Skip to main content
SpringerLink
Log in

Diversity of ectomycorrhizal Thelephoraceae in Tuber melanosporum-cultivated orchards of Northern Spain

  • Original Article
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Truffles are edible hypogeous ascomycetes highly appreciated worldwide, especially the black truffle (Tuber melanosporum Vittad.). In recent decades, the cultivation of the black truffle has expanded across the Mediterranean climate regions in and outside its native range. Members of the Thelephoraceae (Thelephorales, Agaricomycetes, Basidiomycota) are commonly found in truffle plantations, but their co-occurrence with Tuber species and other members of the fungal community has been scarcely reported. Thelephoraceae is one of the most represented families of the ectomycorrhizal fungal community in boreal and Mediterranean forests. To reveal the diversity of these fungi in T. melanosporum-cultivated plantations, ten orchards located in the Navarra region (Northern Spain) were surveyed for 2 years. Morphological and molecular approaches were used to detect and identify the Thelephoraceae ectomycorrhizas present in those plantations. Ten different mycorrhizal types were detected and described. Four of them were morphologically identified as Tomentella galzinii, Quercirhiza cumulosa, Q. squamosa, and T39 Thelephoraceae type. Molecular analyses revealed 4–6 operational taxonomic units (OTUs), depending on the nucleotide database used, but similarities remained under 95 % and no clear species assignments could be done. The results confirm the diversity and abundance of this fungal family in the ectomycorrhizal community of black truffle plantations, generally established in Mediterranean areas. The occurrence and relative abundance of Thelephoraceae ectomycorrhizas is discussed in relation to their possible influence on truffle production.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abarenkov K, Kõljalg U, Suvi T, Jairus T, Saar I, Tedersoo L (2008) High global diversity of Tomentella and Thelephora (Thelephorales, Basidiomycota). 21st New Phytologist Symposium. The ecology of ectomycorrhizal fungi. Montpellier (France)

  • Agerer R (1986) Studies on ectomycorrhizae II. Introducing remarks on characterization and identification. Mycotaxon 26:473–492

  • Agerer R (ed) (1987–2012) Colour atlas of ectomycorrhizae. 1st–15th delivery, Einhorn-Verlag + Druck GmbH, Schwäbisch Gmünd

  • Agerer R (1994a) Pseudotomentella tristis (Thelephoraceae). Eine Analyse von Fruchtkörper und Ektomykorrhizen. Z Mykol 60:143–158

    Google Scholar 

  • Agerer R (1994b) Pseudotomentella tristis. In: Agerer R (ed) Colour atlas ot ectomycorrhizae, plate 84. Einhorn-Verlag, Sshwäbisch Gmünd

    Google Scholar 

  • Agerer R (1999) Never change a functionally successful principle: the evolution of Boletales s.l. (Hymenomycetes, Basidiomycotina) as seen from below-ground features. Sendtnera 6:5–91

    Google Scholar 

  • Agerer R (2001) Exploration types of ectomycorrhizae. A proposal to clasify ectomycorrhizal mycelial systems according to their patterns of differentiation and putative ecological importance. Mycorrhiza 11:107–114. doi:10.1007/s005720100108

    Article  Google Scholar 

  • Agerer R (2006) Fungal relationships and structural identity of their ectomycorrhizae. Mycol Prog 5:67–107. doi:10.1007/s11557-006-0505-x

    Article  Google Scholar 

  • Agerer R, Danielson RM, Egli S, Ingleby K, Luoma D, Treu R (1996–2008) Descriptions of ectomycorrhizae. 1st-12th del., Einhorn-Verlag + Druck GmbH, Schwäbisch Gmünd

  • Águeda B, Fernández-Toirán LM, De Miguel AM, Martínez-Peña F (2010) Ectomycorrhizal status of a mature productive black truffle plantation. For Syst 19:89–97

    Google Scholar 

  • Baciarelli-Falini L, Rubini A, Riccioni C, Paolocci F (2006) Morphological and molecular analyses of ectomycorrhizal diversity in a man-made Tuber melanosporum plantation: description of novel truffle-like morphotypes. Mycorrhiza 16:475–484. doi:10.1007/s00572-006-0066-5

    Article  PubMed  Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2005) GenBank. Nucleic Acids Res 33:D34–D38

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benucci GMN, Raggi L, Alberini E, Grebenc T, Bencivenga M, Falcinelli M, Di Massimo G (2011) Ectomycorrhizal communities in a productive Tuber aestivum Vittad. orchard: composition, host influence and species replacement. FEMS Microbiol Ecol 76:170–184

    Article  CAS  PubMed  Google Scholar 

  • Benucci GMN, Raggi L, Albertini E, Gógán Csorbai A, Donnini D (2014) Assessment of ectomycorrhizal biodiversity in Tuber macrosporum productive sites. Mycorrhiza 24:281–292

    Article  PubMed  Google Scholar 

  • Binder A, Peršoh D, Yorou NS, Verma R, Bässler C, Agerer R (2013) Ectomycorrhizae of Tomentella badia: description and molecular identification. Acta Mycol 48:155–171

    Article  Google Scholar 

  • Clavería V (2007) Estudio de la comunidad ectomicorrícica de un bosque maduro de Quercus ilex subsp. ballota, su caracterización y dinámica espacio-temporal. Doctoral dissertation, University of Navarra

  • Dämmrich F (2004–2015) Tomentella and related genera. Online-key for European species of tomentelloid fungi: (with special regard of distribution in Germany) http://www.tomentella.de/Pages/index_e.htm

  • Danielson RM, Pruden M (1989) The ectomycorrhizal status of urban spruce. Mycologia 81:335–341

    Article  Google Scholar 

  • Danielson RM, Zak JC, Parkinson D (1984) Mycorrhizal inoculum in a peat deposit formed under a white spruce stand in Alberta. Can J Bot 63:2557–2560

    Article  Google Scholar 

  • De Miguel AM, Sáez R (2005) Algunas micorrizas competidoras de plantaciones truferas. Pub Biol Univ Nav Serie Botánica 16:1–18

    Google Scholar 

  • De Miguel AM, De Román M, Etayo ML (2001) Mycorrhizal fungi competing with Tuber melanosporum Vitt. in cultivated truffle beds in NE Spain. Proceedings of the II International Workshop on Edible Mycorrhizal Mushrooms, Christchurch, New Zealand

  • De Miguel AM, Parladé J, Águeda B, Pera J, González-Armada B, Sáez R (2011) Thelephoroid ectomycorrhizae in black truffle plantations. In: Sixth International Workshop on Edible Mycorrhizal Mushrooms (IWEMM6). Rabat, Morocco

  • De Miguel AM, Águeda B, Sánchez S, Parladé J (2014) Ectomycorrhizal fungus diversity and community structure with natural and cultivated truffle hosts: applying lessons learned to future truffle culture. Mycorrhiza 24:S5–S18. doi:10.1007/s00572-013-0554-3

    Article  PubMed  Google Scholar 

  • De Román M, De Miguel AM (2005) Post-fire, seasonal and annual dynamics of the ectomycorrhizal community in a Quercus ilex L. forest over a 3-year period. Mycorrhiza 15:471–482. doi:10.1007/s00572-005-0353-6

    Article  PubMed  Google Scholar 

  • De Román M, Agerer R, De Miguel AM (2002) Quercirhiza cumulosa + Quercus ilex L. subsp. ballota (Desf.) Samp. Descr Ectomyc 6:13–18

    Google Scholar 

  • De Román M, Clavería V, De Miguel AM (2005) A revision of the descriptions of ectomycorrhizas published since 1961. Mycol Res 109:1063–1104

    Article  PubMed  Google Scholar 

  • Duddridge JA, Malibari A, Read DJ (1980) Structure and function of mycorrhizal rhizomorphs with special reference to their role in water transport. Nature 287:834–836

    Article  Google Scholar 

  • Erland S, Taylor AFS (1999) Resupinate ectomycorrhizal Fungi. In: Cairney JWG, Chambers SM (eds) Ectomycorrhizae fungi: key genera in profile. Springer, Berlin, pp 347–364

    Chapter  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for Basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Giraud M (1988) Prélèvement et analyse de mycorrhizas. In: Parra C (ed) CTIFL – La truffe. FNPT, Paris, pp 49–63

    Google Scholar 

  • González-Armada B, De Miguel AM, Cavero RY (2010a) Ectomycorrhizae and vascular plants growing in brulés as indicators of below and above ground microecology of black truffle production areas in Navarra (Northern Spain). Biodivers Conserv 19:3861–3891

    Article  Google Scholar 

  • González-Armada B, De Miguel AM, Cavero RY (2010b) Estudio de la flora vascular y la micobiota micorrícica en quemados truferos de Navarra (España). Atti 3°Congresso Internazionale di Spoleto sul tartufo, pp 152–162

  • Gregori G, Lo Bue G, Maggiorotto G (1990) Caratterizzazione di ectomicorrize in tartufaie naturali e di impianto e valutazione della loro competitivitá nei confronti di Tuber magnatum. Atti del Secondo Congresso Internazionale di Spoleto sul Tartufo, pp 219–246

  • Iotti M, Lancellotti E, Hall I, Zambonelli A (2010) The ectomycorrhizal community in natural Tuber borchii grounds. FEMS Microbiol Ecol 72:250–260. doi:10.1111/j.1574-6941.2010.00844.x

    Article  CAS  PubMed  Google Scholar 

  • Jakucs E, Erős-Honti Z (2008) Morphological-anatomical characterization and identification of Tomentella ectomycorrhizas. Mycorrhiza 18:277–285. doi:10.1007/s00572-008-0183-4

    Article  PubMed  Google Scholar 

  • Jakucs E, Kovács GM, Szedlay G, Erős-Honti Z (2005) Morphological and molecular diversity and abundance of tomentelloid ectomycorrhizae in broad-leaved forest of the Hungarian Plain. Mycorrhiza 15:459–470

    Article  PubMed  Google Scholar 

  • Jakucs E, Erős-Honti Z, Seress D, Kovács GM (2015) Enhancing our understanding of anatomical diversity in Tomentella ectomycorrhizas: characterization of six new morphotypes. Mycorrhiza 25:419–429. doi:10.1007/s00572-014-0622-3

    Article  PubMed  Google Scholar 

  • Kennedy P (2010) Ectomycorrhizal fungi and interspecific competition: species interactions, community structure, coexistence mechanisms, and future research directions. New Phytol 187:895–910. doi:10.1111/j.1469-8137.2010.03399.x

    Article  PubMed  Google Scholar 

  • Kõljalg U (1996) Tomentella (Basidiomycota) and related genera in temperate Eurasia. Synopsis Fungorum 9. Fungiflora, Oslo

    Google Scholar 

  • Kõljalg U, Dahlberg A, Taylor AFS, Larsson E, Hallenberg N, Stenlid J, Larsson KH, Fransson PMA, Kårén O, Jonsson L (2000) Diversity and abundance of resupinate thelephoroid fungi as ectomycorrhizal symbionts in Swedish boreal forests. Mol Ecol 9:1985–1996. doi:10.1046/j.1365-294X.2000.01105.x

    Article  PubMed  Google Scholar 

  • Kõljalg U, Jakucs E, Bóka K, Agerer R (2001) Three ectomycorrhiza with cystidia formed by different Tomentella species as revealed by rDNA ITS sequences and anatomical characteristics. Folia Cryptog Estonica 30:27–39

    Google Scholar 

  • Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Tellería MT, Weiß M, Larsson K-H (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22:5271–5277

    Article  PubMed  Google Scholar 

  • Lee SS, Thi BK, Patahayah M (2010) An ectomycorrhizal thelephoroid fungus of Malaysian dipterocarp seedlings. J Trop For Sci 22:355–363

    Google Scholar 

  • Leonardi M, Iotti M, Oddis M, Lalli G, Pacioni G, Leonardi P, Maccherini S, Perini C, Salerni E, Zambonelli A (2013) Assessment of ectomycorrhizal fungal communities in the natural habitats of Tuber magnatum (Ascomycota, Pezizales). Mycorrhiza 23:349–358

    Article  CAS  PubMed  Google Scholar 

  • Mello A, Napoli C, Murat C, Morin E, Marceddu G, Bonfante P (2011) ITS-1 versus ITS-2 pyrosequencing: a comparison of fungal populations in truffle grounds. Mycologia 103:1184–1193

    Article  CAS  PubMed  Google Scholar 

  • Melo I, Salcedo I, Tellería MT, Blanco M, Illana C (2004) Bases corológicas de Flora Micológica Ibérica Adiciones y números 2179–2238. Cuad Trab Flora Micol Ibérica 20:15–56

    Google Scholar 

  • Melo I, Salcedo I, Tellería MT (2006) Contribution to the knowledge of tomentelloid fungi in the Iberian Peninsula. V. Nova Hedwigia 82:167–187

    Article  Google Scholar 

  • Miller OK (1982) Taxonomy of ecto- and ectendomycorrhizal fungi. In: Schenck NC (ed) Methods and principles of mycorrhzial research. The American Phytopatological Society, St Paul Minn, pp 91–101

    Google Scholar 

  • 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 245:307–313. doi:10.1016/j.femsle.2005.03.019

    Article  CAS  PubMed  Google Scholar 

  • Napoli C, Mello A, Borra A, Vizzini A, Sourzat P, Bonfante P (2010) Tuber melanosporum, when dominant, affects fungal dynamics in truffle grounds. New Phytol 185:237–247. doi:10.1111/j.1469-8137.2009.03053.x

    Article  CAS  PubMed  Google Scholar 

  • Otsing E, Tedersoo L (2015) Temporal dynamics of ectomycorrhizal fungi and persistence of Tuber melanosporum in inoculated Quercus robur seedlings in North Europe. Mycorrhiza 25(1):61–66. doi:10.1007/s00572-014-0591-6

    Article  PubMed  Google Scholar 

  • Palfner G (1995) Quercirhiza squamosa + Quercus. In: Agerer R (ed) Colour atlas of ectomycorrhizae, plate 86

  • Palfner G, Agerer R (1996) “Quercirhiza squamosa” eine nichtidentifizierte Ektomykorrhiza an Quercus robur. Sendtnera 3:137–145

    Google Scholar 

  • Peay K, Kennedy P, Bruns T (2008) Fungal community ecology: a hybrid beast with a molecular master. Bioscience 58:799–810

    Article  Google Scholar 

  • Peintner U, Dämmrich F (2012) Tomentella alpina and other tomentelloid taxa fruiting in a glacier valley. Mycol Prog 11:109–119

    Article  Google Scholar 

  • Pigott CD (1982) Survival of mycorrhiza formed by Cenococcum geophilum Fr. in dry soils. New Phytol 92:513–517

    Article  Google Scholar 

  • 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 112:1344–1354

    Article  PubMed  Google Scholar 

  • Reyna S, García-Barreda S (2014) Black truffle cultivation: a global reality. For Syst 23:317–328

    Google Scholar 

  • Richard F, Millot S, Gardes M, Selosse MA (2005) Diversity and specificity of ectomycorrhizal fungi retrieved from an old-growth Mediterranean forest dominated by Quercus ilex. New Phytol 166:1011–1023

    Article  CAS  PubMed  Google Scholar 

  • Salerni E, D’Aguanno M, Leonardi P, Perini C (2014) Ectomycorrhizal communities above and below ground and truffle productivity in a Tuber aestivum orchard. For Syst 23:329–338

    Google Scholar 

  • Sánchez S (2012) Ectomicorrizas en el cultivo de trufa negra: ecología, diversidad y gestión. Doctoral dissertation, University of Zaragoza

  • Sánchez S, Ágreda T, Águeda B, Martín M, de Miguel AM, Barriuso J (2014) Persistence and detection of black truffle ectomycorrhizas in plantations: comparison between two field detection methods. Mycorrhiza 24:S39–S46. doi:10.1007/s00572-014-0560-0

    Article  PubMed  Google Scholar 

  • Shiryaev A (2008) Diversity and distribution of thelephoroid fungi (Basidiomycota, Thelephorales) in the Sverdlovsk region, Russia. Folia Cryptogamica Estonica 44:131–141

    Google Scholar 

  • Suvi T, Tedersoo L, Abarenkov K, Beaver K, Gerlach J, Kõljalg U (2010) Mycorrhizal symbionts of Pisonia grandis and P. sechellarum in Seychelles: identification of mycorrhizal fungi and description of new Tomentella species. Mycologia 102:522–533. doi:10.3852/09-147

    Article  PubMed  Google Scholar 

  • Suz LM, Martín MP, Fischer CR, Bonet JA, Colinas C (2010) Can NPK fertilizers enhance seedling growth and mycorrhizal status of Tuber melanosporum-inoculated Quercus ilex seedlings? Mycorrhiza 20:349–360. doi:10.1007/s00572-009-0289-3

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tellería MT (1980) Contribución al estudio de los Aphyllophorales españoles. J Cramer Bibliotheca Mycol 74

  • Wei J, Agerer R (2010) Three Ectomycorrhizae of Thelephoraceae on Chinese Pine (Pinus tabulaeformis) and a key to thelephoroid Ectomycorrhizae. Nova Hedwigia 91:165–186

    Article  Google Scholar 

  • White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols. A guide to methods and applications. Academic Press, London, pp 315–322

    Google Scholar 

  • Yorou NS, Diabate M, Agerer R (2012a) Phylogenetic placement and anatomical characterisation of two new West African Tomentella (Basidiomycota, Fungi) species. Mycol Prog 11:171–180

    Article  Google Scholar 

  • Yorou NS, Gardt S, Guissou ML, Diabaté M, Agerer R (2012b) Three new Tomentella species from West Africa identified by anatomical and molecular data. Mycol Prog 11:449–462

    Article  Google Scholar 

Download references

Acknowledgments

Authors would like to thank Navarra’s truffle plantation owners for their invaluable collaboration through the years. This study was supported by Gobierno de Navarra—Educación (2005 Project) and the Spanish Ministry of Economy MINECO project AGL 2012-40035-C03.

Author information

Authors and Affiliations

  1. Departamento de Biología Ambiental, Universidad de Navarra, 31008, Pamplona, Spain

    Ana María De Miguel

  2. Área de Botánica, Departamento de Ciencias Agroforestales, EU de Ingenierías Agrarias, Universidad de Valladolid, Campus Duques de Soria, 42004, Soria, Spain

    Beatriz Águeda

  3. INTIA, Avda. Serapio Huici 22, 31610, Villava, Navarra, Spain

    Raimundo Sáez

  4. IRTA, Centre de Cabrils, Ctra. Cabrils km. 2, 08348, Cabrils, Barcelona, Spain

    Javier Parladé

  5. Unidad de Recursos Forestales, Centro de Investigación y Tecnología Agroalimentaria de Aragón (CITA), Instituto Agroalimentario de Aragón – IA2 (CITA-Universidad de Zaragoza), Avenida de Montañana 930, 50059, Zaragoza, Spain

    Sergio Sánchez

Authors
  1. Ana María De Miguel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Beatriz Águeda
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Raimundo Sáez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sergio Sánchez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Javier Parladé
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Javier Parladé.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

De Miguel, A.M., Águeda, B., Sáez, R. et al. Diversity of ectomycorrhizal Thelephoraceae in Tuber melanosporum-cultivated orchards of Northern Spain. Mycorrhiza 26, 227–236 (2016). https://doi.org/10.1007/s00572-015-0665-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-015-0665-0

Keywords

Search

Navigation