Skip to main content

Soil spore bank in Tuber melanosporum: up to 42% of fruitbodies remain unremoved in managed truffle grounds

Abstract

Fungi fruiting hypogeously are believed to form spore banks in soil especially because some fruitbodies are not removed by animals. However, little is known on the proportion of fruitbodies that are not removed by animals. We took advantage of the brûlé phenomenon, which allows delineation of the mycelium distribution, to assess the proportion of unremoved black truffle (Tuber melanosporum) fruitbodies in the context of plantations where fruitbodies are actively sought and harvested by truffle growers. We inspected portions of the brûlés after the harvest season to find unremoved fruitbodies. On average, from six truffle grounds in which a total of 38 brûlés were investigated, unremoved fruitbodies represented 33% of the whole fruitbody production (42% when averaging all the brûlés). We discuss this value and its high variability among truffle grounds. Beyond the local and variable accidental reasons that may lead to this high proportion, we speculate that the formation of some undetectable fruitbodies may be under selection pressure, given the reproductive biology of T. melanosporum.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Bertault G, Rousset F, Fernandez D, Berthomieu A, Hochberg ME, Callot G, Raymond M (2001) Population genetics and dynamics of the black truffle in a man-made truffle field. Heredity 86:451–458

    CAS  Article  Google Scholar 

  2. Bonito G, Smith ME, Brenneman T, Vilgalys R (2012) Assessing ectomycorrhizal fungal spore banks of truffle producing soils with pecan seedling trap-plants. Plant Soil 356:357–366

    CAS  Article  Google Scholar 

  3. Bruns TD, Peay KG, Boynton PJ, Grubisha LC, Hynson NA, Nguyen NH, Rosenstock NP (2009) Inoculum potential of Rhizopogon spores increases with time over the first 4 yr of a 99-yr spore burial experiment. New Phytol 181:463–470

    Article  Google Scholar 

  4. Callot G (1999) La Truffe, la Terre, la Vie. Editions Quae, Paris

    Google Scholar 

  5. Colgan W, Claridge AW (2002) Mycorrhizal effectiveness of Rhizopogon spores recovered from faecal pellets of small forest-dwelling mammals. Myc Res 106:314–320

    Article  Google Scholar 

  6. De la Varga H, Le Tacon F, Lagoguet M, Todesco F, Varga T, Miquel I, Barry-Etienne D, Robin C, Halkett F, Martin F, Murat C (2017) Five years investigation of female and male genotypes in périgord black truffle (Tuber melanosporum Vittad.) revealed contrasted reproduction strategies. Environ Microbiol 19:2604–2615

    Article  Google Scholar 

  7. Douhan G, Vincenot L, Gryta H, Selosse MA (2011) Population genetics of ectomycorrhizal fungi: from current knowledge to emerging directions. Fungal Biol 115:569–597

    Article  Google Scholar 

  8. Dunham SM, Mujic AB, Spatafora JW, Kretzer AM (2013) Within-population genetic structure differs between two sympatric sister-species of ectomycorrhizal fungi, Rhizopogon vinicolor and R vesiculosus. Mycologia 105:814–826

    Article  Google Scholar 

  9. Glassman SI, Peay KG, Talbot JM, Smith DP, Chung JA, Taylor JW, Vilgalys R, Bruns TD (2015) A continental view of pine-associated ectomycorrhizal fungal spore banks: a quiescent functional guild with a strong biogeographic pattern. New Phytol 205:1619–1631

    CAS  Article  Google Scholar 

  10. Imbert E (2002) Ecological consequences and ontogeny of seed heteromorphism. Perspect Plant Ecol Evol Syst 5:13–36

    Article  Google Scholar 

  11. Kjøller R, Bruns TD (2003) Rhizopogon spore bank communities within and among California pine forests. Mycologia 95:603–613

    Article  Google Scholar 

  12. Kretzer AM, Dunham S, Molina R, Spatafora JW (2005) Patterns of vegetative growth and gene flow in Rhizopogon vinicolor and R. vesiculosus (Boletales, Basidiomycota). Mol Ecol 14:2259–2268

    CAS  Article  Google Scholar 

  13. Le Tacon F (2017) Les truffes. Biologie, écologie et domestication. AgroParisTech, Nancy

    Google Scholar 

  14. Murat C (2015) Forty years of inoculating seedlings with truffle fungi: past and future perspectives. Mycorrhiza 25:77–81

    Article  Google Scholar 

  15. Murat C, Rubini A, Riccioni C, De la Varga H, Akroume E, Belfiori B, Guaragno M, Le Tacon F, Robin C, Halkett F, Martin F, Paolocci F (2013) Fine-scale spatial genetic structure of the black truffle (Tuber melanosporum) investigated with neutral microsatellites and functional mating type genes. New Phytol 199:176–187

    CAS  Article  Google Scholar 

  16. Murat C, Bonneau L, De La Varga H, Olivier JM, Sandrine F, Le Tacon F (2016) Trapping truffle production in holes: a promising technique for improving production and unravelling truffle life cycle. Italian J Mycol 45:47–53

    Google Scholar 

  17. Murata M, Nagata Y, Nara K (2017) Soil spore banks of ectomycorrhizal fungi in endangered Japanese Douglas-fir forests. Ecol Res 32:469–479

    Article  Google Scholar 

  18. Riccioni C, Belfiori B, Rubini A, Passeri V, Arcion S, Paolocci F (2008) Tuber melanosporum outcrosses: analysis of the genetic diversity within and among its natural populations under this new scenario. New Phytol 180:466–478

    CAS  Article  Google Scholar 

  19. Schneider-Maunoury L, Clément C, Coves H, Lambourdière J, Leclercq S, Richard F, Selosse M-A, Taschen E (2018) Is Tuber melanosporum colonizing the roots of herbaceous, non-ectomycorrhizal plants? Fungal Ecol 31:59–68

    Article  Google Scholar 

  20. Schneider-Maunoury L, Deveau A, Moreno M, Todesco F, Murat C, Courty P-E, Jakalski M, Selosse M-A (2019). Two ectomycorrhizal truffles, Tuber melanosporum and T. aestivum, colonize endophytically roots of non-ectomycorrhizal plant in natural environments. New Phytol, in press

  21. Selosse M-A, Taschen E, Giraud T (2013) Do black truffles avoid sexual harassment by linking mating type and vegetative incompatibility? New Phytol 199:10–13

    Article  Google Scholar 

  22. Selosse M-A, Schneider-Maunoury L, Taschen E, Rousset F, Richard F (2017) Black truffle, a hermaphrodite with forced unisexual behaviour. Trends Microbiol 25:784–787

    CAS  Article  Google Scholar 

  23. Séne S, Selosse M-A, Forget M, Lambourdière J, Cissé K, Diédhiou AG, Rivera-Ocasio E, Kodja H, Kameyama N, Nara K, Vincenot L, Mansot J-L, Weber J, Roy M, Sylla SN, Bâ A (2018) A pantropically introduced tree is followed by specific ectomycorrhizal symbionts due to pseudo-vertical transmission. ISME J 12:1806–1816

    Article  Google Scholar 

  24. Splivallo R, Ottonello S, Mello A, Karlovsky P (2011) Truffle volatiles: from chemical ecology to aroma biosynthesis. New Phytol 189:688–699

    CAS  Article  Google Scholar 

  25. Splivallo R, Valdez N, Kirchhoff N, Ona MC, Schmidt JP, Feussner I, Karlovsky P (2012) Intraspecific genotypic variability determines concentrations of key truffle volatiles. New Phytol 194:823–835

    CAS  Article  Google Scholar 

  26. Streiblová E, Gryndlerová H, Gryndler M (2012) Truffle brûlé: an efficient fungal life strategy. FEMS Microbiol Ecol 80:1–8

    Article  Google Scholar 

  27. Taschen E, Rousset F, Sauve M, Benoit L, Dubois M-P, Richard F, Selosse M-A (2016) How the truffle got its mate: insights from genetic structure in spontaneous and planted Mediterranean populations of Tuber melanosporum. Mol Ecol 25:5611–5627

    CAS  Article  Google Scholar 

  28. Urban A (2017) Truffles and small mammals. In: Zambonelli A, Iotti M, Murat C (eds) True truffle (Tuber spp.) in the world. Springer, Berlin, pp 353–373

    Google Scholar 

  29. Vašutová M, Mleczko P, López-García A, Maček I, Boros G, Ševčík J, Fujii S, Hackenberger D, Tuf IH, Hornung E, Páll-Gergely, Kjøller R (2019) Taxi drivers: the role of animals in transporting mycorrhizal fungi. Mycorrhiza in press

    Article  Google Scholar 

  30. Vincenot L, Selosse M-A (2017). Population biology and ecology of ectomycorrhizal fungi. Ecol Studies 230:39–59

Download references

Acknowledgments

We are very grateful to Lucien Bonneau, Francis Caulet, Jean-Paul Laurents, Lucien Romieu, Patrick Savary, and Jean-François Tourette for having carried out the protocol on, or given access to, their truffle ground. We thank Dominique Barry-Etienne and Claude Murat for information on truffle fruitbody decomposition in soil, David Marsh for English corrections, two anonymous referees and Jan Colpaert for insightful comments on earlier versions of this paper, and Lucien Bonneau for providing pictures of the experiment (supplementary figure S1).

Author information

Affiliations

Authors

Contributions

LSM and MAS designed the study, contributed a new spore bank evaluation method, analyzed the data, and wrote the paper. All authors performed the research and improved the manuscript.

Corresponding author

Correspondence to Marc-André Selosse.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Figure S1.

Search for unremoved T. melanosporum fruitbodies at the end of the harvest season. (a) Delineation of a 30 × 30 cm surface, arbitrarily located. (b) Digging of a well to harvest the unremoved fruitbodies. (c) Five unremoved fruitbodies. Courtesy Lucien Bonneau. Figure S2. Number of unremoved fruitbodies per square meter is not correlated with the number of harvested truffles per square meter. (A) all brûlés (linear regression model, P = 0.17); (B) all truffle grounds (linear regression model, P = 0.46). (PDF 235 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Schneider-Maunoury, L., Taschen, E., Richard, F. et al. Soil spore bank in Tuber melanosporum: up to 42% of fruitbodies remain unremoved in managed truffle grounds. Mycorrhiza 29, 663–668 (2019). https://doi.org/10.1007/s00572-019-00912-3

Download citation

Keywords

  • Ascomycetes life cycle
  • Brûlé
  • Mycorrhizae
  • Spore dispersal