New Phytol. 2011;189:688-699.   DOI
11 Liao LY, He YF, Li L, et al. A preliminary review of studies on adaptogens: comparison of their bioactivity in TCM with that of ginseng-like herbs used worldwide. Chin Med. 2018;13:57.   DOI
12 Nayak S, Nayak BS. Ganoderma lucidum: multitherapeutic values mushroom. Pharm Adv Res. 2018;1:323-328.
13 Wang S, Marcone MF. The biochemistry and biological properties of the world's most expensive underground edible mushroom: truffles. Food Res Int. 2011;44(9):2567-2581.   DOI
14 Wolf F, Wolf FT. The fungi. Vol. 1. New York (NY): Jon Wiley and Sons, Inc; 1947.
15 Jeandroz S, Murat C, Wang Y, et al. Molecular phylogeny and historical biogeography of the genus Tuber, the "true truffles. J Biogeography. 2008;35(5):815-829.   DOI
16 Luard E. Truffles. Childs hill, London: Berry & Co., Ltd; 2006.
17 Shavit E. The history of desert truffle use. Desert truffles phylogeny, physiology, distribution and domestication. Berlin, Germany: Springer; 2014. p. 217-241.
18 Robinson T. An account of the Tubera Terrae, or truffles found at Rushton in Northamptonshire; with some remarks thereon. Philos Trans Royal Soc Lond. 1693;17(202):824-826.   DOI
19 Gilkey HM. Tuberales of North America. Oregon State Monographs Studies in Botany. 1939;1:1-63.
20 Benjamin DR. Mushrooms: poisons and panaceas. A handbook for naturalists, mycologists, and physicians. New York (NY): W. H Freeman and Company; 1995.
21 Tietel Z, Masaphy S. True morels (Morchella)-nutritional and phytochemical composition, health benefits and flavor: a review. Crit Rev Food Sci Nutr. 2018;58(11):1888-1901.   DOI
22 Claridge AW, Trappe JM. Sporocarp mycophagy: nutritional, behavioral, evolutionary, and physiological aspects. The fungal community-its organization and role in the ecosystem. Boca Raton (FL): CRC Press; 2005. p. 599-611.
23 De Angelis F, Arcadi A, Marinelli F, et al. Partial structures of truffle melanins. Phytochemistry. 1996;43(5):1103-1106.   DOI
24 Patel S. Food, health and agricultural importance of truffles: a review of current scientific literature. Curr Trend Biotechnol Pharm. 2012;6:15-27.
25 Shashkina MY, Shashkin PN, Sergeev AV. Chemical and medicobiological properties of chaga. Pharm Chem J. 2006;40(10):560-568.   DOI
26 Amicarelli F, Bonfigli A, Colafarina S, et al. Glutathione dependent enzymes and antioxidant defences in truffles: organisms living in microaerobic environments. Mycol Res . 1999; 103(12):1643-1648.   DOI
27 Kagan-Zur V, Roth-Bejerano N, Sitrit Y, et al. Desert truffles. Phylogeny physiology, distribution and domestication. Berlin, Germany: Springer Science & Business Media; 2013.
28 O'Donnell K, Cigelnik E, Weber NS, et al. Phylogenetic relationships among ascomycetous truffles and the true and false morels inferred from 18S and 28S ribosomal DNA sequence analysis. Mycologia. 1997;89(1):48-65.   DOI
29 Laessoe T, Hansen K. Truffle trouble: what happened to the Tuberales? Mycol Res. 2007;111:1075-1099.   DOI
30 Louro R, Natario B, Santos-Silva C. Morphological characterization of the in vitro mycorrhizae formed between four Terfezia species (Pezizaceae) with Cistus salviifolius and Cistus ladanifer-towards desert truffles production in acid soils. J Fungi. 2021;7(1):35.   DOI
31 Splivallo R, Fischer U, GoBel C, et al. Truffles regulate plant root morphogenesis via the production of auxin and ethylene. Plant Physiol. 2009;150(4):2018-2029.   DOI
32 Paz A, Bellanger JM, Lavoise C, et al. The genus Elaphomyces (Ascomycota, Eurotiales): a ribosomal DNA-based phylogeny and revised systematics of European 'deer truffles.' Persoonia. 2017;38:197-239.   DOI
33 Linde CC, Selmes H. Genetic diversity and mating type distribution of Tuber melanosporum and their significance to truffle cultivation in artificially planted truffieres in Australia. Appl Environ Microbiol. 2012;78(18):6534-6539.   DOI
34 Jacobs R. The truffle underground. A tale of mystery, mayhem, and manipulation in the shadowy market of the world's most expensive fungus. New York (NY): Clarkson Potter/Publishers; 2019.
35 Moore AMD, Pithavadian R. Aphrodisiacs in the global history of medical thought. J Glob Hist. 2021;16(1):20-24.
36 Walker N. Dirty sex: pigs and truffles. Pleiades. 2019;39(2):161-165.   DOI
37 March RE, Richards DS, Ryan RW. Volatile compounds from six species of truffle - head-space analysis and vapor analysis at high mass resolution. Int J Mass Spectrom. 2006;249-250:60-67.   DOI
38 McGee H. Nose dive: a field guide to the world's smells. New York (NY): Penguin Press; 2020.
39 Harki E, Bouya D, Dargent R. Maturation-associated alterations of the biochemical characteristics of the black truffle Tuber melanosporum Vitt. Food Chem. 2006;99(2):394-400.   DOI
40 Liu RS, Zhou H, Li HM, et al. Metabolism of L-methionine linked to the biosynthesis of volatile organic sulfur-containing compounds during the submerged fermentation of Tuber melanosporum. Appl Microbiol Biotechnol. 2013;97(23):9981e9992.   DOI
41 Eugenia B. Mycophilia. Revelations from the weird world of mushrooms. New York (NY): Rodale; 2011.
42 Kanchiswamy CN, Malnoy M, Maffei ME. Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front Plant Sci. 2015;6:151..   DOI
43 Helttula A. Truffles in ancient Greece and Rome. ARCTOS. Acta Philol Fenn. 1996;30:33-47.
44 New International Version Bible. The International Bible Society. Grand Rapids (MI): Zondervan; 1973.
45 Khalifa SAM, Farag MA, Yosri N, et al. Truffles: from Islamic culture to chemistry, pharmacology, and food trends in recent times. Trends Food Sci Technol. 2019;91:193-218.   DOI
46 Mennell S. All manners of food: eating and taste in England and France from the middle ages to the present. 2nd ed., Vol. 65-66. Champaign (IL): University of Illinois Press; 1996. p. 69-71.
47 Harkness HW. Californian hypogeous fungi. Proceedings of the California Academy of Science. Vol. 3. San Francisco (CA): The California Academy of the Sciences; 1899. p. 241-292.
48 Maser C, Claridge AW, Trappe JM. Trees, truffles and beasts: how forests function. Piscataway (NJ): Rutgers University Press; 2008.
49 Ackerman D. A natural history of the senses. Vintage books. New York (NY): Random House; 1990.
50 Wang R, Sun Q, Chang Q. Soil type effects on grape and wine composition in Helan Mountain area of Ningxia. PLoS One. 2015;10(2):e0116690..   DOI
51 Mustafa AM, Angeloni S, Nzekoue FK, et al. An overview on truffle aroma and main volatile compounds. Molecules. 2020;25(24):5948.   DOI
52 Xiao DR, Liu RS, He L, et al. Aroma improvement by repeated freeze-thaw treatment during Tuber melanosporum fermentation. Sci Rep. 2015;5:17120..   DOI
53 Cullere L, Ferreira V, Chevret B, et al. Characterization of aroma active compounds in black truffles (Tuber melanosporum) and summer truffles (Tuber aestivum) by gas chromatographyolfactometry. Food Chem. 2010;122(1):300-306.   DOI
54 Splivallo R, Ebeler SE. Sulfur volatiles of microbial origin are key contributors to human-sensed truffle aroma. Appl Microbiol Biotechnol. 2015;99:2583-2592.   DOI
55 Mauriello G, Marino R, D'Auria M, et al. Determination of volatile organic compounds from truffles via SPME-GC-MS. J Chromatogr Sci. 2004;42(6):299-305.   DOI
56 Stephens RB, Trowbridge AM, Ouimette AP, et al. Signaling from below: rodents select for deeper fruiting truffles with stronger volatile emissions. Ecology. 2020;101(3):e02964.
57 Fraatz MA, Zorn H. Fungal flavours. The Mycota X: industrial applications. Berlin, Heidelberg: Springer-Verlag; 2010. p. 249-264.
58 Menotta M, Amicucci A, Sisti D, et al. Differential gene expression during pre-symbiotic interaction between Tuber borchii Vittad. and Tilia americana L. Current Genet. 2004;46:158-165.
59 Trappe JM, Molina R, Luoma DL, et al. Diversity, ecology, and conservation of truffle fungi in forests of the Pacific Northwest. U. S. Department of agriculture, general technical report PNW-GTR-772. 2009. Available from: https://www.fs.fed.us/pnw/pubs/pnw_gtr772.pdf
60 Splivallo R, Deveau A, Valdez N, et al. Bacteria associated with truffle-fruiting bodies contribute to truffle aroma. Environ Microbiol. 2015;17(8):2647-2660.   DOI
61 Pacioni G. Effects of Tuber metabolites on the rhizospheric environment. Mycol Res. 1991;95(12):1355-1358.(09)80384-5.   DOI
62 Wu Z, Meenu M, Xu B. Nutritional value and antioxidant activity of Chinese black truffle (Tuber indicum) grown in different geographical regions in China. Lwt Food Sci Technol. 2021;135:110226.   DOI
63 Martin F, Kohler A, Murat C, et al. Perigord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature. 2010;464:1033-1038.   DOI
64 Hall IR, Brown G, Byars J. The black truffle: its history, uses and cultivation. Christchurch, New Zealand: New Zealand Institute for Crop & Food Research Limited; 1994.
65 Winslow LC, Kroll DJ. Herbs as medicines. Arch Intern Med. 1998;158(20):2192-2199.   DOI
66 Dogan HH, Aydin S. Determination of antimicrobial effect, antioxidant activity and phenolic contents of desert truffle in Turkey. Afr J Tradit Complement Altern Med. 2013;10(4):52e58.
67 Pacioni G, Rapino C, Zarivi O, et al. Truffles contain endocannabinoid metabolic enzymes and anandamide. Phytochemistry. 2015;110:104-110.   DOI
68 Rubini A, Riccioni C, Belfiori B, et al. Impact of the competition between mating types on the cultivation of Tuber melanosporum: Romeo and Juliet and the matter of space and time. Mycorrhiza. 2014;24(S1):19-27.   DOI
69 Burke R, Cairney J. Laccases and other polyphenol oxidases in ecto- and ericoid mycorrhizal fungi. Mycorrhiza. 2002;12(3):105e116-105e116..
70 Bach C, Beacco P, Cammaletti P, et al. First production of Italian white truffle (Tuber magnatum Pico) ascocarps in an orchard outside its natural range distribution in France. Mycorrhiza. 2021;31(3):383-388.   DOI
71 Stark R. The book of aphrodisiacs. New York (NY): Stein and Day; 1981.
72 Wang G, Li YY, Li DS, et al. Determination of 5alpha-androst-16-en-3alpha-ol in truffle fermentation broth by solid-phase extraction coupled with gas chromatography-flame ionization detector/electron impact mass spectrometry. J Chromatogr B Anal Technol Biomed Life Sci. 2008;870(2):209e215..
73 Pieroni A. The changing ethnoecological cobweb of white truffle (Tuber magnatum Pico) gatherers in South Piedmont, NW Italy. J Ethnobiol Ethnomed. 2016;12:18.   DOI
74 Patterson D. Hocus-Pocus, and a beaker of truffles. New York Times; 2007. Available from: https://www.nytimes.com/2007/05/16/dining/16truf.html.
75 El Enshasy H, Elsayed EA, Aziz R, et al. Mushrooms and truffles: historical biofactories for complementary medicine in Africa and in the middle East. Evid Based Complement Alternat Med. 2013;2013:620451.
76 Pacioni G, Bologna MA, Laurenzi M. Insect attraction by Tuber: a chemical explication. Mycol. Res. 1991;95(12):1359-1363.   DOI
77 Lefevre C, Hall I. The status of truffle cultivation: a global perspective. Acta Hortic. 2001;556(556):513-520.   DOI
78 Berch SM. Truffle cultivation and commercially harvested native truffles. Proceedings International symposium on Forest Mushroom. Seoul, South Korea: Korea Forest Research Institute; 2013. Korean Forest Mushroom Society. http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.396.7265&rep=rep1&type=pdf.
79 Tang YJ, Liu RS, Li HM. Current progress on truffle submerged fermentation: a promising alternative to its fruiting bodies. Appl Microbiol Biotechnol. 2015;99(5):e2053-2053..
80 Barwich AS. Smellosophy: what the nose tells the mind. Cambridge (MA): Harvard University Press; 2020.
81 Pacioni G, Cerretani L, Procida G, et al. Composition of commercial truffle flavored oils with GC-MS analysis and discrimination with an electronic nose. Food Chem. 2014;146:30-35..   DOI
82 Saltarelli R, Ceccaroli P, Cesari P, et al. Effect of storage on biochemical and microbiological parameters of edible truffle species. Food Chem. 2008;109:8-16.   DOI
83 Ramsbottom J. Mushrooms & toadstools: a study of the activities of fungi. London: Collins, St. James's Place; 1953.
84 Patel S, Rauf A, Khan H, et al. Potential health benefits of natural products derived from truffles: a review. Trends in Food Science & Technology. 2017;70:1-8..   DOI
85 Hall IR, Brown GT, Zambonelli A. Taming the truffle. The history, lore, and science of the ultimate mushroom. Portland, Oregon: Timber Press; 2007.
86 Ainsworth GC, Sussman AS. Historical introduction to mycology. The fungi. An advanced treatise. Vol. 1. New York (NY): Academic Press; 1965. p. 3-20.