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A multigene phylogeny demonstrates that Tuber aestivum and Tuber uncinatum are conspecific

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Abstract

For almost 2 centuries it has been disputed whether Tuber aestivum and Tuber uncinatum constitute two different species of truffles. Molecular markers have been applied previously to contribute to resolving this question, coming to different conclusions. In this study, we address this question by analyzing the genetic structure of truffles assigned to either of the two putative species from a geographically broad sampling across Europe. We used an approach involving multigene phylogenies and coalescent analyses of nine regions from five genes. All tests conducted supported the conspecificity of Tuber aestivum and Tuber uncinatum.

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References

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology. doi:10.1016/s0022-2836(05)80360-2.

    PubMed  Google Scholar 

  • Bonito, G., Trappe, J. M., Rawlinson, P., & Vilgalys, R. (2010a). Improved resolution of major clades within Tuber and taxonomy of species within the Tuber gibbosum complex. Mycologia, 102, 1042–1057. doi:10.3852/09-213.

    Article  PubMed  Google Scholar 

  • Bonito, G. M., Gryganskyi, A. P., Trappe, J. M., & Vilgalys, R. (2010b). A global meta-analysis of Tuber ITS rDNA sequences: species diversity, host associations and long-distance dispersal. Molecular Ecology. doi:10.1111/j.1365-294X.2010.04855.x.

    PubMed  Google Scholar 

  • Bonito, G. M., Smith, M., Nowak, M., Healy, R., Guevara, G., Cázares, E., et al. (2013). Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage. PLoS One. doi:10.1371/journal.pone.0052765.

    Google Scholar 

  • Chatin, A. (1887). Une nouvelle espèce de truffe. Les Comptes Rendus de L'Académie Des Sciences, 104, 1132–1135.

    Google Scholar 

  • Chevalier, G., & Frochot, H. (1997). La truffe de Bourgogne. Levallois-Perret: Éditions Pétrarque.

    Google Scholar 

  • Chevalier, G., Desmas, C., Frochot, H., & Riousset, L. (1979). L’espèce Tuber aestivum Vitt.: I. Définition. Mushroom Science, X(Part 1), 957–975.

    Google Scholar 

  • Cunningham, C. W. (1997). Can three incongruence tests predict when data should be combined? Molecular Biology and Evolution, 14, 733–740.

    Article  PubMed  CAS  Google Scholar 

  • Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology. doi:10.1186/1471-2148-7-214.

    PubMed  Google Scholar 

  • Drummond, A. J., Ho, S. Y. W., Phillips, M. J., & Rambaut, A. (2006). Relaxed phylogenetics and dating with confidence. PLoS Biology. doi:10.1371/journal.pbio.0040088.

    PubMed  Google Scholar 

  • Drummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution. doi:10.1093/molbev/mss075.

    Google Scholar 

  • Du Mortier, B. C. (1822). Commentationes botanicae: Observations botaniques, dédiées à la Société d'horticulture de Tournay.

  • Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology. doi:10.1111/j.1365-294X.2005.02553.x.

    Google Scholar 

  • Gandeboeuf, D., Dupré, C., & Chevalier, G. (1994). Use of isoenzyme analysis to differentiate truffles from Europe. Acta Botanica Gallica, 141, 455–463.

    Article  CAS  Google Scholar 

  • Gardes, M., & Bruns, T. D. (1993). ITS primers with enhanced specificity for basidiomycetes - Application to the identification of mycorrhizae and rusts. Molecular Ecology, 2, 113–118.

    Article  PubMed  CAS  Google Scholar 

  • Geiser, D. M., Pitt, J. I., & Taylor, J. W. (1998). Cryptic speciation and recombination in the aflatoxin-producing fungus Aspergillus flavus. Proceedings of the National Academy of Sciences of the United States of America, 95, 388–393.

    Article  PubMed  CAS  Google Scholar 

  • Glass, N. L., & Donaldson, G. C. (1995). Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Applied and Environmental Microbiology, 61, 1323–1330.

    PubMed  CAS  Google Scholar 

  • Guillemaud, T., Raymond, M., Callot, G., Cleyet-Marel, J. C., & Fernandez, D. (1996). Variability of nuclear and mitochondrial ribosomal DNA of a truffle species (Tuber aestivum). Mycological Research, 100, 547–550.

    Article  CAS  Google Scholar 

  • Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology. doi:10.1093/sysbio/syq010.

    PubMed  Google Scholar 

  • Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    CAS  Google Scholar 

  • Hansen, K., LoBuglio, K. F., & Pfister, D. H. (2005). Evolutionary relationships of the cup-fungus genus Peziza and Pezizaceae inferred from multiple nuclear genes: RPB2, beta-tubulin, and LSU rDNA. Molecular Phylogenetics and Evolution. doi:10.1016/j.ympev.2005.03.010.

    PubMed  Google Scholar 

  • Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. doi:10.1093/bioinformatics/17.8.754.

    PubMed  Google Scholar 

  • Jeandroz, S., Murat, C., Wang, Y. J., Bonfante, P., & Le Tacon, F. (2008). Molecular phylogeny and historical biogeography of the genus Tuber, the 'true truffles'. Journal of Biogeography. doi:10.1111/j.1365-2699.2007.01851.x.

    Google Scholar 

  • Larsson, E., & Jeppson, M. (2008). Phylogenetic relationships among species and genera of Lycoperdaceae based on ITS and LSU sequence data from north European taxa. Mycological Research. doi:10.1016/i.mycres.2007.10.018.

    Google Scholar 

  • Librado, P., & Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. doi:10.1093/bioinformatics/btp187.

    PubMed  Google Scholar 

  • Maddison, W. P., & Knowles, L. L. (2006). Inferring phylogeny despite incomplete lineage sorting. Systematic Biology. doi:10.1080/10635150500354928.

    PubMed  Google Scholar 

  • Maddison, W. P., & Maddison, D. (2011). Mesquite: A modular system for evolutionary analysis. Version 2.75.

  • Matheny, P. B. (2005). Improving phylogenetic inference of mushrooms with RPB1 and RPB2 nucleotide sequences (Inocybe; Agaricales). Molecular Phylogenetics and Evolution. doi:10.1016/j.ympev.2004.11.014.

    Google Scholar 

  • Matheny, P. B., Liu, Y. J. J., Ammirati, J. F., & Hall, B. D. (2002). Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). American Journal of Botany, 89, 688–698.

    Article  PubMed  CAS  Google Scholar 

  • Mello, A., Cantisani, A., Vizzini, A., & Bonfante, P. (2002). Genetic variability of Tuber uncinatum and its relatedness to other black truffles. Environmental Microbiology, 4, 584–594.

    Article  PubMed  CAS  Google Scholar 

  • Molitor, C., Inthavong, B., Sage, L., Geremia, R. A., & Mouhamadou, B. (2010). Potentiality of the cox1 gene in the taxonomic resolution of soil fungi. FEMS Microbiology Letters. doi:10.1111/j.1574-6968.2009.01839.x.

    PubMed  Google Scholar 

  • Mouches, C., Duthil, P., Poitou, N., Delmas, J., & Bove, J. (1981). Caractérisation des espèces truffières par analyse de leurs protéines en gels de polyacrylamide et application de ces techniques à la taxonomie des champignons. Mushroom Science, 11, 819–831.

    Google Scholar 

  • Paolocci, F., Rubini, A., Riccioni, C., Topini, F., & Arcioni, S. (2004). Tuber aestivum and Tuber uncinatum: two morphotypes or two species? FEMS Microbiology Letters, 235, 109–115.

    Article  PubMed  CAS  Google Scholar 

  • Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution. doi:10.1093/molbev/msn083.

    Google Scholar 

  • Posada, D., & Buckley, T. R. (2004). Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology. doi:10.1080/10635150490522304.

    PubMed  Google Scholar 

  • Rambaut, A. (2009). FigTree v1.3.1. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh.

  • Rambaut, A., & Drummond, A. J. (2006). TreeAnnotator 1.4.5. http://beastbioedacuk/TreeAnnotator.

  • Rambaut, A., & Drummond, A. J. (2007). Tracer v1.4. Available from http://beastbioedacuk/Tracer.

  • Riousset, L., Riousset, G., Chevalier, G., & Bardet, M. C. (2001). Truffes d’Europe et de Chine. Paris: INRA Editions.

    Google Scholar 

  • Rokas, A., Williams, B. L., King, N., & Carroll, S. B. (2003). Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature. doi:10.1038/nature02053.

    PubMed  Google Scholar 

  • Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. doi:10.1093/bioinformatics/btg180.

    PubMed  Google Scholar 

  • Roux, C., Sejalon-Delmas, N., Martins, M., Parguey-Leduc, A., Dargent, R., & Becard, G. (1999). Phylogenetic relationships between European and Chinese truffles based on parsimony and distance analysis of ITS sequences. FEMS Microbiology Letters, 180, 147–155.

    Article  PubMed  CAS  Google Scholar 

  • Spatafora, J. W., Sung, G. H., Johnson, D., Hesse, C., O'Rourke, B., Serdani, M., et al. (2006). A five-gene phylogeny of Pezizomycotina. Mycologia, 98, 1018–1028.

    Article  PubMed  CAS  Google Scholar 

  • Splivallo, R., Valdez, N., Kirchhoff, N., Ona, M. C., Schmidt, J. P., Feussner, I., et al. (2012). Intraspecific genotypic variability determines concentrations of key truffle volatiles. New Phytologist. doi:10.1111/j.1469-8137.2012.04077.x.

    PubMed  Google Scholar 

  • Stockinger, H., Walker, C., & Schussler, A. (2009). 'Glomus intraradices DAOM197198', a model fungus in arbuscular mycorrhiza research, is not Glomus intraradices. New Phytologist. doi:10.1111/j.1469-8137.2009.02874.x.

    Google Scholar 

  • Swofford, D. L. (2002). PAUP*: Phylogenetic analysis using parsimony (*and Other Methods) (40th ed.). Sunderland: Sinauer.

    Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution. doi:10.1093/molbev/msr121.

    Google Scholar 

  • Taylor, J. W., Jacobson, D. J., Kroken, S., Kasuga, T., Geiser, D. M., Hibbett, D. S., et al. (2000). Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology. doi:10.1006/fgbi.2000.1228.

    Google Scholar 

  • Templeton, A. R. (1983). Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and the apes. Evolution. doi:10.2307/2408332.

    Google Scholar 

  • Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). Clustal-w—improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research. doi:10.1093/nar/22.22.4673.

    Google Scholar 

  • Urbanelli, S., Sallicandro, P., De Vito, E., Bullini, L., & Biocca, E. (1998). Biochemical systematics of some species in the genus Tuber. Mycologia, 90, 537–546.

    Article  CAS  Google Scholar 

  • van Tuinen, D., Zhao, B., & Gianinazzi-Pearson, V. (1998). PCR in studies of AM fungi: From primers to application (pp. 387–399). Berlin Heidelberg New York: Springer.

  • Vittadini, C. (1831). Monographia tuberacearum. Milan: Rusconi.

    Google Scholar 

  • Wang, Y. J., Tan, Z. M., Zhang, D. C., Murat, C., Jeandroz, S., & Le Tacon, F. (2006). Phylogenetic relationships between Tuber pseudoexcavatum, a Chinese truffle, and other Tuber species based on parsimony and distance analysis of four different gene sequences. FEMS Microbiology Letters. doi:10.1111/j.1574-6868.2006.00283.x.

    Google Scholar 

  • Weden, C., Danell, E., & Tibell, L. (2005). Species recognition in the truffle genus Tuber—the synonyms Tuber aestivum and Tuber uncinatum. Environmental Microbiology. doi:10.1111/j.1462-2920.2005.00837.x.

    PubMed  Google Scholar 

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols. San Diego: A Guide to Methods and Applications Academic Press.

    Google Scholar 

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Acknowledgments

This study was supported by the Burgundy Regional Council. We are grateful to Henri Frochot for providing Tuber aestivum samples. We thank Gian Carlo Ponzi and Claude Murat for providing Tuber macrosporum and Tuber magnatum samples, respectively. We are grateful to Gregory Bonito for providing primer sequences for the elongation factor 1α gene. We also thank Régis Courtecuisse for accepting our exsiccata samples in the LIP herbarium.

The authors declare that the experiments comply with the current laws of France.

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Authors and Affiliations

  1. UMR Agroécologie INRA 1347/Agrosup/Université de Bourgogne, Pôle “Interaction Plantes-Micro-organismes” ERL CNRS 6300, 17 rue Sully, BP 86510, 21065, Dijon Cedex, France

    Virginie Molinier, Diederik van Tuinen, Daniel Wipf & Dirk Redecker

  2. Résidence Cristelle, Cournon d’Auvergnes, France

    Gérard Chevalier

  3. Inoplant, 13 rue des Souhaits, 21110, Aiserey, France

    Armelle Gollotte

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  1. Virginie Molinier
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  2. Diederik van Tuinen
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  3. Gérard Chevalier
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Correspondence to Virginie Molinier.

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Molinier, V., van Tuinen, D., Chevalier, G. et al. A multigene phylogeny demonstrates that Tuber aestivum and Tuber uncinatum are conspecific. Org Divers Evol 13, 503–512 (2013). https://doi.org/10.1007/s13127-013-0146-2

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