Skip to main content
SpringerLink
Log in

Impact of the competition between mating types on the cultivation of Tuber melanosporum: Romeo and Juliet and the matter of space and time

  • Review
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Major breakthroughs in our understanding of the life cycles of the symbiotic ascomycetes belonging to the genus Tuber have occurred over the last several years. A number of Tuber species produce edible fruiting bodies, known as truffles, that are marketed worldwide. A better understanding of the basic biological characteristics of Tuber spp. is likely to have tremendous practical relevance for their cultivation. Tuber melanosporum produces the most valuable black truffles and its genome has been recently sequenced. This species is now serving as a model for studying the biology of truffles. Here, we review recent progress in the understanding of sexual reproduction modalities in T. melanosporum. The practical relevance of these findings is outlined. In particular, the discoveries that T. melanosporum is heterothallic and that strains of different mating types compete to persist on the roots of host plants suggest that the spatial and temporal distributional patterns of strains of different mating types are key determinants of truffle fructification. The spatial segregation of the two mating types in areas where T. melanosporum occurs likely limits truffle production. Thus, host plant inoculation techniques and agronomic practices that might be pursued to manage T. melanosporum orchards with a balanced presence of the two mating partners are described.

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

  • Antony-Babu S, Deveau A, Van Nostrand JD, Zhou J, Le Tacon F, Robin C, Frey-Klett P, Uroz S (2013) Black truffle-associated bacterial communities during the development and maturation of Tuber melanosporum ascocarps and putative functional roles. Environ Microbiol. doi:10.1111/1462-2920.12294

    PubMed  Google Scholar 

  • Arnault C, Dufournel I (1994) Genome and stresses: reactions against aggressions, behavior of transposable elements. Genetica 93:149–160

    Article  PubMed  CAS  Google Scholar 

  • Barbieri E, Guidi C, Bertaux J, Frey-Klett P, Garbaye J, Ceccaroli P, Saltarelli R, Zambonelli A, Stocchi V (2007) Occurrence and diversity of bacterial communities in Tuber magnatum during truffle maturation. Environ Microbiol 9:2234–2246

    Article  PubMed  Google Scholar 

  • Belfiori B, Riccioni C, Paolocci F, Rubini A (2013) Mating type locus of Chinese black truffles reveals heterothallism and the presence of cryptic species within the T. indicum species complex. PLoS ONE 8(12):e82353

    Google Scholar 

  • Bertault G, Raymond M, Berthomieu A, Callot G, Fernandez D (1998) Trifling variation in truffles. Nature 394:734

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Billiard S, López-Villavicencio M, Hood ME, Giraud T (2012) Sex outcrossing and mating type: unsolved questions in fungi and beyond. J Evol Biol 25:1020–1038

    Article  PubMed  CAS  Google Scholar 

  • Bonet JA, Oliach D, Fischer C, Olivera A, de Aragón JM, Colinas C (2009) Cultivation methods of the black truffle, the most profitable Mediterranean non-wood forest product; a state of the art review. In: Palahí M, Birot Y, Bravo F, Gorriz E (eds) Modelling, valuing and managing Mediterranean forest ecosystems for non-timber goods and services. EFI Proceedings n. 57 pp 57–71

  • Büntgen U, Tegel W, Egli S, Stobbe U, Sproll L, Stenseth NC (2011) Truffles and climate change. Front Ecol Environ 9:150–151

    Article  Google Scholar 

  • Büntgen U, Egli S, Camarero JJ, Fischer EM, Stobbe U, Kauserud H, Tegel W, Sproll L, Stenseth NC (2012) Drought-induced decline in Mediterranean truffle harvest. Nat Climate Change 2:827–829

    Article  Google Scholar 

  • Butler G (2007) The evolution of MAT: the ascomycetes. In: Heitman J, Kronstad JW, Taylor JW, Casselton L (eds) Sex in fungi: molecular determination and evolutionary implications. ASM, Washington, DC, pp 3–18

    Chapter  Google Scholar 

  • Buzzini P, Gasparetti C, Turchetti B, Cramarossa MR, Vaughan-Martini A, Martini A, Pagnoni UM, Forti L (2005) Production of volatile organic compounds (VOCs) by yeasts isolated from the ascocarps of black (Tuber melanosporum Vitt.) and white (Tuber magnatum Pico) truffles. Arch Microbiol 184:187–193

    Article  PubMed  CAS  Google Scholar 

  • C. Plinii Secundi (79) Naturalis historia

  • Callot G (1999) La truffe, la terre, la vie. INRA, Paris

    Google Scholar 

  • Casacuberta E, González J (2013) The impact of transposable elements in environmental adaptation. Mol Ecol 22:1503–1517

    Article  PubMed  CAS  Google Scholar 

  • Chevalier G, Dupré C (1988) Recherche et experimentation sur la truffe et la trufficulture en France. In: Bencivenga M, Granetti B (eds) Atti del Secondo Congresso Internazionale sul tartufo, Spoleto, pp 157–166

  • Chevalier G, Frochot H (1997) La maitrise de culture de la truffe. Champignons et mycorhizes en foret. Revue-Forestiere-Francaise Special Issue 49:201–213

    Article  Google Scholar 

  • Choi GH, Dawe AL, Churbanov A, Smith ML, Milgroom MG, Nuss DL (2012) Molecular characterization of vegetative incompatibility genes that restrict hypovirus transmission in the chestnut blight fungus Cryphonectria parasitica. Genetics 190:113–127

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ciccarelli A (1564) Opusculum de Tuberibus. Pavia, Italy

  • Daboussi MJ, Capy P (2003) Transposable elements in filamentous fungi. Annu Rev Microbiol 57:275–299

    Article  PubMed  CAS  Google Scholar 

  • Debets AJM, Griffiths AJF (1998) Polymorphism in het genes prevents resource plundering in Neurospora crassa. Mycol Res 102:1343–1349

    Article  CAS  Google Scholar 

  • Debuchy R, Berteaux-Lecellier V, Silar P (2010) Mating systems and sexual morphogenesis in ascomycetes. In: Borkowich KA, Ebbole DJ (eds) Cellular and molecular biology of filamentous fungi. ASM, Washington, DC, pp 501–535

    Google Scholar 

  • Egger KN (2006) The surprising diversity of ascomycetous mycorrhizas. New Phytol 170:421–423

    Article  PubMed  Google Scholar 

  • Fassi B, Fontana A (1967) Sintesi micorrizica tra Pinus strobus e Tuber maculatum. I. Micorrize e sviluppo dei semenzali del secondo anno. Allionia 13:177–186

    Google Scholar 

  • Feschotte C, Jiang N, Wessler SR (2002) Plant transposable elements: where genetics meets genomics. Nat Rev 3:329–341

    Article  CAS  Google Scholar 

  • Fraser JA, Heitman J (2003) Fungal mating-type loci. Curr Biol 13:R792–R795

    Article  PubMed  CAS  Google Scholar 

  • Glass NL, Jacobson DJ, Patrick KTS (2000) The genetics of hyphal fusion and vegetative incompatibility filamentous ascomycete fungi. Annu Rev Genet 34:165–186

    Article  PubMed  CAS  Google Scholar 

  • Hall IR, Yun W, Amicucci A (2003) Cultivation of edible ectomycorrhizal mushrooms. Trends Biotechnol 21:433–438

    Article  PubMed  CAS  Google Scholar 

  • Healy RA, Smith ME, Bonito GM, Pfister DH, Ge ZW, Guevara GG, Williams G, Stafford K, Kumar L, Lee T, Hobart C, Trappe J, Vilgarys R, Mclaughlin DJ (2013) High diversity and widespread occurrence of mitotic spore mats in ectomycorrhizal Pezizales. Mol Ecol 22:1717–1732

    Article  PubMed  CAS  Google Scholar 

  • Hirochika H, Sugimoto K, Otsuki Y, Tsugawa H, Kanda M (1996) Retrotransposons of rice involved in mutations induced by tissue culture. Proc Natl Acad Sci U S A 93:7783–7788

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Iotti M, Rubini A, Tisserant E, Kholer A, Paolocci F, Zambonelli A (2012) Self/nonself recognition in Tuber melanosporum is not mediated by a heterokaryon incompatibility system. Fungal Biol 116:261–275

    Article  PubMed  CAS  Google Scholar 

  • Kronstad JW (2007) Self-fertility: the genetics of sex in lonely fungi. Curr Biol 17:R843–R845

    Article  PubMed  CAS  Google Scholar 

  • Linde CC, Selmes H (2012) Genetic diversity and mating type distribution of Tuber melanosporum and their significance to truffle cultivation in artificially planted truffieres in Australia. Appl Environ Microbiol 78:6534–6539

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Martin F, Kohler A, Murat C et al (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464:1033–1038

    Article  PubMed  CAS  Google Scholar 

  • Martin F, Murat C, Paolocci F, Rubini A, Riccioni C, Belfiori B, Arcioni S (2012) Molecular method for the identification of mating type genes of truffles species. European Patent Application EP2426215

  • Metzenberg RL, Glass NL (1990) Mating type and mating strategies in Neurospora. BioEssays 12:53–59

    Article  PubMed  CAS  Google Scholar 

  • Molière JBP (1664) Le Tartuffe ou l’Imposteur, Comedie. Paris, France

  • Murat C, Díez J, Luis P, Delaruelle C, Dupré C, Chevalier G, Bonfante P, Martin F (2004) Polymorphism at the ribosomal DNA ITS and its relation to postglacial re-colonization routes of the Perigord truffle Tuber melanosporum. New Phytol 164:401–411

    Article  CAS  Google Scholar 

  • Murat C, Riccioni C, Belfiori B, Cichocki N, Labbé J, Morin E, Tisserant E, Paolocci F, Rubini A, Martin F (2011) Distribution and localization of microsatellites in the Perigord black truffle genome and identification of new molecular markers. Fungal Genet Biol 48:592–601

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Murtagh GJ, Dyer PS, Crittenden PD (2000) Reproductive systems: sex and the single lichen. Nature 404:564

    Article  PubMed  CAS  Google Scholar 

  • Otto S, Lenormand T (2002) Evolution of sex: resolving the paradox of sex and recombination. Nat Rev Genet 3:252–261

    Article  PubMed  CAS  Google Scholar 

  • Pacioni G, Leonardi M, Aimola P, Ragnelli AM, Rubini A, Paolocci F (2007) Isolation and characterization of some mycelia inhabiting Tuber ascomata. Mycol Res 111:1450–1460

    Article  PubMed  CAS  Google Scholar 

  • Paoletti M, Seymour FA, Alcocer MJC, Kaur N, Calvo AM, Archer DB, Dyer PS (2007) Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans. Curr Biol 17:1384–1389

    Article  PubMed  CAS  Google Scholar 

  • Paolocci F, Rubini A, Riccioni C, Arcioni S (2006) Reevaluation of the life cycle of Tuber magnatum. Appl Environ Microbiol 72:2390–2393

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Parladé J, De la Varga H, De Miguel AM, Sáez R, Pera J (2013) Quantification of extraradical mycelium of Tuber melanosporum in soils from truffle orchards in northern Spain. Mycorrhiza 23:99–106

    Article  PubMed  Google Scholar 

  • Perrin N (2012) What uses are mating types? The “developmental switch” model. Evolution 66:947–956

    Article  PubMed  Google Scholar 

  • Piepho HP, Koch G (2000) Codominant analysis of banding data from a dominant marker system by normal mixtures. Genetics 155:1459–1468

    PubMed Central  PubMed  CAS  Google Scholar 

  • Potter SS, Brorein WJJ, Dunsmuir P, Rubin GM (1979) Transposition of elements of the 412, copia and 297 dispersed repeated gene families in Drosophila. Cell 17:415–427

    Article  PubMed  CAS  Google Scholar 

  • Rakocevic A, Mondy S, Tirichine L, Cosson V, Brocard L, Iantcheva A, Cayrel A, Devier B, Abu El-Heba GA, Pl R (2009) MERE1, a low-copy-number copia-type retroelement in Medicago truncatula active during tissue culture. Plant Physiol 151:1250–1263

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Riccioni C, Belfiori B, Rubini A, Passeri V, Arcioni 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

    Article  PubMed  CAS  Google Scholar 

  • Rubini A, Paolocci F, Granetti B, Arcioni S (2001) Morphological characterization of molecular-typed Tuber magnatum ectomycorrhizae. Mycorrhiza 11:179–185

    Article  CAS  Google Scholar 

  • Rubini A, Topini F, Riccioni C, Paolocci F, Arcioni S (2004) Isolation and characterization of polymorphic microsatellite loci in white truffle (Tuber magnatum). Mol Ecol Notes 4:116–118

    Article  CAS  Google Scholar 

  • Rubini A, Paolocci F, Riccioni C, Vendramin GG, Arcioni S (2005) Genetic and phylogeographic structures of the symbiotic fungus Tuber magnatum. Appl Environ Microbiol 71:6584–6589

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Rubini A, Riccioni C, Arcioni S, Paolocci F (2007) Troubles with truffles: unveiling more of their biology. New Phytol 174:256–259

    Article  PubMed  Google Scholar 

  • Rubini A, Belfiori B, Riccioni C, Tisserant E, Arcioni S, Martin F, Paolocci F (2011a) Isolation and characterization of MAT genes in the symbiotic ascomycete Tuber melanosporum. New Phytol 189:710–722

    Article  PubMed  CAS  Google Scholar 

  • Rubini A, Belfiori B, Riccioni C, Arcioni S, Martin F, Paolocci F (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 189:723–735

    Article  PubMed  Google Scholar 

  • Rubini A, Belfiori B, Riccioni C, Paolocci F (2012) Genomics of Tuber melanosporum: new knowledge concerning reproductive biology, symbiosis and aroma production. In: Zambonelli A, Bonito GM (eds) Edible ectomycorrhizal mushrooms. Soil biology, vol 34. Springer, Berlin, pp 57–72

    Chapter  Google Scholar 

  • Sacerdot C, Mercier G, Todeschini AL, Dutreix M, Springer M et al (2005) Impact of ionizing radiation on the life cycle of Saccharomyces cerevisiae Ty1 retrotransposon. Yeast 22:441–455

    Article  PubMed  CAS  Google Scholar 

  • Sehgal A, Lee CY, Espenshade PJ (2007) SREBP controls oxygen-dependent mobilization of retrotransposons in fission yeast. PLoS Genet 3:e131. doi:10.1371/journal.pgen.0030131

    Article  PubMed Central  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Shakespeare W (1597) Romeo and Juliet

  • Sourzat P (1997) Guide pratique de trufficulture. Station d’expérimentations sur la truffe (ed). Le Montat, France. 96 p

  • Urban A, Neuner-Plattner I, Krisai-Greilhuber I, Haselwandter K (2004) Molecular studies on terricolous microfungi reveal novel anamorphs of two Tuber species. Mycol Res 108:749–758

    Article  PubMed  CAS  Google Scholar 

  • Wik L, Karlsson M, Johannesson H (2008) The evolutionary trajectory of the mating-type (mat) genes in Neurospora relates to reproductive behavior of taxa. BMC Evol Biol 8:109

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yun W, Hall IR (2004) Edible ectomycorrhizal mushrooms: challenges and achievements. Can J Bot 82:1063–1073

    Article  Google Scholar 

  • Zampieri E, Murat C, Cagnasso M, Bonfante P, Mello A (2010) Soil analysis reveals the presence of an extended mycelial network in a Tuber magnatum truffle-ground. FEMS Microbiol Ecol 71:43–49

    Article  PubMed  CAS  Google Scholar 

  • Zampieri E, Balestrini R, Kohler A, Abbà S, Martin F, Bonfante P (2011) The Perigord black truffle responds to cold temperature with an extensive reprogramming of its transcriptional activity. Fungal Genet Biol 48:585–591

    Article  PubMed  CAS  Google Scholar 

  • Zampieri E, Rizziello R, Bonfante P, Mello A (2012) The detection of mating type genes of Tuber melanosporum in productive and non productive soils. Appl Soil Ecol 57:9–15

    Article  Google Scholar 

  • Zeller B, Bréchet C, Maurice JP, Le Tacon F (2008) Saprotrophic versus symbiotic strategy during truffle ascocarp development under holm oak. A response based on 13C and 15N natural abundance. Ann For Sci 65:607

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Biosciences and BioResources—Perugia Division, National Research Council, Via della Madonna Alta 130, 06128, Perugia, Italy

    Andrea Rubini, Claudia Riccioni, Beatrice Belfiori & Francesco Paolocci

Authors
  1. Andrea Rubini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claudia Riccioni
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Beatrice Belfiori
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francesco Paolocci
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Francesco Paolocci.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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 24 (Suppl 1), 19–27 (2014). https://doi.org/10.1007/s00572-013-0551-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-013-0551-6

Keywords

Search

Navigation