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A Multigene Phylogeny Demonstrates That Tuber Aestivum and Tuber Uncinatum Are Conspecific

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A Multigene Phylogeny Demonstrates That Tuber Aestivum and Tuber Uncinatum Are Conspecific Org Divers Evol (2013) 13:503–512 DOI 10.1007/s13127-013-0146-2 ORIGINAL ARTICLE A multigene phylogeny demonstrates that Tuber aestivum and Tuber uncinatum are conspecific Virginie Molinier & Diederik van Tuinen & Gérard Chevalier & Armelle Gollotte & Daniel Wipf & Dirk Redecker Received: 4 February 2013 /Accepted: 6 July 2013 /Published online: 10 August 2013 # Gesellschaft für Biologische Systematik 2013 Abstract For almost 2 centuries it has been disputed wheth- Tuber P. Micheli ex F.H. Wigg (Bonito et al. 2013). The er Tuber aestivum and Tuber uncinatum constitute two dif- commonly named “true truffles” belong to this genus. The ferent species of truffles. Molecular markers have been ap- latter exclusively includes hypogeous fungi, which establish plied previously to contribute to resolving this question, symbiotic relationships (ectomycorrhizae) with different host coming to different conclusions. In this study, we address trees within the families Betulaceae, Fagaceae, Pinaceae,and this question by analyzing the genetic structure of truffles even Tiliaceae. In the genus Tuber, according to the Index assigned to either of the two putative species from a geo- Fungorum, more than 225 taxa are recognized (Jeandroz graphically broad sampling across Europe. We used an ap- et al. 2008). In Europe, about 30 species have been found and proach involving multigene phylogenies and coalescent described. Due to their famous organoleptic properties, some of analyses of nine regions from five genes. All tests conducted them, such as Tuber magnatum (the Alba truffle) and Tuber supported the conspecificity of Tuber aestivum and Tuber melanosporum (the Périgord truffle), have high economic uncinatum. values. Tuber species have been generally differentiated and named based on ascomata and their phenotypic characteristics, Keywords Phylogenetic analyses . Multi-marker study . using morphological features of asci and spores. But, with the Tuber uncinatum . Tuber aestivum increasing use of molecular tools in biology, species identifi- cation is usually supported by phylogenetic approaches. Nevertheless, even though new classifications based on molec- Introduction ular markers of the family Tuberaceae and the genus Tuber have recently been proposed (Bonito et al. 2010a; Jeandroz The family Tuberaceae, described for the first time in 1822 et al. 2008), ambiguities in species delimitation and phyloge- (Du Mortier 1822), comprises seven genera, among them netic placement remain for some species. Tuber aestivum Vittad. (the Summer truffle), for instance, described for the first time in 1831 by Carlo Vittadini (Vittadini 1831), and common- Electronic supplementary material The online version of this article ly present in Europe, has a maturation period during the sum- (doi:10.1007/s13127-013-0146-2) contains supplementary material, mer and a light brown gleba (spore-bearing) with a black which is available to authorized users. peridium. However, in 1887, Adolphe Chatin described a new V. Molinier (*) : D. van Tuinen : D. Wipf : D. Redecker truffle species, Tuber uncinatum Chatin. (the Burgundy truffle), UMR Agroécologie INRA 1347/Agrosup/Université de very similar to T. aestivum (Chatin 1887). According to his “ ” Bourgogne, Pôle Interaction Plantes-Micro-organismes ERL description, the new species mainly differed from T. aestivum CNRS 6300, 17 rue Sully, BP 86510, 21065 Dijon Cedex, France e-mail: [email protected] by the presence of hooks in the spore reticulum. This criterion was later shown to be an artifact, but for more than 2 centuries, G. Chevalier scientists have been divided concerning the taxonomic classifi- ’ Résidence Cristelle, Cournon d Auvergnes, France cation of T. aestivum and T. uncinatum as other morphological A. Gollotte and ecological criteria suggested considerable differences be- Inoplant, 13 rue des Souhaits, 21110 Aiserey, France tween these two taxa (Chevalier and Frochot 1997; Riousset 504 V. Molinier et al. et al. 2001). Other morphology-based studies concluded that T. nine different genetic markers from five genes commonly uncinatum and T. aestivum constitute a single species used for phylogenetic analysis. We used the robust maxi- (Gandeboeuf et al. 1994; Mouches et al. 1981; Urbanelli et al. mum likelihood and Bayesian inference methods for phylo- 1998). Using molecular marker genes, three major studies have genetic analyses and performed coalescent analyses, which focused on possible genetic differentiation between the two are powerful tools to infer species history. Finally, several putative taxa. In 2002, Mello et al. using phylogenetic analyses tests were used to study the potential genetic structure and mainly based on the Internal Transcribed Spacers (ITS), geographic correlation within the sampling. assigned the two forms to two different taxa (Mello et al. 2002). Paolocci et al. (2004), using RFLP analyses, ITS, beta-tubulin and elongation factor alpha sequences from a Materials and methods subset of the samples, concluded that they belong to a single species. The samples analyzed by Mello et al. Sampling, amplification and sequencing (2002) and Paolocci et al. (2004) originated mostly or even exclusively from Italy; therefore, it seems unlikely that the Fungal samples were prepared from 26 exsiccata coming whole genetic diversity of the two forms across their geo- from natural habitats and previously assigned to either T. graphic range from Sweden to Spain through central Europe aestivum or T. uncinatum according to morphological was addressed in these studies. Weden et al. (2005) analyzed criteria. Morphological aspects of spores were characterized, possible correlations between the spore reticulum (which is the including spore dimensions and the reticulum and alveole morphological character commonly used to distinguish T. shape (Chevalier et al. 1979). A lower reticulum height and aestivum and T. uncinatum) and ITS sequences in a broader less regular alveoles were considered to be characteristic for geographical sample of fruit bodies. These authors came to the T. aestivum. Two outgroup taxa, T. macrosporum and T. conclusion that the spore reticulum is not a useful diagnostic magnatum, were added. Details about the samples analyzed character and that T. aestivum and T. uncinatum were are provided in Table 1. The exsiccata were deposited in the intermingled in the phylogenies, thus indicating conspecificity. herbarium of the University of Lille (LIP). Genomic DNAs The contrasting conclusions obtained in the three cited of the ascomata were isolated from 20 mg of dried gleba of studies may have been due to the differences in the geographic each sample using DNeasy® Plant Mini Kit (Qiagen, Hilden, origin of the samples, the number of phylogenetic markers used Germany) according to the manufacturer’s instructions. or to the phylogenetic methods used. It is evident that a limited Extracts were eluted in 190 μl of Buffer AE supplied in the geographic sampling area can bias results toward genetic ho- kit. DNA concentration was estimated using a NanoDrop mogeneity. The small number of marker genes used may not (Thermo Scientific) spectrophotometer. Nine different loci have provided sufficient resolution for all taxa analyzed or may were amplified by polymerase chain reaction (PCR) from have resulted in weakly supported phylogenies. Indeed, gene ascoma extracts: internal transcribed spacers 1 and 2, a history cannot always be equated to species history, for in- fragment each of the nuclear ribosomal large subunit (nu stance, due to horizontal gene transfer, deep coalescence or LSU), the nuclear ribosomal small subunit (nu SSU), the gene duplication (Maddison and Knowles 2006). mitochondrial ribosomal large subunit (mt LSU) and the Due to the difficulties in using morphological and biolog- mitochondrial ribosomal small subunit (mt SSU), the beta- ical species concepts in fungi, which however are widely tubulin (β-tubulin) gene, elongation factor 1-α (EF1α) and useful for many plants and animals, phylogenetic species the RPB2 gene, which encodes the second largest subunit of recognition approaches have been proposed for fungi, re- RNA polymerase II (RPB2_7_11). All PCR amplifications quiring DNA sequences of multiple marker genes (Taylor were performed using 50 ng of template DNA in a final et al. 2000). The advantage of these approaches is that they volume of 20 μl containing 10X PCR Buffer (Invitrogen), define precise tests for the probability that two taxa are 1UofTaq DNA polymerase (Invitrogen), 0.125 mM of each conspecific. dNTP, 0.5 μM of each forward and reverse primer, and It has to be stated that in spite of the long debate over the sterile water to adjust the volume. For each locus, primer conspecificity of T. aestivum and T. uncinatum, this question sequences, MgCl2, DMSO and BSA concentrations (if to date has not been stringently addressed using multiple added) and cycling conditions are listed in Table 2. One- marker genes and a sufficiently broad geographic sampling. directional Sanger sequencing was performed by GATC Therefore, our goal was to investigate the genetic diversity Biotech (Konstanz, Germany). Sequences were edited and among Tuber samples assigned either to the T. aestivum manually trimmed using BioEdit 7.0.5.3 (Hall 1999). morphotype or to the T. uncinatum morphotype by robust Sequences were queried against the NCBI public database and powerful methods using multiple marker genes. Tuber GenBank using the BLASTN algorithm (Altschul et al. ascomata were sampled from numerous
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