Advertisement

Mycorrhiza

, Volume 29, Issue 3, pp 219–226 | Cite as

New insights into black truffle biology: discovery of the potential connecting structure between a Tuber aestivum ascocarp and its host root

  • Aurélie DeveauEmail author
  • Philippe Clowez
  • François Petit
  • Jean-Paul Maurice
  • Flora Todesco
  • Claude Murat
  • Maryline Harroué
  • Julien Ruelle
  • François Le Tacon
Original Article

Abstract

According to isotopic labeling experiments, most of the carbon used by truffle (Tuber sp.) fruiting bodies to develop underground is provided by host trees, suggesting that trees and truffles are physically connected. However, such physical link between trees and truffle fruiting bodies has never been observed. We discovered fruiting bodies of Tuber aestivum adhering to the walls of a belowground quarry and we took advantage of this unique situation to analyze the physical structure that supported these fruiting bodies in the open air. Observation of transversal sections of the attachment structure indicated that it was organized in ducts made of gleba-like tissue and connected to a network of hyphae traveling across soil particles. Only one mating type was detected by PCR in the gleba and in the attachment structure, suggesting that these two organs are from maternal origin, leaving open the question of the location of the opposite paternal mating type.

Keywords

Truffle Tuber aestivum Ectomycorrhizae Symbiosis Fruiting body Anatomy Mating type 

Notes

Acknowledgments

We are very grateful to the two reviewers who have greatly improved the text.

Author contributions

Conceived and designed the work: FLT, AD. Contributed reagents/materials/analysis tools: AD, PC, FP, JPM, FT, MH, JR, CM. Analyzed the data: AD, FLT. Wrote the first draft: FLT. Edited manuscript: FLT, AD, CM. All authors read and commented on the manuscript.

Funding information

This work was funded by the Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems (ARBRE; ANR-11-LABX 0002 01).

References

  1. Antony-Babu S, Deveau A, Van Nostrand JD et al (2014) Black truffle-associated bacterial communities during the development and maturation of Tuber melanosporum ascocarps and putative functional roles. Environ Microbiol 16:2831–2847CrossRefGoogle Scholar
  2. Barry D, Callot G, Janex-Favre MC, Parguey-Leduc A., Pargney JC (1993) Morphologie et structure des hyphes externes observées sur le péridium des Tuber à écailles: évolution au cours du développement de l'ascocarpe . Canadian Journal of Botany 71 (4):609–619Google Scholar
  3. Barry D, Staunton S, Callot G (1994) Mode of the absorption of water and nutrients by ascocarps of Tuber melanosporum and Tuber aestivum. A radioactive tracer technique. Can J Bot 72:317–322CrossRefGoogle Scholar
  4. Callot G (1999) La truffe, la terre, la vie. INRA Ed, ParisGoogle Scholar
  5. De la Varga H, Le Tacon F, Lagoguet M et al (2017) Five years investigation of female and male genotypes in Périgord black truffle (Tuber melanosporum Vittad.) revealed contrasted reproduction strategies. Environ Microbiol 19:2604–2615CrossRefGoogle Scholar
  6. Duchaufour P, Bonneau M (1959) Une nouvelle méthode de dosage du phosphore assimilable dans les sols forestiers. Bull Assoc Fr Étude Sol 4:193–198Google Scholar
  7. Duddridge JA, Malibari A, Read DJ (1980) Structure and function of mycorrhizal rhizomorphs with special reference to their role in water transport. Nature 287:834–836CrossRefGoogle Scholar
  8. Le Tacon F (2017) Les truffes. Biologie, écologie, domestication. AgroParitech, NancyGoogle Scholar
  9. Le Tacon F, Zeller B, Plain C et al (2013) Carbon transfer from the host to Tuber melanosporum mycorrhizas and ascocarps followed using a 13C pulse-labeling technique. PLoS One 8:e64626CrossRefGoogle Scholar
  10. Le Tacon F, Rubini A, Murat C et al (2015) Certainties and uncertainties about the life cycle of the Périgord black truffle (Tuber melanosporum Vittad.). Ann For Sci 73:105–117CrossRefGoogle Scholar
  11. Metson, A.J., 1956. Methods of chemical analysis for soil survey samples. NZ Soil Bur Bull n°12Google Scholar
  12. Molinier V, Bouffaud M-L, Castel T, Mounier A, Colombet A, Recorbet G, Frochot H, Wipf D (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
  13. Molinier V, Murat C, Frochot H, Wipf D, Splivallo R (2015) Fine-scale spatial genetic structure analysis of the black truffle Tuber aestivum and its link to aroma variability. Environ Microbiol 17:3039–3050CrossRefGoogle Scholar
  14. Molinier V, Peter M, Stobbe U, Egli S (2016) The Burgundy truffle (Tuber aestivum syn. uncinatum): a truffle species with a wide habitat range over Europe. In: A Zambonelli, M Iotti & CM (ed) True truffle (Tuber spp.) world. Soil Ecol Syst Biochem Springer, pp 33–47Google Scholar
  15. Murat C (2015) Forty years of inoculating seedlings with truffle fungi: past and future perspectives. Mycorrhiza 25:77–81CrossRefGoogle Scholar
  16. 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 199:176–187CrossRefGoogle Scholar
  17. Robinson JBD (1967) Soil particle-size fractions and nitrogen mineralization. J Soil Sci 18:109–117CrossRefGoogle Scholar
  18. Rouquerolle T, Payre H (1975) Conséquences de quelques particularités biologiques des Tuber sur les caractères des cultures de mycélium et sur la formation des truffes. Rev Mycol 29:213–224Google Scholar
  19. Stobbe U, Egli S, Tegel W, Peter M, Sproll L, Büntgen U (2013) Potential and limitations of Burgundy truffle cultivation. Appl Microbiol Biotechnol 97:5215–5224CrossRefGoogle Scholar
  20. Taschen E, Rousset F, Sauve M, Benoit L, Dubois MP, Richard F, Selosse MA (2016) How the truffle got its mate: insights from genetic structure in spontaneous and planted Mediterranean populations of Tuber melanosporum. Mol Ecol 25:5611–5627CrossRefGoogle Scholar
  21. Teramoto M, Wu B, Hogetsu T (2012) Transfer of 14C-photosynthate to the sporocarp of an ectomycorrhizal fungus Laccaria amethystina. Mycorrhiza 22:219–225CrossRefGoogle Scholar
  22. Zarivi O, Cesare P, Ragnelli AM, Aimola P, Leonardi M, Bonfigli A, Colafarina S, Poma AM, Miranda M, Pacioni G (2015) Validation of reference genes for quantitative real-time PCR in Périgord black truffle (Tuber melanosporum) developmental stages. Phytochemistry 116:78–86.  https://doi.org/10.1016/j.phytochem.2015.02.024 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Institut national de la recherche agronomique (INRA)Unité Mixte de Recherche 1136 INRA-Université de Lorraine, Interactions Arbres/MicroorganismesChampenouxFrance
  2. 2.Pont-l’EvêqueFrance
  3. 3.FleurinesFrance
  4. 4.Groupe mycologique VosgienNeufchâteauFrance
  5. 5.Institut national de la recherche agronomique (INRA)Unité Mixte de Recherche 1137 INRA-Université de LorraineChampenouxFrance

Personalised recommendations