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Truffle Ecology: Genetic Diversity, Soil Interactions and Functioning

  • Antonietta MelloEmail author
  • Elisa Zampieri
  • Alessandra Zambonelli
Chapter

Abstract

Truffles are fungi producing hypogeous fruiting bodies belonging to at least 13 phylogenetically distant orders. The most studied are “true truffles” belonging to the genus Tuber, which is the most economically important group. Truffle fruiting bodies are colonized by bacteria, yeasts, guest filamentous fungi and viruses that, all together, constitute the truffle microbiota. Research on the role of this community has demonstrated that bacteria contribute to truffle aroma. From the ecological point of view, truffle aroma attracts mycophagous animals, which in turn disperse and diffuse truffle spores in the soil, and mediates interactions with microorganisms and plant roots. Truffles have a heterothallic organization, whereby for truffle reproduction it is necessary that strains of opposite mating type meet. Regarding truffle development, the truffle ascocarps use carbon coming from the host plant and not from dead host tissues or soil organic matter as believed so far. In addition to form ectomycorrhizae with a wide diversity of host plants, some truffle species are able to form also arbutoid and orchid mycorrhizas.

Knowledge of truffle diversity, traditionally relied on the survey and molecular identification of fruiting bodies, moved over the years towards the survey of mycorrhizas and, recently, on the distribution in soil of the mycelium, with the determination of genets and mating types. The possibility of studying (micro)organisms directly in the field (metagenomics or environmental genomics) and the introduction of high-throughput sequencing techniques (454 pyrosequencing) have given a strong impulse to the study of the microbial communities interacting with truffles and their habitat.

Keywords

Arbuscular Mycorrhizal Fungus Fruiting Body Mating Type Ectomycorrhizal Fungus Opposite Mating Type 
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.

References

  1. Barbieri E, Gioacchini AM, Zambonelli A et al (2005) Determination of microbial volatile organic compounds from Staphylococcus pasteuri against Tuber borchii using solid-phase microextraction and gas chromatography/ion trap mass spectrometry. Rapid Commun Mass Spectrom 19:3411–3415PubMedCrossRefGoogle Scholar
  2. Belfiori B, Riccioni C, Paolocci F et al (2013) Mating type locus of Chinese black truffles reveals heterothallism and the presence of cryptic species within the Tuber indicum species complex. PLoS One 8:e82353PubMedPubMedCentralCrossRefGoogle Scholar
  3. Belfiori B, Riccioni C, Paolocci F et al (2016) Characterization of the reproductive mode and life cycle of the whitish truffle T. borchii. Mycorrhiza 26:515–527PubMedCrossRefGoogle Scholar
  4. Bencivenga M, Urbani G (1992) Note sull’ecologia e sulla coltivazione del tartufo bianco (Tuber magnatum Pico). L’inf Agrar 48:64–69Google Scholar
  5. Benucci GM, Raggi L, Albertini E et al (2011) Ectomycorrhizal communities in a productive Tuber aestivum Vittad. orchard: composition, host influence and species replacement. FEMS Microbiol Ecol 76:170–184PubMedCrossRefGoogle Scholar
  6. Benucci GMN, Bonito G, Baciarelli LF et al (2012) Mycorrhization of Pecan trees (Carya illinoinensis) with commercial truffle species: Tuber aestivum Vittad. and Tuber borchii Vittad. Mycorrhiza 22:383–392PubMedCrossRefGoogle Scholar
  7. Berch SM, Bonito G (2014) Cultivation of Mediterranean species of Tuber (Tuberaceae) in British Columbia, Canada. Mycorrhiza 24:473–479PubMedCrossRefGoogle Scholar
  8. Berch SM, Bonito G (2016) Truffle diversity (Tuber, Tuberaceae) in British Columbia. Mycorrhiza 26:587–594PubMedCrossRefGoogle Scholar
  9. Bertault G, Raymond M, Berthomieu A et al (1998) Trifling variation in truffles. Nature 394:734–734CrossRefGoogle Scholar
  10. Bertini L, Rossi I, Zambonelli A et al (2006) Molecular identification of Tuber magnatum ectomycorrhizas in the field. Microbiol Res 161:59–64PubMedCrossRefGoogle Scholar
  11. Bonito G, Smith ME (2016) General systematic position of the truffles: evolutionary theories. In: Zambonelli A, Iotti M, Murat C (eds) True truffle (Tuber spp.) in the World. Soil Biol 47:3–18 (in press)Google Scholar
  12. Bonito G, Gryganskyi A, Vilgalys R et al (2010a) A global metaanalysis of Tuber ITS rDNA sequences: species diversity, host specificity, and long-distance dispersal. Mol Ecol 19:4994–5008PubMedCrossRefGoogle Scholar
  13. Bonito G, Trappe JM, Rawlinson P et al (2010b) Improved resolution of major clades within Tuber and taxonomy of species within the Tuber gibbosum complex. Mycologia 102:1042–1057PubMedCrossRefGoogle Scholar
  14. Bonito G, Brenneman T, Vilgalys R (2011a) Ectomycorrhizal fungal diversity in orchards of cultivated pecan (Carya illinoinensis; Juglandaceae). Mycorrhiza 21(7):601–612PubMedCrossRefGoogle Scholar
  15. Bonito G, Trappe JM, Donovan S et al (2011b) The Asian black truffle Tuber indicum can form ectomycorrhizas with North American host plants and complete its life cycle in non-native soils. Fungal Ecol 4:83–93CrossRefGoogle Scholar
  16. Bonito G, Smith ME, Nowak M et al (2013) Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage. PLoS One 8:e52765PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bonuso E, Zambonelli A, Bergemann SE et al (2010) Multilocus phylogenetic and coalescent analyses identify two cryptic species in the Italian bianchetto truffle, Tuber borchii Vittad. Conserv Genet 11:1453–1466CrossRefGoogle Scholar
  18. Bragato G (2014) Is truffle brûlé a case of perturbational niche construction? For Syst 23:349–356Google Scholar
  19. Bragato G, Vignozzi N, Pellegrini S et al (2010) Physical characteristics of the soil environment suitable for Tuber magnatum production in fluvial landscapes. Plant Soil 329:51–63CrossRefGoogle Scholar
  20. Callot G (1999) La truffe, la terre, la vie. INRA, Quae, p 210Google Scholar
  21. Ceruti A, Fontana A, Nosenzo C (2003) Le Specie Europee del Genere Tuber, Una revisione storica. Museo regionale di scienze Naturali, monografie XXXVII, TorinoGoogle Scholar
  22. Chen J, Liu PG (2007) Tuber latisporum sp. nov. and related taxa, based on morphology and DNA sequence data. Mycologia 99:475–481PubMedCrossRefGoogle Scholar
  23. Chevalier G, Desmas C, Frochot H et al (1979) L’espéce Tuber aestivum Vitt: I. Dèfinition. Mushroom Sci X (Part 1) 10:957–975Google Scholar
  24. Christopoulos V, Psoma P, Diamandis S (2013) Site characteristics of Tuber magnatum in Greece. Acta Mycol 48:27–32CrossRefGoogle Scholar
  25. Comandini O, Pacioni G (1997) Mycorrhizae of Asian black truffles, Tuber himalayense and T. indicum. Mycotaxon 63:77–86Google Scholar
  26. Di Massimo G, García-Montero LG, Bencivenga M et al (1996) Tuber indicum Cooke et Massee, un tartufo orientale simile a Tuber melanosporum Vitt. Micol Veg Mediterr 11:107–114Google Scholar
  27. Fan L, Yue SF (2013) Phylogenetic divergence of three morphologically similar truffles: Tuber sphaerosporum, T. sinosphaerosporum, and T. pseudosphaerosporum sp. nov. Mycotaxon 125:283–288CrossRefGoogle Scholar
  28. Fan L, Liu X, Cao J (2015) Tuber turmericum sp. nov., a Chinese truffle species based on morphological and molecular data. Mycol Prog 14:1–6CrossRefGoogle Scholar
  29. Fan L, Han L, Zhang PR et al (2016a) Molecular analysis of Chinese truffles resembling Tuber californicum in morphology reveals a rich pattern of species diversity with emphasis on four new species. Mycologia 108:344–353PubMedCrossRefGoogle Scholar
  30. Fan L, Zhang PR, Yan XY et al (2016b) Phylogenetic analyses of Chinese Tuber species that resemble T. borchii reveal the existence of the new species T. hubeiense and T. wumengense. Mycologia 108:354–362PubMedCrossRefGoogle Scholar
  31. García-Montero LG, Di Massimo G, Manjón JL et al (2008) New data on ectomycorrhizae and soils of the Chinese truffles Tuber pseudoexcavatum and Tuber indicum, and their impact on truffle cultivation. Mycorrhiza 19:7–14PubMedCrossRefGoogle Scholar
  32. García-Montero LG, Díaz P, Di Massimo G et al (2010) A review of research on Chinese Tuber species. Mycol Prog 9:315–335CrossRefGoogle Scholar
  33. García-Montero LG, Moreno D, Monleon VJ et al (2014) Natural production of Tuber aestivum in central Spain: Pinus spp. versus Quercus spp. brûles. For Syst 23:394–399Google Scholar
  34. Gardin L (2005) I tartufi minori in Toscana. Gli ambienti di crescita dei tartufi marzuolo e scorzone. Quad ARSIA 1:1–56Google Scholar
  35. Gryndler M, Trilčová J, Hršelová H et al (2013) Tuber aestivum Vittad. mycelium quantified: advantages and limitations of a qPCR approach. Mycorrhiza 23:341–348PubMedCrossRefGoogle Scholar
  36. Gryndler M, Cerná L, Bukovská P et al (2014) Tuber aestivum association with non-host roots. Mycorrhiza 24:603–610PubMedCrossRefGoogle Scholar
  37. Gryndler M, Beskid O, Hršelová H et al (2015) Mutabilis in mutabili: spatiotemporal dynamics of a truffle colony in soil. Soil Biol Biochem 90:62–70CrossRefGoogle Scholar
  38. Guevara G, Bonito G, Trappe JM et al (2013) New North American truffles (Tuber spp.) and their ectomycorrhizal associations. Mycologia 105:194–209PubMedCrossRefGoogle Scholar
  39. Hall IR, Haslam W (2012) Truffle cultivation in southern hemisphere. In: Zambonelli A, Bonito GM (eds) Edible ectomycorrhizal mushrooms. Soil Biol 34:191–208Google Scholar
  40. Hall IR, Zambonelli A (2012) The cultivation of mycorrhizal mushrooms—still the next frontier! In: Zhang J, Wang H, Chen M (eds) Mushroom science XVIII. China Agricultural Press, Beijing, pp 16–27Google Scholar
  41. Hall IR, Zambonelli A, Primavera F (1998) Ectomycorrhizal fungi with edible fruiting bodies 3. Tuber magnatum, Tuberaceae. Econ Bot 52:192–200CrossRefGoogle Scholar
  42. Hall I, Brown G, Zambonelli A (2007) Taming the truffle. The history, lore, and science of the ultimate mushroom. Timber Press, PortlandGoogle Scholar
  43. Healy RA, Smith ME, Bonito GM et al (2013) High diversity and wide spread occurrence of mitotic spore mats in ectomycorrhizal Pezizales. Mol Ecol 22:1717–1732PubMedCrossRefGoogle Scholar
  44. Healy RA, Zurier H, Bonito G et al (2016) Mycorrhizal detection of native and non-native truffles in a historic arboretum and the discovery of a new North American species, Tuber arnoldianum sp. nov. Mycorrhiza 26:781–792PubMedCrossRefGoogle Scholar
  45. Hilszczańska D, Sierota Z, Palenzona M (2008) New Tuber species found in Poland. Mycorrhiza 18:223–226PubMedCrossRefGoogle Scholar
  46. Huang JY, Hu HT, Shen WC (2009) Phylogenetic study of two truffles, Tuber formosanum and Tuber furfuraceum, identified from Taiwan. FEMS Microbiol Lett 294:157–171PubMedCrossRefGoogle Scholar
  47. Iotti M, Lancellotti E, Hall I et al (2010) The ectomycorrhizal community in natural Tuber borchii grounds. FEMS Microbiol Ecol 72:250–260PubMedCrossRefGoogle Scholar
  48. Iotti M, Leonardi M, Oddis M et al (2012a) Development and validation of a real time PCR assay for detection and quantification of Tuber magnatum in soil. BMC Microbiol 12:93PubMedPubMedCentralCrossRefGoogle Scholar
  49. Iotti M, Piattoni F, Zambonelli A (2012b) Techniques for host plant inoculation with truffles and other edible ectomycorrhizal mushrooms. In: Zambonelli A, Bonito G (eds) Edible ectomycorrhizal mushrooms. Soil Biol 34:145–161Google Scholar
  50. Iotti M, Rubini A, Tisserant E et al (2012c) Self/nonself recognition in Tuber melanosporum is not mediated by a heterokaryon incompatibility system. Fungal Biol 116:261–275PubMedCrossRefGoogle Scholar
  51. Iotti M, Leonardi M, Lancellotti E et al (2014) Spatio-temporal dynamic of Tuber magnatum mycelium in natural truffle grounds. PLoS One 9:e115921PubMedPubMedCentralCrossRefGoogle Scholar
  52. Iotti M, Piattoni F, Leonardi P et al (2016) First evidence for truffle production from plants inoculated with mycelial pure cultures. Mycorrhiza 26:793–798PubMedCrossRefGoogle Scholar
  53. Jeandroz S, Murat C, Wang Y et al (2008) Molecular phylogeny and historical biogeography of the genus Tuber, the “true truffles”. J Biogeogr 35:815–829CrossRefGoogle Scholar
  54. Kagan Zur V, Freeman S, Luzzati Y et al (2000) Emergence of the first black Périgord truffle (Tuber melanosporum) in Israel. Mycol Veg Mediterr 15:187–192Google Scholar
  55. Kinoshita A, Sasaki H, Nara K (2011) Phylogeny and diversity of Japanese truffles (Tuber spp.) inferred from sequences of four nuclear loci. Mycologia 103:779–794PubMedCrossRefGoogle Scholar
  56. Krpata D, Peintner U, Langer I et al (2008) Ectomycorrhizal communities associated with Populus tremula growing on a heavy metal contaminated site. Mycol Res 112:1069–1079PubMedCrossRefGoogle Scholar
  57. Lalli G, Leonardi M, Oddis M et al (2015) Expanding the understanding of a forest ectomycorrhizal community by combining root tips and fruiting bodies: a case study of Tuber magnatum stands. Turk J Bot 39:527–534CrossRefGoogle Scholar
  58. Lancellotti E, Iotti M, Zambonelli A et al (2014) Characterization of Tuber borchii and Arbutus unedo mycorrhizas. Mycorrhiza 24:481–486PubMedCrossRefGoogle Scholar
  59. Lanza B, Owczarek M, DeMarco A et al (2004) Evaluation of phytotoxicity and genotoxicity of substances produced by Tuber aestivum and distributed in the soil using Vicia faba root micronucleus test. Fresen Environ Bull 13:1410–1414Google Scholar
  60. Le Tacon F, Zeller B, Plain C et al (2013) Carbon transfer from the host to Tuber melanosporum mycorrhizas and ascocarps followed using a13C pulse-labeling technique. PLoS One 8:e64626PubMedPubMedCentralCrossRefGoogle Scholar
  61. Le Tacon F, Rubini R, Murat C et al (2016) Certainties and uncertainties about the life cycle of the perigord black truffle (Tuber melanosporum Vittad.) Ann For Sci 73:105–117CrossRefGoogle Scholar
  62. Lefevre C (2013) Native and cultivated truffles of North America. In: Zambonelli A, Bonito G (eds) Edible ectomycorrhizal mushrooms. Soil Biol 34:209–226Google Scholar
  63. Leonardi M, Iotti M, Oddis M et al (2013) Assessment of ectomycorrhizal fungal communities in the natural habitats of Tuber magnatum (Ascomycota, Pezizales). Mycorrhiza 23:349–358PubMedCrossRefGoogle Scholar
  64. Linde CC, Selmes H (2012) Genetic diversity and mating type distribution of Tuber melanosporum and their significance to truffle cultivation in artificially planted truffiéres in Australia. Appl Environ Microbiol 78:6534–6539PubMedPubMedCentralCrossRefGoogle Scholar
  65. Liu PG, Wang XH, Yu FQ et al (2003) Key taxa of larger members in higher fungi of biodiversity from China. Acta Bot Yunnan 25:285–296Google Scholar
  66. Lulli L, Pagliai M, Bragato G et al (1993) La combinazione dei caratteri che determinano il pedoambiente favorevole alla crescita del Tuber magnatum Pico nei suoli dei depositi marnosi dello Schlier in Acqualagna (Marche). Quad Sci Suolo 5:143–155Google Scholar
  67. Luo Q, Zhang J, Yan L et al (2011) Composition and antioxidant activity of water-soluble polysaccharides from Tuber indicum. J Med Food 14:1609–1616PubMedPubMedCentralCrossRefGoogle Scholar
  68. Marjanović Ž, Grebenc T, Marković M et al (2010) Ecological specificities and molecular diversity of truffles (genus Tuber) originating from mid-west of the Balkan Peninsula. Sydowia 62:67–87Google Scholar
  69. Marjanović Ž, Glišić A, Mutavdžić D et al (2015) Ecosystems supporting Tuber magnatum Pico production in Serbia experience specific soil environment seasonality that may facilitate truffle lifecycle completion. Appl Soil Ecol 95:179–190CrossRefGoogle Scholar
  70. Martin F, Kohler A, Murat C et al (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464:1033–1038PubMedCrossRefGoogle Scholar
  71. Mello A, Murat C, Vizzini A et al (2005) Tuber magnatum Pico, a species of limited geographical distribution: its genetic diversity inside and outside a truffleground. Environ Microbiol 7:55–65PubMedCrossRefGoogle Scholar
  72. Mello A, Miozzi L, Vizzini A et al (2010) Bacterial and fungal communities associated with Tuber magnatum-productive niches. Plant Biosyst 144:323–332CrossRefGoogle Scholar
  73. Mello A, Napoli C, Murat C et al (2011) ITS-1 versus ITS-2 pyrosequencing: a comparison of fungal populations in truffle-grounds. Mycologia 103:1184–1193PubMedCrossRefGoogle Scholar
  74. Mello A, Ding GC, Piceno YM et al (2013) Truffle brûlés have an impact on the diversity of soil bacterial communities. PLoS One 8:e61945PubMedPubMedCentralCrossRefGoogle Scholar
  75. Mello A, Lumini E, Napoli C et al (2015) Arbuscular mycorrhizal fungal diversity in the Tuber melanosporum brûlé. Fungal Biol 19:518–527CrossRefGoogle Scholar
  76. Menta C, García-Montero LG, Pinto S et al (2014) Does the natural “microcosm” created by Tuber aestivum affect soil microarthropods? A new hypothesis based on Collembola in truffle culture. Appl Soil Ecol 84:31–37CrossRefGoogle Scholar
  77. Molinier V, Bouffaud ML, Castel T et al (2013) Monitoring the fate of a 30-year-old truffle orchard in Burgundy: from Tuber melanosporum to Tuber aestivum. Agrofor Syst 87:1439–1449CrossRefGoogle Scholar
  78. Molinier V, Murat C, Frochot H et al (2015) Fine-scale spatial genetic structure analysis of the black truffle Tuber aestivum and its link to aroma variability. Environ Microbiol 17:3039–3050PubMedCrossRefGoogle Scholar
  79. Molinier V, Murat C, Peter M et al (2016) SSR-based identification of genetic groups within European populations of Tuber aestivum Vittad. Mycorrhiza 26:99–110PubMedCrossRefGoogle Scholar
  80. 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 245:307–313PubMedCrossRefGoogle Scholar
  81. Murat C, Zampieri E, Vizzini A et al (2008) Is the Perigord black truffle threatened by an invasive species? We dreaded it and it has happened! New Phytol 178:699–702PubMedCrossRefGoogle Scholar
  82. Murat C, Rubini A, Riccioni C et al (2013) Fine-scale spatial genetic structure of the black truffle (Tuber melanosporum) investigated with neutral microsatellites and functional mating type genes. New Phytol 199:176–187PubMedCrossRefGoogle Scholar
  83. Napoli C, Mello A, Borra A et al (2010) Tuber melanosporum, when dominant, affects fungal dynamics in truffle grounds. New Phytol 85:237–247CrossRefGoogle Scholar
  84. Orgiazzi A, Bianciotto V, Bonfante P et al (2013) 454 pyrosequencing analysis of fungal assemblages from geographically distant, disparate soils reveals spatial patterning and a core mycobiome. Diversity 51:73–98CrossRefGoogle Scholar
  85. Pacioni G (1991) Effects of Tuber metabolites on the rhizospheric environment. Mycol Res 95:1355–1358CrossRefGoogle Scholar
  86. Paolocci F, Rubini A, Riccioni C et al (2006) Reevaluation of the life cycle of Tuber magnatum. Appl Environ Microbiol 72:2390–2393PubMedPubMedCentralCrossRefGoogle Scholar
  87. Pérez F, Palfner G, Brunel N et al (2007) Synthesis and establishment of Tuber melanosporum Vitt. ectomycorrhizae on two Nothofagus species in Chile. Mycorrhiza 17:627–632PubMedCrossRefGoogle Scholar
  88. Pfister DH, Kimbrough JW (2001) Discomycetes. In: McLaughlin DJ, McLaughlin EG, Lemke PA (eds) The mycota VII Part A. Systematics and evolution. Springer, New York, Berlin, Heidelberg, pp 257–281Google Scholar
  89. Piattoni F, Ori F, Amicucci A et al (2016) Interrelationships between wild boars (Sus scrofa) and truffles. In Zambonelli A, Iotti M, Murat C (eds) True truffle (Tuber spp.) in the world. Soil Biol 47:375–389 (in press)Google Scholar
  90. Pinkas Y, Maimon M, Maimon E et al (2000) Inoculation, isolation and identification of Tuber melanosporum from old and new oak hosts in Israel. Mycol Res 104:472–477CrossRefGoogle Scholar
  91. Pruett G, Bruhn J, Mihail J (2008) Temporal dynamics of ectomycorrhizal community composition on root systems of oak seedlings infected with Burgundy truffle. Mycol Res 112:1344–1354PubMedCrossRefGoogle Scholar
  92. Pruett GE, Bruhn JN, Mihail JD (2009) Greenhouse production of Burgundy truffle mycorrhizae on oak roots. New For 37:43–52CrossRefGoogle Scholar
  93. Ratti C, Iotti M, Zambonelli A et al (2016) Mycoviruses infecting true truffles. In: Zambonelli A, Iotti M, Murat C (eds) True truffle (Tuber spp.) in the world. Soil Biol 47:333–349Google Scholar
  94. Reyna S, García Barreda S (2014) Black truffle cultivation: a global reality. For Syst 23:317–328Google Scholar
  95. Riccioni C, Belfiori B, Rubini A et al (2008) Tuber melanosporum outcrosses: analysis of the genetic diversity within and among its natural populations under this new scenario. New Phytol 180:466–478PubMedCrossRefGoogle Scholar
  96. Riousset L, Riousset G, Chevalier G et al (2001) Truffes d’Europe et de Chine. Institut National de la Recherche Agronomique INRA, ParisGoogle Scholar
  97. Rubini A, Belfiori B, Riccioni C et al (2011a) Isolation and characterization of MAT genes in the symbiotic ascomycete Tuber melanosporum. New Phytol 189:710–722PubMedCrossRefGoogle Scholar
  98. Rubini A, Belfiori B, Riccioni C et al (2011b) Tuber melanosporum: mating type distribution in a natural plantation and dynamics of strains of different mating types on the roots of nursery-inoculated host plants. New Phytol 189:723–735PubMedCrossRefGoogle Scholar
  99. Rubini A, Riccioni C, Belfiori B et al (2014) Impact of the competition between mating types on the cultivation of Tuber melanosporum: Romeo and Juliet and the matter of space and time. Mycorrhiza 24:19–27CrossRefGoogle Scholar
  100. Salerni E, D’Aguanno M, Leonardi P et al (2014a) Ectomycorrhizal communities above and below ground and truffle productivity in a Tuber aestivum orchard. For Syst 23:329–338Google Scholar
  101. Salerni E, Iotti M, Leonardi P et al (2014b) Effects of soil tillage on Tuber magnatum development in natural truffières. Mycorrhiza 24(Suppl 1):79–87CrossRefGoogle Scholar
  102. Selosse M-A, Faccio A, Scappaticci P et al (2004) Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal septomycetes, including truffles. Microbiol Ecol 47:416–426CrossRefGoogle Scholar
  103. Selosse M-A, Taschen E, Giraud T (2013) Do black truffles avoid sexual harassment by linking mating type and vegetative incompatibility? New Phytol 199:10–13PubMedCrossRefGoogle Scholar
  104. Shamekh S, Donnini D, Zambonelli A et al (2009) Wild Finnish truffles. Yunnan Zhiwu Yanjiu 16:69–71Google Scholar
  105. Shamekh S, Grebenc T, Leisola M et al (2014) The cultivation of oak seedlings inoculated with Tuber aestivum Vittad. in the boreal region of Finland. Mycol Prog 13:373–380CrossRefGoogle Scholar
  106. Song MS, Cao JZ, Yao YJ (2005) Occurrence of Tuber aestivum in China. Mycotaxon 91:75–80Google Scholar
  107. Splivallo R, Novero M, Bertea CM et al (2007) Truffle volatiles inhibit growth and induce an oxidative burst in Arabidopsis thaliana. New Phytol 175:3417–3424CrossRefGoogle Scholar
  108. Splivallo R, Ottonello S, Mello A et al (2011) Truffle volatiles: from chemical ecology to aroma biosynthesis. New Phytol 189:688–699PubMedCrossRefGoogle Scholar
  109. Staudenrausch S, Kaldorf M, Renker C (2005) Diversity of the ectomycorrhiza community at a uranium mining heap. Biol Fertil Soils 41:439–446CrossRefGoogle Scholar
  110. Stielow B, Menzel W (2010) Complete nucleotide sequence of TaV1, a novel totivirus isolated from a black truffle ascocarp (Tuber aestivum Vittad.). Arch Virol 155:2075–2078Google Scholar
  111. Stielow JB, Klenk HP, Menzel W (2011a) Complete genome sequence of the first endornavirus from the ascocarp of the ectomycorrhizal fungus Tuber aestivum Vittad. Arch Virol 156:343–345PubMedCrossRefGoogle Scholar
  112. Stielow B, Klenk HP, Winter S et al (2011b) A novel Tuber aestivum (Vittad.) mitovirus. Arch Virol 156:1107–1110PubMedCrossRefGoogle Scholar
  113. Stielow B, Bratek Z, Klenk HP et al (2012) A novel mitovirus from the hypogeous ectomycorrhizal fungus Tuber excavatum. Arch Virol 157:787–790PubMedCrossRefGoogle Scholar
  114. Stobbe U, Buntgen U, Sproll L et al (2012) Spatial distribution and ecological variation of re-discovered German truffle habitats. Fungal Ecol 5:591–599CrossRefGoogle Scholar
  115. Stobbe U, Egli S, Tegel W et al (2013a) Potential and limitations of Burgundy truffle cultivation. Mini-review. Appl Microbiol Biotechnol 97:5215–5224PubMedCrossRefGoogle Scholar
  116. Stobbe U, Stobbe A, Sproll L et al (2013b) New evidence for the symbiosis between Tuber aestivum and Picea abies. Mycorrhiza 23:669–673PubMedCrossRefGoogle Scholar
  117. Streiblová E, Gryndlerová H, Gryndler M (2012) Truffle brûlé: an efficient fungal life strategy. FEMS Microbiol Ecol 80:1–8PubMedCrossRefGoogle Scholar
  118. Taschen E, Sauve M, Taudiere A et al (2015) Whose truffle is this? Distribution patterns of ectomycorrhizal fungal diversity in Tuber melanosporum brûlés developed in multi-host Mediterranean plant communities. Environ Microbiol 17:2747–2761PubMedCrossRefGoogle Scholar
  119. Trappe JM, Claridge AW (2010) The hidden life of truffles. Sci Am 302:78–84PubMedCrossRefGoogle Scholar
  120. Turgeman T, Sitrit Y, Danai O et al (2012) Introduced Tuber aestivum replacing introduced Tuber melanosporum: a case study. Agrofor Syst 84:337–343CrossRefGoogle Scholar
  121. Urban A (2016) Truffles and small mammals. In: Zambonelli A, Iotti M, Murat C (eds) True truffle (Tuber spp.) in the world. Soil Biol 47:353–374Google Scholar
  122. Urban A, Neuner-Plattner I, Krisai-Greilhuber I et al (2004) Molecular studies on terricolous microfungi reveal novel anamorphs of two Tuber species. Mycol Res 108:749–758PubMedCrossRefGoogle Scholar
  123. Vahdatzadeh M, Deveau, Splivallo R (2015) The role of the microbiome of truffles in aroma formation: a meta-analysis approach. Appl Environ Microbiol 81:6946–6952PubMedPubMedCentralCrossRefGoogle Scholar
  124. Vasquez G, Gargano ML, Zambonelli A et al (2014) New distributive and ecological data on Tuber magnatum (Tuberaceae) in Italy. FL Mediterr 24:239–245Google Scholar
  125. Wang XH (2012) Truffle cultivation in China. In: Zambonelli A, Bonito G (eds) Edible ectomycorrhizal mushrooms. Soil Biol 34:227–240Google Scholar
  126. Wang Y, Tan ZM, Zhang DG et al (2006a) Phylogenetic and populational study of the Tuber indicum complex. Mycol Res 110:1034–1045PubMedCrossRefGoogle Scholar
  127. Wang Y, Tan ZM, Zhang DC et al (2006b) Phylogenetic relationships between Tuber pseudoexcavatum, a Chinese truffle, and other Tuber species based on parsimony and distance analysis of four different gene sequences. FEMS Microbiol Lett 259:269–281PubMedCrossRefGoogle Scholar
  128. Wang Y, Tan ZM, Murat C et al (2007) Molecular taxonomy of Chinese truffles belonging to the Tuber rufum and Tuber puberulum groups. Fungal Divers 24:301–328Google Scholar
  129. Wang Y, Peigui L, Chen J et al (2008) China–a newly emerging truffle-producing nation. In: Reynal B (ed) Actes du colloques la culture de la truffe dans le monde. Imprimerie Georges Lachaise, Brive-La-Gaillarde, pp 35–44Google Scholar
  130. Wang XH, Benucci GMN, Xie XD et al (2013) Morphological, mycorrhizal and molecular characterization of Finnish truffles belonging to the Tuber anniae species-complex. Fungal Ecol 6:269–280CrossRefGoogle Scholar
  131. Wedén K, Danell E, Camacho FJ et al (2004) The population of the hypogeous fungus Tuber aestivum syn. T. uncinatum on the island of Gotland. Mycorrhiza 14:19–23PubMedCrossRefGoogle Scholar
  132. Wedén C, Pettersson L, Danell E (2009) Truffle cultivation in Sweden: results from Quercus robur and Corylus avellana field trials on the island of Gotland. Scand J For Res 24:37–53CrossRefGoogle Scholar
  133. Yang MC (2001) Truffles in Southwest China. In: Corvoisier M, Olivier JM, Chevalier G (eds) Federation Française des trufficulteurs. Proceedings du Ve Congrès International Science et Culture de la Truffe, Aix-en-Provence, 4–6 Mars 1999. Paris, pp 248–249Google Scholar
  134. Zambonelli A, Iotti M (2001) Effects of fungicides on Tuber borchii and Hebeloma sinapizans ectomycorrhizas. Mycol Res 105:611–614CrossRefGoogle Scholar
  135. Zambonelli A, Tibiletti E, Pisi A (1997) Caratterizzazione anatomo-morfologica delle micorriza di Tuber indicum Cooke and Massee su Pinus pinea L. and Quercus cerris L. Micol Ital 1:29–36Google Scholar
  136. Zambonelli A, Iotti M, Rossi I et al (2000) Interactions between Tuber borchii and other ectomycorrhizal fungi in a field plantation. Mycol Res 104:698–702CrossRefGoogle Scholar
  137. Zambonelli A, Iotti M, Barbieri E et al (2009) The microbial communities and fruiting of edible ectomycorrhizal mushrooms. Yunnan Zhiwu Yanjiu 16:81–85Google Scholar
  138. Zambonelli A, Iotti M, Boutahir S et al (2012a) Ectomycorrhizal fungal communities of edible ectomycorrhizal mushrooms. In: Zambonelli A, Bonito G (eds) Edible ectomycorrhizal mushrooms, Soil Biol 34:105–124Google Scholar
  139. Zambonelli A, Iotti M, Piattoni F (2012b) Chinese Tuber aestivum sensu lato in Europe. Open Mycol J 6:22–26CrossRefGoogle Scholar
  140. Zambonelli A, Perini C, Pacioni G (2012c) Progetto MAGNATUM. Monitoraggio delle Attività di Gestione delle Tartufaie Naturali di Tuber magnatum. Risultati e consigli pratici. Alimat Edizioni CesenaGoogle Scholar
  141. Zambonelli A, Iotti M, Hall I (2015) Current status of truffle cultivation: recent results and future perspectives. Micol Ital 44:31–40Google Scholar
  142. Zampieri E, Murat C, Cagnasso M et al (2010) Soil analysis reveals the presence of an extended mycelial network in a Tuber magnatum truffle-ground. FEMS Microbiol Ecol 71:43–49PubMedCrossRefGoogle Scholar
  143. Zampieri E, Rizzello R, Bonfante P et al (2012) The detection of mating type genes of Tuber melanosporum in productive and non productive soils. Appl Soil Ecol 57:9–15CrossRefGoogle Scholar
  144. Zampieri E, Chiapello M, Daghino S et al (2016) Soil metaproteomics reveals an inter-kingdom stress response to the presence of black truffles. Sci Rep 6:25773PubMedPubMedCentralCrossRefGoogle Scholar
  145. Zhang JP, Liu PG, Chen J (2012) Tuber sinoaestivum sp. nov. an edible truffle from southwestern China. Mycotaxon 122:73–82CrossRefGoogle Scholar
  146. Zhao L, Wang K, Yang R et al (2012) Antioxidant activity of the water-soluble and alkali-soluble polysaccharides from Chinese Truffle Tuber sinense. J Anim Vet Adv 11:1753–1756CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Antonietta Mello
    • 1
    Email author
  • Elisa Zampieri
    • 2
    • 3
  • Alessandra Zambonelli
    • 4
  1. 1.Istituto per la Protezione Sostenibile delle Piante, SS Torino - CNRTorinoItaly
  2. 2.Dipartimento di Scienze Agrarie, Forestali e Alimentari (DISAFA)Università di TorinoGrugliascoItaly
  3. 3.Rice Research Unit, CREACouncil for Agricultural Research and EconomicsVercelliItaly
  4. 4.Dipartimento di Scienze Agrarie (DipSA)Alma Mater Studiorum Università di BolognaBolognaItaly

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