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      New Insights into the Complex Relationship between Weight and Maturity of Burgundy Truffles ( Tuber aestivum)

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          Abstract

          Despite an increasing demand for Burgundy truffles ( Tuber aestivum), gaps remain in our understanding of the fungus’ overall lifecycle and ecology. Here, we compile evidence from three independent surveys in Hungary and Switzerland. First, we measured the weight and maturity of 2,656 T. aestivum fruit bodies from a three-day harvest in August 2014 in a highly productive orchard in Hungary. All specimens ranging between 2 and 755 g were almost evenly distributed through five maturation classes. Then, we measured the weight and maturity of another 4,795 T. aestivum fruit bodies harvested on four occasions between June and October 2015 in the same truffière. Again, different maturation stages occurred at varying fruit body size and during the entire fruiting season. Finally, the predominantly unrelated weight and maturity of 81 T. aestivum fruit bodies from four fruiting seasons between 2010 and 2013 in Switzerland confirmed the Hungarian results. The spatiotemporal coexistence of 7,532 small-ripe and large-unripe T. aestivum, which accumulate to ~182 kg, differs from species-specific associations between the size and ripeness that have been reported for other mushrooms. Although size-independent truffle maturation stages may possibly relate to the perpetual belowground environment, the role of mycelial connectivity, soil property, microclimatology, as well as other abiotic factors and a combination thereof, is still unclear. Despite its massive sample size and proof of concept, this study, together with existing literature, suggests consideration of a wider ecological and biogeographical range, as well as the complex symbiotic fungus-host interaction, to further illuminate the hidden development of belowground truffle fruit bodies.

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          The mycorrhiza helper bacteria revisited.

          In natural conditions, mycorrhizal fungi are surrounded by complex microbial communities, which modulate the mycorrhizal symbiosis. Here, the focus is on the so-called mycorrhiza helper bacteria (MHB). This concept is revisited, and the distinction is made between the helper bacteria, which assist mycorrhiza formation, and those that interact positively with the functioning of the symbiosis. After considering some examples of MHB from the literature, the ecological and evolutionary implications of the relationships of MHB with mycorrhizal fungi are discussed. The question of the specificity of the MHB effect is addressed, and an assessment is made of progress in understanding the mechanisms of the MHB effect, which has been made possible through the development of genomics. Finally, clear evidence is presented suggesting that some MHB promote the functioning of the mycorrhizal symbiosis. This is illustrated for three critical functions of practical significance: nutrient mobilization from soil minerals, fixation of atmospheric nitrogen, and protection of plants against root pathogens. The review concludes with discussion of future research priorities regarding the potentially very fruitful concept of MHB.
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            Fruiting body production in Basidiomycetes.

            Mushroom cultivation presents an economically important biotechnological industry that has markedly expanded all over the world in the past few decades. Mushrooms serve as delicacies for human consumption and as nutriceuticals, as "food that also cures". Mushrooms, the fruiting bodies of basidiomycetous fungi, contain substances of various kinds that are highly valued as medicines, flavourings and perfumes. Nevertheless, the biological potential of mushrooms is probably far from exploited. A major problem up to now is that only a few species can be induced to fruit in culture. Our current knowledge on the biological processes of fruiting body initiation and development is limited and arises mostly from studies of selected model organisms that are accessible to molecular genetics. A better understanding of the developmental processes underlying fruiting in these model organisms is expected to help mushroom cultivation of other basidiomycetes in the future.
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              Historical Biogeography and Diversification of Truffles in the Tuberaceae and Their Newly Identified Southern Hemisphere Sister Lineage

              Truffles have evolved from epigeous (aboveground) ancestors in nearly every major lineage of fleshy fungi. Because accelerated rates of morphological evolution accompany the transition to the truffle form, closely related epigeous ancestors remain unknown for most truffle lineages. This is the case for the quintessential truffle genus Tuber, which includes species with socio-economic importance and esteemed culinary attributes. Ecologically, Tuber spp. form obligate mycorrhizal symbioses with diverse species of plant hosts including pines, oaks, poplars, orchids, and commercially important trees such as hazelnut and pecan. Unfortunately, limited geographic sampling and inconclusive phylogenetic relationships have obscured our understanding of their origin, biogeography, and diversification. To address this problem, we present a global sampling of Tuberaceae based on DNA sequence data from four loci for phylogenetic inference and molecular dating. Our well-resolved Tuberaceae phylogeny shows high levels of regional and continental endemism. We also identify a previously unknown epigeous member of the Tuberaceae – the South American cup-fungus Nothojafnea thaxteri (E.K. Cash) Gamundí. Phylogenetic resolution was further improved through the inclusion of a previously unrecognized Southern hemisphere sister group of the Tuberaceae. This morphologically diverse assemblage of species includes truffle (e.g. Gymnohydnotrya spp.) and non-truffle forms that are endemic to Australia and South America. Southern hemisphere taxa appear to have diverged more recently than the Northern hemisphere lineages. Our analysis of the Tuberaceae suggests that Tuber evolved from an epigeous ancestor. Molecular dating estimates Tuberaceae divergence in the late Jurassic (∼156 million years ago), with subsequent radiations in the Cretaceous and Paleogene. Intra-continental diversification, limited long-distance dispersal, and ecological adaptations help to explain patterns of truffle evolution and biodiversity.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                26 January 2017
                2017
                : 12
                : 1
                : e0170375
                Affiliations
                [1 ]Department of Geography, University of Cambridge, Cambridge, United Kingdom
                [2 ]Swiss Federal Research Institute WSL, Birmensdorf, Switzerland
                [3 ]CzechGlobe Research Institute CAS and Masaryk University Brno, Brno, Czech Republic
                [4 ]Truffleminers Ltd, Taksony Kinizsi, Hungary
                [5 ]Goethe University Frankfurt, Institute for Molecular Bio Science, Frankfurt, Germany
                [6 ]Integrative Fungal Research Cluster (IPF), Frankfurt, Germany
                [7 ]UMR 5175 CEFE - University of Montpellier, Montpellier, France
                [8 ]Université de Lorraine, UMR1136 Interactions Arbres-Microorganismes, Vandoeuvre-lès-Nancy, France
                [9 ]INRA, UMR1136 Interactions Arbres-Microorganismes, Champenoux, France
                [10 ]Chair of Forest Growth, Albert-Ludwigs University, Freiburg, Germany
                [11 ]Chair of Forest Botany, Albert-Ludwigs University, Freiburg & Deutsche Trüffelbäume, Radolfzell, Germany
                [12 ]Agrifood Research and Technology Centre of Aragon CITA, Zaragoza, Spain
                [13 ]European Mycological Institute EGTC-EMI, Soria, Spain
                University of Perugia, ITALY
                Author notes

                Competing Interests: We have the following interests: István Bagi and Oszkár Fekete are employed by Truffleminers Ltd. However, there are no patents, products in development or marketed products to declare. This does not alter our adherence to all the PLOS ONE policies on sharing data and materials, as detailed online in the guide for authors.

                • Conceptualization: UB SE.

                • Formal analysis: UB SE IB VM MP DN BM RS LH.

                • Funding acquisition: UB RS IB OF CM.

                • Investigation: UB IB VM MP RS MV DN BM SE.

                • Methodology: UB RS SE.

                • Project administration: UB SE IB OF.

                • Resources: OF RS.

                • Supervision: UB.

                • Visualization: UB IB OF RS MV SE.

                • Writing – original draft: UB VM MP RS FR CM WT US FMP LS SE.

                • Writing – review & editing: UB SE LH.

                Article
                PONE-D-16-33354
                10.1371/journal.pone.0170375
                5268403
                28125633
                5a1e3611-e1c8-40df-be33-ad229937395e
                © 2017 Büntgen et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 20 August 2016
                : 4 January 2017
                Page count
                Figures: 7, Tables: 0, Pages: 15
                Funding
                Supported by the WSL-internal DITREC project, the Ernst Göhner Foundation, as well as the Swiss State Secretariat for Education, Research and Innovation (SERI): COST Action FP1203. Moreover, U. Büntgen received funding from the Ministry of Education, Youth and Sports of CR within the National Sustainability Program I (NPU I), grant number LO1415., whereas R. Splivallo and M. Vahdatzadeh were supported by the LOEWE research-funding program of the government of Hessen, in the framework of the Integrative Fungal Research Cluster (IPF) and by the German Research Foundation (DFG) – grant number 1191/4-1. The UMR1136 is supported by a grant overseen by the French National Research Agency (ANR) as part of the "Investissements d'Avenir" program (ANR-11-LABX-0002-01, Lab of Excellence ARBRE). Truffleminers Ltd provided support in the form of salaries for authors [IB, OF], but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section. The funder provided support in the form of salaries for authors [UB, RS, MV, CM, IB, OF], but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.
                Categories
                Research Article
                Biology and Life Sciences
                Agriculture
                Crop Science
                Crops
                Fruits
                Biology and Life Sciences
                Organisms
                Plants
                Fruits
                Biology and Life Sciences
                Agriculture
                Farms
                Orchards
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Dogs
                Earth Sciences
                Seasons
                Ecology and Environmental Sciences
                Soil Science
                Soil Ecology
                Biology and Life Sciences
                Physiology
                Physiological Parameters
                Body Weight
                Medicine and Health Sciences
                Physiology
                Physiological Parameters
                Body Weight
                Biology and Life Sciences
                Biogeography
                Ecology and Environmental Sciences
                Biogeography
                Earth Sciences
                Geography
                Biogeography
                Physical Sciences
                Materials Science
                Materials by Attribute
                Pigments
                Organic Pigments
                Melanin
                Custom metadata
                All data are included in the supplementary material.

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