Two ectomycorrhizal truffles, Tuber melanosporum and T. aestivum, endophytically colonise roots of non-ectomycorrhizal plants in natural environments.
Black Périgord truffle
Burgundy truffle
FISH
brûlé
ectomycorrhizas
endophytism
truffle dioecy
truffle life cycle
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
03 2020
03 2020
Historique:
received:
18
09
2019
accepted:
30
10
2019
pubmed:
17
11
2019
medline:
15
5
2021
entrez:
17
11
2019
Statut:
ppublish
Résumé
Serendipitous findings and studies on Tuber species suggest that some ectomycorrhizal fungi, beyond their complex interaction with ectomycorrhizal hosts, also colonise roots of nonectomycorrhizal plants in a loose way called endophytism. Here, we investigate endophytism of T. melanosporum and T. aestivum. We visualised endophytic T. melanosporum hyphae by fluorescent in situ hybridisation on nonectomycorrhizal plants. For the two Tuber species, microsatellite genotyping investigated the endophytic presence of the individuals whose mating produced nearby ascocarps. We quantified the expression of four T. aestivum genes in roots of endophyted, non-ectomycorrhizal plants. Tuber melanosporum hyphae colonised the apoplast of healthy roots, confirming endophytism. Endophytic Tuber melanosporum and T. aestivum contributed to nearby ascocarps, but only as maternal parents (forming the flesh). Paternal individuals (giving only genes found in meiotic spores of ascocarps) were not detected. Gene expression of T. aestivum in non-ectomycorrhizal plants confirmed a living status. Tuber species, and likely other ectomycorrhizal fungi found in nonectomycorrhizal plant roots in this study, can be root endophytes. This is relevant for the ecology (brûlé formation) and commercial production of truffles. Evolutionarily speaking, endophytism may be an ancestral trait in some ectomycorrhizal fungi that evolved from root endophytes.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2542-2556Informations de copyright
© 2019 The Authors New Phytologist © 2019 New Phytologist Trust.
Références
Almario J, Jeena G, Wunder J, Langen G, Zuccaro A, Coupland G, Bucher M. 2017. Root-associated fungal microbiota of nonmycorrhizal Arabis alpina and its contribution to plant phosphorus nutrition. Proceedings of the National Academy of Sciences, USA 114: E9403-E9412.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. Journal of Molecular Biology 215: 403-410.
Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA. 1990. Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl. Environ. Microbiol. 56: 1919-1925.
Angelini P, Tirillini B, Properzi A, Rol C, Venanzoni R. 2015. Identification and bioactivity of the growth inhibitors in Tuber spp. methanolic extracts. Plant Biosystems 149: 1000-1009.
Antony-Babu S, Deveau A, Nostrand JDV, Zhou J, Tacon FL, Robin C, Frey-Klett P, Uroz S. 2014. Black truffle-associated bacterial communities during the development and maturation of Tuber melanosporum ascocarps and putative functional roles. Environmental Microbiology 16: 2831-2847.
Arnaud-Haond S, Belkhir K. 2007. GENCLONE: a computer program to analyse genotypic data, test for clonality and describe spatial clonal organization. Molecular Ecology Notes 7: 15-17.
Behie SW, Zelisko PM, Bidochka MJ. 2012. Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336: 1576-1577.
Bertaux J, Schmid M, Prevost-Boure NC, Churin JL, Hartmann A, Garbaye J, Frey-Klett P. 2003. In situ identification of intracellular bacteria related to Paenibacillus spp. in the mycelium of the ectomycorrhizal fungus Laccaria bicolor. Applied and Environmental Microbiology 69: 4243-4248.
Bödeker ITM, Clemmensen KE, de Boer W, Martin F, Olson Å, Lindahl BD. 2014. Ectomycorrhizal Cortinarius species participate in enzymatic oxidation of humus in northern forest ecosystems. New Phytologist 203: 245-256.
Bonito G, Smith ME, Nowak M, Healy RA, Guevara G, Cázares E, Kinoshita A, Nouhra ER, Domínguez LS, Tedersoo L et al. 2013. Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage (JE Stajich, Ed.). PLoS ONE 8: e52765.
Bougoure DS, Parkin PI, Cairney JWG, Alexander IJ, Anderson IC. 2007. Diversity of fungi in hair roots of Ericaceae varies along a vegetation gradient. Molecular Ecology 16: 4624-4636.
Brundrett MC, Tedersoo L. 2018. Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytologist 220: 1108-1115.
Cao L, Qiu Z, You J, Tan H, Zhou S. 2004. Isolation and characterization of endophytic Streptomyces strains from surface-sterilized tomato (Lycopersicon esculentum) roots. Letters in applied microbiology 39: 425-430.
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7: 335-336.
Chauvet E, Cornut J, Sridhar KR, Selosse M-A, Bärlocher F. 2016. Beyond the water column: aquatic hyphomycetes outside their preferred habitat. Fungal Ecology 19: 112-127.
De la Varga H, Le Tacon F, Lagoguet M, Todesco F, Varga T, Miquel I, Barry-Etienne D, Robin C, Halkett F, Martin F et al. 2017. Five years investigation of female and male genotypes in périgord black truffle (Tuber melanosporum Vittad.) revealed contrasted reproduction strategies. Environmental Microbiology 19: 2604-2615.
Delaux P-M, Varala K, Edger PP, Coruzzi GM, Pires JC, Ané J-M. 2014. Comparative phylogenomics uncovers the impact of symbiotic associations on host genome evolution. PLoS Genetics 10: e1004487.
Deveau A, Clowez P, Petit F, Maurice J-P, Todesco F, Murat C, Harroué M, Ruelle J, Le Tacon F. 2019. New insights into black truffle biology: discovery of the potential connecting structure between a Tuber aestivum ascocarp and its host root. Mycorrhiza 29: 219-226.
Dighton J, White JF. 2017. The fungal community: its organization and role in the ecosystem. Rotterdam, the Netherlands: CRC Press.
Douet JP, Castroviejo M, Mabru D, Chevalier G, Dupré C, Bergougnoux F, Ricard JM, Médina B. 2004. Rapid molecular typing of Tuber melanosporum, T. brumale and T. indicum from tree seedlings and canned truffles. Analytical and Bioanalytical Chemistry 379: 668-673.
Dupont J, Dequin S, Giraud T, Tacon FL, Marsit S, Ropars J, Richard F, Selosse M-A. 2017. Fungi as a source of food. Microbiology Spectrum 5: 1-22.
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R. 2011. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27: 2194-2200.
Girlanda M, Selosse MA, Cafasso D, Brilli F, Delfine S, Fabbian R, Ghignone S, Pinelli P, Segreto R, Loreto F et al. 2006. Inefficient photosynthesis in the Mediterranean orchid Limodorum abortivum is mirrored by specific association to ectomycorrhizal Russulaceae. Molecular Ecology 15: 491-504.
Gonneau C, Jersáková J, de Tredern E, Till-Bottraud I, Saarinen K, Sauve M, Roy M, Hájek T, Selosse M-A. 2015. Photosynthesis in perennial mixotrophic Epipactis spp. (Orchidaceae) contributes more to shoot and fruit biomass than to hypogeous survival. Journal of Ecology 102: 1183-1194.
Gryndler M, Černá L, Bukovská P, Hršelová H, Jansa J. 2014. Tuber aestivum association with non-host roots. Mycorrhiza 24: 603-610.
Gryndler M, Trilčová J, Hršelová H, Streiblová E, Gryndlerová H, Jansa J. 2013. Tuber aestivum Vittad. mycelium quantified: advantages and limitations of a qPCR approach. Mycorrhiza 23: 341-348.
Hansen K, Perry BA, Dranginis AW, Pfister DH. 2013. A phylogeny of the highly diverse cup-fungus family Pyronemataceae (Pezizomycetes, Ascomycota) clarifies relationships and evolution of selected life history traits. Molecular Phylogenetics and Evolution 67: 311-335.
Hardoim PR, van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A. 2015. The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiology and Molecular Biology Reviews 79: 293-320.
Harrington TJ, Mitchell DT. 2002. Colonization of root systems of Carex flacca and C. pilulifera by Cortinarius (Dermocybe) cinnamomeus. Mycological Research 106: 452-459.
van der Heijden MGA, Martin FM, Selosse M-A, Sanders IR. 2015. Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytologist 205: 1406-1423.
Hess J, Pringle A. 2014. The natural histories of species and their genomes. Advances in Botanical Research 70: 235-257.
Hibbett DS, Ohman A, Kirk PM. 2009. Fungal ecology catches fire. New Phytologist 184: 279-282.
Huang J-Y, Hu H-T, Shen W-C. 2009. Phylogenetic study of two truffles, Tuber formosanum and Tuber furfuraceum, identified from Taiwan. FEMS Microbiology Letters 294: 157-171.
Jacquemyn H, Waud M, Brys R, Lallemand F, Courty P-E, Robionek A, Selosse M-A. 2017. Mycorrhizal associations and trophic modes in coexisting orchids: an ecological continuum between auto- and mixotrophy. Frontiers in Plant Science 8: 1497.
Klironomos JN, Hart MM. 2001. Animal nitrogen swap for plant carbon. Nature 410: 651-652.
Kohler A, Kuo A, Nagy LG, Morin E, Barry KW, Buscot F, Canbäck B, Choi C, Cichocki N, Clum A et al. 2015. Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists. Nature Genetics 47: 410-415.
Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM et al. 2013. Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology 22: 5271-5277.
Le Tacon F. 2017. Les Truffes. Biologie, écologie et domestication. Nancy, France: AgroParisTech.
Le Tacon F, Zeller B, Plain C, Hossann C, Bréchet C, Martin F, Kohler A, Villerd J, Robin C. 2015. Study of nitrogen and carbon transfer from soil organic matter to Tuber melanosporum mycorrhizas and ascocarps using 15N and 13C soil labelling and whole-genome oligoarrays. Plant and Soil 395: 351-373.
Le Tacon F, Zeller B, Plain C, Hossann C, Bréchet C, Robin C. 2013. Carbon transfer from the host to Tuber melanosporum mycorrhizas and ascocarps followed using a 13C pulse-labeling technique (P Shaw, Ed.). PLoS ONE 8: e64626.
Leonardi P, Murat C, Puliga F, Iotti M, Zambonelli A. 2019. Ascoma genotyping and mating type analyses of mycorrhizas and soil mycelia of Tuber borchii in a truffle orchard established by mycelial inoculated plants. Environmental Microbiology. doi: 10.1111/1462-2920.14777.
Lofgren LA, LeBlanc NR, Certano AK, Nachtigall J, LaBine KM, Riddle J, Broz K, Dong Y, Bethan B, Kafer CW et al. 2018. Fusarium graminearum: pathogen or endophyte of North American grasses? New Phytologist 217: 1203-1212.
Mahé F, Rognes T, Quince C, de Vargas C, Dunthorn M. 2014. Swarm: robust and fast clustering method for amplicon-based studies. PeerJ 2: e593.
Mamoun M, Olivier JM. 1997. Mycorrhizal inoculation of cloned hazels by Tuber melanosporum: effect of soil disinfestation and co-culture with Festuca ovina. Plant and Soil 188: 221-226.
Martegoute J-C, Courdeau A. 2002. Plantes des Causses et des truffières. Périgueux, France: Fédération Départementale des trufficulteurs du Périgord.
Martin M. 2011. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.journal 17: 10-12.
Martin F, Kohler A, Murat C, Balestrini R, Coutinho PM, Jaillon O, Montanini B, Morin E, Noel B, Percudani R et al. 2010. Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464: 1033-1038.
Mello A, Lumini E, Napoli C, Bianciotto V, Bonfante P. 2015. Arbuscular mycorrhizal fungal diversity in the Tuber melanosporum brûlé. Fungal Biology 19: 518-527.
Molinier V, Bouffaud M-L, Castel T, Mounier A, Colombet A, Recorbet G, Frochot H, Wipf D. 2013a. Monitoring the fate of a 30-year-old truffle orchard in Burgundy: from Tuber melanosporum to Tuber aestivum. Agroforestry Systems 87: 1439-1449.
Molinier V, Murat C, Frochot H, Wipf D, Splivallo R. 2015. Fine-scale spatial genetic structure analysis of the black truffle Tuber aestivum and its link to aroma variability. Environmental Microbiology 17: 3039-3050.
Molinier V, Murat C, Morin E, Gollotte A, Wipf D, Martin F. 2013b. First identification of polymorphic microsatellite markers in the Burgundy truffle, Tuber aestivum (Tuberaceae). Applications in Plant Sciences 1: 1200220.
Molinier V, Murat C, Peter M, Gollotte A, De la Varga H, Meier B, Egli S, Belfiori B, Paolocci F, Wipf D. 2016. SSR-based identification of genetic groups within European populations of Tuber aestivum Vittad. Mycorrhiza 26: 99-110.
Murat C. 2015. Forty years of inoculating seedlings with truffle fungi: past and future perspectives. Mycorrhiza 25: 77-81.
Murat C, Kuo A, Barry KW, Clum A, Dockter RB, Fauchery L, Iotti M, Kohler A, LaButti K, Lindquist EA et al. 2018. Draft genome sequence of Tuber borchii Vittad., a whitish edible truffle. Genome Announcements 6: e00537-18.
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 Genetics and Biology 48: 592-601.
Murat C, Rubini A, Riccioni C, De la Varga H, Akroume E, Belfiori B, Guaragno M, Le Tacon F, Robin C, Halkett F et al. 2013. Fine-scale spatial genetic structure of the black truffle (Tuber melanosporum ) investigated with neutral microsatellites and functional mating type genes. New Phytologist 199: 176-187.
Murata H, Yamada A, Maruyama T, Endo N, Yamamoto K, Ohira T, Shimokawa T. 2013. Root endophyte interaction between ectomycorrhizal basidiomycete Tricholoma matsutake and arbuscular mycorrhizal tree Cedrela odorata, allowing in vitro synthesis of rhizospheric “shiro”. Mycorrhiza 23: 235-242.
Murata H, Yamada A, Yokota S, Maruyama T, Endo N, Yamamoto K, Ohira T, Neda H. 2014. Root endophyte symbiosis in vitro between the ectomycorrhizal basidiomycete Tricholoma matsutake and the arbuscular mycorrhizal plant Prunus speciosa. Mycorrhiza 24: 315-321.
Newsham KK. 2011. A meta-analysis of plant responses to dark septate root endophytes. New Phytologist 190: 783-793.
Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG. 2016. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecology 20: 241-248.
Nilsson RH, Anslan S, Bahram M, Wurzbacher C, Baldrian P, Tedersoo L. 2019. Mycobiome diversity: high-throughput sequencing and identification of fungi. Nature Reviews Microbiology 17: 95-109.
Olivera A, Fischer CR, Bonet JA, Martínez de Aragón J, Oliach D, Colinas C. 2011. Weed management and irrigation are key treatments in emerging black truffle (Tuber melanosporum) cultivation. New Forests 42: 227-239.
Olivier J-M, Savignac J-C, Sourzat P. 2012. Truffe et trufficulture. Périgueux, France: Pierre Fanlac (Fanlac edition).
Pacioni G. 1991. Effects of Tuber metabolites on the rhizospheric environment. Mycological Research 95: 1355-1358.
Paolocci F, Rubini A, Granetti B, Arcioni S. 1999. Rapid molecular approach for a reliable identification of Tuber spp. ectomycorrhizae. FEMS Microbiology Ecology 28: 23-30.
Paolocci F, Rubini A, Riccioni C, Arcioni S. 2006. Reevaluation of the life cycle of Tuber magnatum. Applied and Environmental Microbiology 72: 2390-2393.
Plattner I, Hall IR. 1995. Parasitism of non-host plants by the mycorrhizal fungus Tuber melanosporum. Mycological Research 99: 1367-1370.
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 Phytologist 180: 466-478.
Rineau F, Shah F, Smits MM, Persson P, Johansson T, Carleer R, Troein C, Tunlid A. 2013. Carbon availability triggers the decomposition of plant litter and assimilation of nitrogen by an ectomycorrhizal fungus. The ISME Journal 7: 2010-2022.
Rodriguez RJ, White JF Jr, Arnold AE, Redman RS. 2009. Fungal endophytes: diversity and functional roles. New Phytologist 182: 314-330.
Rubini A, Belfiori B, Riccioni C, Arcioni S, Martin F, Paolocci F. 2011a. 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 Phytologist 189: 723-735.
Rubini A, Belfiori B, Riccioni C, Tisserant E, Arcioni S, Martin F, Paolocci F. 2011b. Isolation and characterization of MAT genes in the symbiotic ascomycete Tuber melanosporum. New Phytologist 189: 710-722.
Schiebold JM-I, Bidartondo MI, Karasch P, Gravendeel B, Gebauer G. 2017. You are what you get from your fungi: nitrogen stable isotope patterns in Epipactis species. Annals of Botany 119: 1085-1095.
Schneider-Maunoury L, Leclercq S, Clément C, Covès H, Lambourdière J, Sauve M, Richard F, Selosse M-A, Taschen E. 2018. Is Tuber melanosporum colonizing the roots of herbaceous, non-ectomycorrhizal plants? Fungal Ecology 31: 59-68.
Selosse M-A, Dubois M-P, Alvarez N. 2009. Do Sebacinales commonly associate with plant roots as endophytes? Mycological Research 113: 1062-1069.
Selosse M-A, Faccio A, Scappaticci G, Bonfante P. 2004. Chlorophyllous and achlorophyllous specimens of Epipactis microphylla (Neottieae, Orchidaceae) are associated with ectomycorrhizal Septomycetes, including truffles. Microbial Ecology 47: 416-426.
Selosse M-A, Martos F. 2014. Do chlorophyllous orchids heterotrophically use mycorrhizal fungal carbon? Trends in Plant Science 19: 683-685.
Selosse M-A, Martos F, Perry BA, Padamsee M, Roy M, Pailler T. 2010. Saprotrophic fungal mycorrhizal symbionts in achlorophyllous orchids. Plant Signaling & Behavior 5: 1-5.
Selosse M-A, Roy M. 2009. Green plants that feed on fungi: facts and questions about mixotrophy. Trends in Plant Science 14: 64-70.
Selosse M-A, Schneider-Maunoury L, Martos F. 2018. Time to re-think fungal ecology? Fungal ecological niches are often prejudged. New Phytologist 217: 968-972.
Selosse M-A, Schneider-Maunoury L, Taschen E, Rousset F, Richard F. 2017. Black truffle, a hermaphrodite with forced unisexual behaviour. Trends in Microbiology 25: 784-787.
Selosse M-A, Taschen E, Giraud T. 2013. Do black truffles avoid sexual harassment by linking mating type and vegetative incompatibility? New Phytologist 199: 10-13.
Shefferson RP, WeIß M, Kull T, Taylor DL. 2005. High specificity generally characterizes mycorrhizal association in rare lady's slipper orchids, genus Cypripedium. Molecular Ecology 14: 613-626.
Smith SE, Read D. 2008. Mycorrhizal symbiosis. London, UK: Academic Press.
Splivallo R, Fischer U, Göbel C, Feussner I, Karlovsky P. 2009. Truffles regulate plant root morphogenesis via the production of auxin and ethylene. Plant Physiology 150: 2018-2029.
Splivallo R, Vahdatzadeh M, Maciá-Vicente JG, Molinier V, Peter M, Egli S, Uroz S, Paolocci F, Deveau A. 2019. Orchard conditions and fruiting body characteristics drive the microbiome of the Black Truffle Tuber aestivum. Frontiers in Microbiology 10: 1437.
Streiblová E, Gryndlerová H, Gryndler M. 2012. Truffle brûlé: an efficient fungal life strategy. FEMS Microbiology Ecology 80: 1-8.
Taschen E, Rousset F, Sauve M, Benoit L, Dubois M-P, Richard F, Selosse M-A. 2016. How the truffle got its mate: insights from genetic structure in spontaneous and planted Mediterranean populations of Tuber melanosporum. Molecular Ecology 25: 5611-5627.
Taschen E, Sauve M, Taudiere A, Parlade J, Selosse M-A, Richard F. 2015. Whose truffle is this? Distribution patterns of ectomycorrhizal fungal diversity in Tuber melanosporum brûlés developed in multi-host Mediterranean plant communities. Environmental Microbiology 17: 2747-2761.
Taschen E, Sauve M, Vincent B, Parladé J, van Tuinen D, Aumeeruddy-Thomas Y, Assenat B, Selosse M-A, Richard F. 2019. Insight into the truffle brûlé: tripartite interactions between the black truffle (Tuber melanosporum), holm oak (Quercus ilex) and arbuscular mycorrhizal plants. Plant and Soil, in press. doi: 10.1007/s11104-019-04340-2.
Todesco F, Belmondo S, Guignet Y, Laurent L, Fizzala S, Le Tacon F, Murat C. 2019. Soil temperature and hydric potential influences the monthly variations of soil Tuber aestivum DNA in a highly productive orchard. Scientific Reports 9: 12964.
Toju H, Sato H. 2018. Root-associated fungi shared between arbuscular mycorrhizal and ectomycorrhizal conifers in a temperate forest. Frontiers in Microbiology 9: 433.
Vandenkoornhuyse P, Baldauf SL, Leyval C, Straczek J, Young JPW. 2002. Extensive fungal diversity in plant roots. Science 295: 2051.
Wang Z, Johnston PR, Takamatsu S, Spatafora JW, Hibbett DS. 2006. Toward a phylogenetic classification of the Leotiomycetes based on rDNA data. Mycologia 98: 1065-1075.
Weiß M, Sýkorová Z, Garnica S, Riess K, Martos F, Krause C, Oberwinkler F, Bauer R, Redecker D. 2011. Sebacinales everywhere: previously overlooked ubiquitous fungal endophytes. PLoS ONE 6: e16793.
Weiß M, Waller F, Zuccaro A, Selosse M-A. 2016. Sebacinales - one thousand and one interactions with land plants. New Phytologist 211: 20-40.
Wilson D. 1995. Endophyte: the evolution of a term, and clarification of its use and definition. Oikos 73: 274-276.
Zambonelli A, Iotti M, Murat C. 2016. True truffle (Tuber spp.) in the world: soil ecology, systematics and biochemistry. New York, NY, USA: Springer.
Zeller B, Bréchet C, Maurice J-P, Tacon F. 2008. Saprotrophic versus symbiotic strategy during truffle ascocarp development under holm oak. A response based on 13C and 15N natural abundance. Annals of Forest Science 65: 607-607.
Zuccaro A, Lahrmann U, Güldener U, Langen G, Pfiffi S, Biedenkopf D, Wong P, Samans B, Grimm C, Basiewicz M et al. 2011. Endophytic life strategies decoded by genome and transcriptome analyses of the mutualistic root symbiont Piriformospora indica. PLoS Pathogens 7: e1002290.