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2. Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle

Author

Murat, Claude, Payen, Thibaut, Noel, Benjamin, Kuo, Alan, Morin, Emmanuelle, Chen, Juan, Kohler, Annegret, Krizsán, Krisztina, Balestrini, Raffaella, Da Silva, Corinne, Montanini, Barbara, Hainaut, Mathieu, Levati, Elisabetta, Barry, Kerrie W, Belfiori, Beatrice, Cichocki, Nicolas, Clum, Alicia, Dockter, Rhyan B, Fauchery, Laure, Guy, Julie, Iotti, Mirco, Le Tacon, François, Lindquist, Erika A, Lipzen, Anna, Malagnac, Fabienne, Mello, Antonietta, Molinier, Virginie, Miyauchi, Shingo, Poulain, Julie, Riccioni, Claudia, Rubini, Andrea, Sitrit, Yaron, Splivallo, Richard, Traeger, Stefanie, Wang, Mei, Žifčáková, Lucia, Wipf, Daniel, Zambonelli, Alessandra, Paolocci, Francesco, Nowrousian, Minou, Ottonello, Simone, Baldrian, Petr, Spatafora, Joseph W, Henrissat, Bernard, Nagy, Laszlo G, Aury, Jean-Marc, Wincker, Patrick, Grigoriev, Igor V, Bonfante, Paola, and Martin, Francis M

Subjects
Microbiology, Biological Sciences, Genetics, Human Genome, Biotechnology, Ascomycota, DNA, Fungal, Genome, Fungal, Life History Traits, Mycorrhizae, Phylogeny, Sequence Analysis, DNA, Symbiosis, Ecology, Evolutionary biology, Environmental management
Abstract

Tuberaceae is one of the most diverse lineages of symbiotic truffle-forming fungi. To understand the molecular underpinning of the ectomycorrhizal truffle lifestyle, we compared the genomes of Piedmont white truffle (Tuber magnatum), Périgord black truffle (Tuber melanosporum), Burgundy truffle (Tuber aestivum), pig truffle (Choiromyces venosus) and desert truffle (Terfezia boudieri) to saprotrophic Pezizomycetes. Reconstructed gene duplication/loss histories along a time-calibrated phylogeny of Ascomycetes revealed that Tuberaceae-specific traits may be related to a higher gene diversification rate. Genomic features in Tuber species appear to be very similar, with high transposon content, few genes coding lignocellulose-degrading enzymes, a substantial set of lineage-specific fruiting-body-upregulated genes and high expression of genes involved in volatile organic compound metabolism. Developmental and metabolic pathways expressed in ectomycorrhizae and fruiting bodies of T. magnatum and T. melanosporum are unexpectedly very similar, owing to the fact that they diverged ~100 Ma. Volatile organic compounds from pungent truffle odours are not the products of Tuber-specific gene innovations, but rely on the differential expression of an existing gene repertoire. These genomic resources will help to address fundamental questions in the evolution of the truffle lifestyle and the ecology of fungi that have been praised as food delicacies for centuries.

Published
2018

6. Exploring new biodiversity hotspots in Tuber aestivum natural distribution

Author

Belfiori, Beatrice, Riccioni, Claudia, Gómez-Molina, Eva, Sánchez, Sergio, Gallo, Luigi, García-Barreda, Sergi, Henkrar, Fatima, Khabar, Lahsen, Marjanović, Žaklina, Rubini, Andrea, Belfiori, Beatrice, Riccioni, Claudia, Gómez-Molina, Eva, Sánchez, Sergio, Gallo, Luigi, García-Barreda, Sergi, Henkrar, Fatima, Khabar, Lahsen, Marjanović, Žaklina, and Rubini, Andrea

Abstract

Tuber aestivum is associated with a wide range of tree species and is the most widespread edible truffle. Its capability of colonizing many different areas along with a long reaping period, increased in the last decades scientific studies and commercial interest. A number of large- and fine-scale population genetics studies have been conducted to explore its genetic diversity and genetic structure. Recent investigations based on ITS sequence analyses revealed a strong phylogenetic pattern and a higher level of genetic diversity in Turkish and southern European populations than in northern European populations, suggesting that Turkey and southern Europe may have acted as glacial refugia for this species. Despite these findings, the southernmost distributional range of the species is not yet fully explored. With the aim of evaluating other potential diversity hotspots in this study we expand previous investigation, extending the sampling to other southernmost natural T. aestivum areas, such as Moroccan mountainous regions (Middle Atlas), Serbia and several Spanish regions. The ongoing analyses based on haplotypes alignment of the ITS region of the rDNA, reveal as preliminary result a pronounced genetic variability among Moroccan T. aestivum populations, suggesting a possible phylogeographic differentiation also in these new areas of investigation. Additional analyses are underway to better trace natural populations of T. aestivum according to their geographic origin. These aims could be critical both for truffle industry interest in selecting well-adapted inoculum for the production of mycorrhizal seedlings or traceability of truffles provenance, and for the establishment of programs devoted to biodiversity conservation.

Published
2023

20. Comparative genomics and population genetics provide new insights on the life cycle of the black truffle of Périgord (Tuber melanosporum Vittad.)

Author

Riccioni, Claudia, MURAT-FURMINIEUX, Claude, De la Varga Pastor, Herminia, Todesco, Flora, Rubini, Andrea, Belfiori, Beatrice, Payen, Thibaut, Le Tacon, François, Robin, Christophe, Paolocci, Francesco, Martin, Francis, Institute of Biosciences and Bioresources, Consiglio Nazionale delle Ricerche [Roma] (CNR), Interactions Arbres-Microorganismes (IAM), Institut National de la Recherche Agronomique (INRA)-Université de Lorraine (UL), Laboratoire Agronomie et Environnement (LAE), and ProdInra, Migration

Subjects
[SDV] Life Sciences [q-bio], [SDE] Environmental Sciences, genomic, population genetic, [SDV]Life Sciences [q-bio], black truffe, [SDE]Environmental Sciences
Abstract

International audience; Truffles are ectomycorrhizal fungi living in symbiosis with many trees and shrubs. Inoculated seedlings with truffles are available since forty years and the interest in truffle cultivation is increasing worldwide. However, novel management guidelines for sustainable truffle orchards, in which the production is less unpredictable even in the climate change context, are needed. A better understanding of the biological and ecological mechanisms driving the truffle life cycle is one of the approaches to reach these goals. The genomic resources available for Tuber melanosporum allowed us to unravel its sexual reproduction mode by identifying mating type genes and to characterize new polymorphic markers allowing population genetics analyses. The study of genet distribution in truffle orchards showed a non-random spatial distribution of ectomycorrhizas formed by both T. melanosporum mating types, as well as a rapid yearly turnover of these genets. This analysis revealed a striking competition between genets based on their mating-type genes to colonize plant root system and questioned the localization of both parents in the initiation of the sexual cycle. To gain additional information on T. melanosporum genetic diversity, we re-sequenced the nuclear genome of six geographic accessions. A total of 442,326 single nucleotide polymorphisms (SNPs) corresponding to 3,540 SNPs/Mbps were identified. Based on their SNP density, samples clustered according to their geographic origin and the putative role of the last glaciation in T. melanosporum phylogeography is confirmed. Additionally, genomic regions and genes potentially subjected to positive or purifying selection were identified. Finally, a large-scale analysis of T. melanosporum populations at European scale using highly polymorphic simple sequence repeats (SSR) is also in progress.

Published
2015

21. Molecular method for the identification of mating typegenes of truffles species

Author

Martin, Francis, Murat, Claude, Paolocci, Francesco, Rubini, Andrea, Riccioni, Claudia, Belfiori, Beatrice, Arcioni, Sergio, ProdInra, Migration, Interactions Arbres-Microorganismes (IAM), and Institut National de la Recherche Agronomique (INRA)-Université de Lorraine (UL)

Subjects
[SDV] Life Sciences [q-bio], [SDV]Life Sciences [q-bio], C12Q 1/68
Abstract

The invention concerns a method for determining the Tuber species and fertility of a truffle sample, said method comprising: - identifying whether said truffle sample comprises a first nucleotide sequence associated with a first mating type idiomorph (MAT1-2); and - identifying whether said truffle sample comprises a second nucleotide sequence associated with a second mating type idiomorph (MAT1-1); the fertility of said truffle sample requiring the presence of both the first and the second nucleotide sequences., Cette invention concerne un procédé permettant de déterminer l'espèce Tuber et la fertilité d'un échantillon de truffe, ledit procédé comprenant les étapes consistant à : déterminer si ledit échantillon de truffe comprend ou non une première séquence de nucléotides associée à un premier idiomorphe de type sexuel (MAT1-2) ; et - à déterminer si ledit échantillon de truffe comprend ou non une seconde séquence de nucléotides associée à un second idiomorphe de type sexuel (MAT1-1) ; la fertilité dudit échantillon de truffe exigeant la présence à la fois de la première et de la seconde séquence de nucléotides.

Published
2012

24. Fine‐scale spatial genetic structure of the black truffle ( Tuber melanosporum ) investigated with neutral microsatellites and functional mating type genes

Author

Murat, Claude, primary, Rubini, Andrea, additional, Riccioni, Claudia, additional, la Varga, Herminia, additional, Akroume, Emila, additional, Belfiori, Beatrice, additional, Guaragno, Marco, additional, Tacon, François, additional, Robin, Christophe, additional, Halkett, Fabien, additional, Martin, Francis, additional, and Paolocci, Francesco, additional

Published
2013
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31. Mating Type Locus of Chinese Black Truffles Reveals Heterothallism and the Presence of Cryptic Species within theT. indicum Species Complex.

Author

Belfiori, Beatrice, Riccioni, Claudia, Paolocci, Francesco, and Rubini, Andrea

Subjects
*TRUFFLES, *HETEROTHALLISM in fungi, *ASCOMYCETES, *SHRUBS, *NUCLEOTIDE sequence, *GENETIC polymorphisms, *TRANSPOSONS, *FUNGI
Abstract

Tuber spp. are filamentous ascomycetes which establish symbiosis with the roots of trees and shrub species. By virtue of this symbiosis they produce hypogeous ascocarps, known as truffles. Filamentous ascomycetes can reproduce by homothallism or heterothallism depending on the structure and organization of their mating type locus. The first mating type locus in a truffle species has been recently characterized in Tuber melanosporum and it has been shown that this fungus, endemic in Europe, is heterothallic. The availability of sequence information for T. melanosporum mating type genes is seminal to cloning their orthologs from other Tuber species and assessing their reproductive mode. Here we report on the organization of the mating type region in T. indicum, the black truffle species present in Asia, which is the closest relative to T.melanosporum and is characterized by an high level of morphological and genetic variability. The present study shows that T. indicum is also heterothallic. Examination of Asiatic black truffles belonging to different genetic classes, sorted according to the sequence polymorphism of the internal transcribed spacer rDNA region, has revealed sequence variations and rearrangements in both coding and non-coding regions of the mating type locus, to suggest the existence of cryptic species within the T. indicum complex. The presence of transposable elements within or linked to the mating type region suggests a role of these elements in generating the genotypic diversity present among T. indicum strains. Overall, comparative analyses of the mating type locus have thus allowed us to tackle taxonomical and phylogenetic issues within black truffles and make inferences about the evolution of T. melanosporum-T. indicum lineage. Our results are not only of fundamental but also of applied relevance as T. indicum produces edible fruit bodies that are imported also into Europe and thus may represent a biological threat for T. melanosporum. [ABSTRACT FROM AUTHOR]

Published
2013
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32. Pezizomycetes genomes reveal the molecular basis of ectomycorrhizal truffle lifestyle

Author

Alan Kuo, Rhyan B. Dockter, Juan Chen, Shingo Miyauchi, Thibaut Payen, Benjamin Noel, François Le Tacon, Jean-Marc Aury, Minou Nowrousian, Mei Wang, Emmanuelle Morin, Annegret Kohler, Claude Murat, Petr Baldrian, Laure Fauchery, Julie Poulain, Lucia Žifčáková, Julie Guy, Claudia Riccioni, Corinne Da Silva, Francis Martin, László Nagy, Patrick Wincker, Richard Splivallo, Beatrice Belfiori, Fabienne Malagnac, Anna Lipzen, Paola Bonfante, Stefanie Traeger, Francesco Paolocci, Alicia Clum, Mirco Iotti, Yaron Sitrit, Elisabetta Levati, Igor V. Grigoriev, Alessandra Zambonelli, Barbara Montanini, Erika Lindquist, Joseph W. Spatafora, Kerrie Barry, Mathieu Hainaut, Andrea Rubini, Simone Ottonello, Virginie Molinier, Krisztina Krizsán, Raffaella Balestrini, Nicolas Cichocki, Daniel Wipf, Bernard Henrissat, Antonietta Mello, Interactions Arbres-Microorganismes (IAM), Institut National de la Recherche Agronomique (INRA)-Université de Lorraine (UL), Genoscope - Centre national de séquençage [Evry] (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), US Department of Energy Joint Genome Institute, U.S Department of Energy, U.S. Department of Energy [Washington] (DOE)-U.S. Department of Energy [Washington] (DOE), Institute of medicinal plant development, Chinese Academy of Medical Sciences, Synthet & Syst Biol Unit, Hungarian Academy of Sciences (MTA), CNR, Ist Protez Piante, UOS Torino, Laboratory of Functional Genomics and Protein Engineering, Biochemistry and Molecular Biology Unit, Department of Life Sciences, University of Parma = Università degli studi di Parma [Parme, Italie], Dept Life Sci, Biochem & Mol Biol Unit, Lab Funct Genom & Prot Engn, Joint Genome Institute, United States Department of Energy, Plant Genetics Institute, Consiglio Nazionale delle Ricerche [Roma] (CNR), Department of Energy / Joint Genome Institute (DOE), Los Alamos National Laboratory (LANL), Génomique métabolique (UMR 8030), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université d'Évry-Val-d'Essonne (UEVE), Dipartimento Protez & Valorizzaz Agroalimentare, Alma Mater Studiorum University of Bologna (UNIBO), Institut de génétique et microbiologie [Orsay] (IGM), Université Paris-Sud - Paris 11 (UP11)-Centre National de la Recherche Scientifique (CNRS), Istituto per la Protezione delle Piante, Agroécologie [Dijon], Université de Bourgogne (UB)-Institut National de la Recherche Agronomique (INRA)-Université Bourgogne Franche-Comté [COMUE] (UBFC)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement, IPF – Integrative Fungal Research, Goethe-Universität Frankfurt am Main, Institut für biologie und biotechnologie der pflanzen, Westfälische Wilhelms-Universität Münster (WWU), 0977 Unité associée de Biologie forestière, Institut National de la Recherche Agronomique (INRA), Institute of Microbiology of the CAS, Department of Botany and Plant Pathology, Oregon State University (OSU), Architecture et fonction des macromolécules biologiques (AFMB), Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU)-Institut National de la Recherche Agronomique (INRA), Department of Biochemistry and Molecular Biology, Medical and Health Science Center, Institut de Génomique d'Evry (IG), Institut de Biologie François JACOB (JACOB), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay, Dipartimento di Biologia Vegetale, Università degli studi di Torino (UNITO), French National Research Agency through the project SYSTRUF ANR-14-CE06-0020, ANR-09-STRA-10, French National Research Agency through the project SYMWOOD (Laboratory of Excellence Advanced Research on the Biology of Tree and Forest Ecosystems) ANR-11-LABX 0002 01, Office of Science of the US Department of Energy DE-AC02-05CH11231, France Genomique ANR-10-INBS-09, Region Lorraine Research Council, European Commission (European Regional Development Fund), University of Parma, Interuniversity Consortium for Biotechnologies, Piedmont Region, Czech Science Foundation 16-08916S, German Research Foundation NO407/7-1, Department of General and Molecular Botany, ANR-14-CE06-0020,FUNTUNE,Cocktails enzymatiques inspirés de modèles fongiques pour la déconstruction contrôlée de la biomasse végétale(2014), ANR-10-STRA-0010,COMANCHE,Interactions écosystémiques et impacts anthropiques dans les populations de Coquilles St-Jacques de la Manche(2010), ANR-11-LABX-0002,ARBRE,Recherches Avancées sur l'Arbre et les Ecosytèmes Forestiers(2011), ANR-10-INBS-0009,France-Génomique,Organisation et montée en puissance d'une Infrastructure Nationale de Génomique(2010), Université de Lorraine (UL)-Institut National de la Recherche Agronomique (INRA), U.S. Department of Energy (DOE)-U.S. Department of Energy (DOE), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Recherche Agronomique (INRA)-Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement, Institut National de la Recherche Agronomique (INRA)-Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), ANR-10-INBS-09-01/10-INBS-0009,France-Génomique,Organisation et montée en puissance d'une Infrastructure Nationale de Génomique(2010), Murat, Claude, Payen, Thibaut, Noel, Benjamin, Kuo, Alan, Morin, Emmanuelle, Chen, Juan, Kohler, Annegret, Krizsán, Krisztina, Balestrini, Raffaella, Da Silva, Corinne, Montanini, Barbara, Hainaut, Mathieu, Levati, Elisabetta, Barry, Kerrie W., Belfiori, Beatrice, Cichocki, Nicola, Clum, Alicia, Dockter, Rhyan B., Fauchery, Laure, Guy, Julie, Iotti, Mirco, Le Tacon, Françoi, Lindquist, Erika A., Lipzen, Anna, Malagnac, Fabienne, Mello, Antonietta, Molinier, Virginie, Miyauchi, Shingo, Poulain, Julie, Riccioni, Claudia, Rubini, Andrea, Sitrit, Yaron, Splivallo, Richard, Traeger, Stefanie, Wang, Mei, Žifčáková, Lucia, Wipf, Daniel, Zambonelli, Alessandra, Paolocci, Francesco, Nowrousian, Minou, Ottonello, Simone, Baldrian, Petr, Spatafora, Joseph W., Henrissat, Bernard, Nagy, Laszlo G., Aury, Jean-Marc, Wincker, Patrick, Grigoriev, Igor V., Bonfante, Paola, Martin, Francis M., Università degli studi di Parma = University of Parma (UNIPR), National Research Council of Italy | Consiglio Nazionale delle Ricerche (CNR), Institut National de la Recherche Agronomique (INRA)-Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Université Bourgogne Franche-Comté [COMUE] (UBFC), Westfälische Wilhelms-Universität Münster = University of Münster (WWU), Unité associée de biologie forestière, Université Paris-Saclay-Institut de Biologie François JACOB (JACOB), Università degli studi di Torino = University of Turin (UNITO), and MURAT-FURMINIEUX, Claude

Subjects
0301 basic medicine, volatile organic compound, tuber (truffles), [SDV]Life Sciences [q-bio], champignon, Pezizomycetes, truffle, Tuber aestivum, Mycorrhizae, DNA, Fungal, Life History Traits, Phylogeny, 2. Zero hunger, Truffle, Genome, biology, Ecology, composé organique volatil, food and beverages, Ecology, Evolution, Behavior and Systematics, Tuberaceae, Fungal, expression différentielle, Genome, Fungal, Sequence Analysis, tuber, Evolution, no key words, 03 medical and health sciences, truffe, Behavior and Systematics, Ascomycota, Phylogenetics, ddc:570, Botany, Choiromyces, Genetics, Symbiosis, Comparative genomics, Human Genome, fungi, Sequence Analysis, DNA, DNA, champignon ectomycorhizien, 15. Life on land, biology.organism_classification, Ecology, Evolution, Behavior and Systematic, 030104 developmental biology, Tuber melanosporum
Abstract

Tuberaceae is one of the most diverse lineages of symbiotic truffle-forming fungi. To understand the molecular underpinning of the ectomycorrhizal truffle lifestyle, we compared the genomes of Piedmont white truffle (Tuber magnatum), Périgord black truffle (Tuber melanosporum), Burgundy truffle (Tuber aestivum), pig truffle (Choiromyces venosus) and desert truffle (Terfezia boudieri) to saprotrophic Pezizomycetes. Reconstructed gene duplication/loss histories along a time-calibrated phylogeny of Ascomycetes revealed that Tuberaceae-specific traits may be related to a higher gene diversification rate. Genomic features in Tuber species appear to be very similar, with high transposon content, few genes coding lignocellulose-degrading enzymes, a substantial set of lineage-specific fruiting-body-upregulated genes and high expression of genes involved in volatile organic compound metabolism. Developmental and metabolic pathways expressed in ectomycorrhizae and fruiting bodies of T. magnatum and T. melanosporum are unexpectedly very similar, owing to the fact that they diverged ~100 Ma. Volatile organic compounds from pungent truffle odours are not the products of Tuber-specific gene innovations, but rely on the differential expression of an existing gene repertoire. These genomic resources will help to address fundamental questions in the evolution of the truffle lifestyle and the ecology of fungi that have been praised as food delicacies for centuries.

Published
2018
Full Text
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