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      Truffle biogeography—A case study revealing ecological niche separation of different Tuber species

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          Abstract

          Ecology of hypogeic mycorrhizal fungi, such as truffles, remains largely unknown, both in terms of their geographical distribution and their environmental niches. Occurrence of true truffles ( Tuber spp.) was therefore screened using specific polymerase chain reaction ( PCR) assays and subsequent PCR amplicon sequencing in tree roots collected at 322 field sites across the Czech Republic. These sites spanned a wide range of climatic and soil conditions. The sampling was a priori restricted to areas thought to be suitable for Tuber spp. inasmuch as they were characterized by weakly acidic to alkaline soils, warmer climate, and with tree species previously known to host true truffles. Eight operational taxonomic units ( OTUs) corresponding to Tuber aestivum, T. borchii, T. foetidum, T. rufum, T. indicum, T. huidongense, T. dryophilum, and T. oligospermum were detected. Among these, T. borchii was the OTU encountered most frequently. It was detected at nearly 19% of the sites. Soil pH was the most important predictor of Tuber spp. distribution. Tuber borchii preferred weakly acidic soils, T. foetidum and T. rufum were most abundant in neutral soils, and T. huidongense was restricted to alkaline soils. Distribution of T. aestivum was mainly dictated by climate, with its range restricted to the warmest sites. Host preferences of the individual Tuber spp. were weak compared to soil and climatic predictors, with the notable exception that T. foetidum appeared to avoid oak trees. Our results open the way to better understanding truffle ecology and, through this new knowledge, also to better‐informed trufficulture.

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          Most cited references 51

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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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            A global meta-analysis of Tuber ITS rDNA sequences: species diversity, host associations and long-distance dispersal.

            Truffles (Tuber) are ectomycorrhizal fungi characterized by hypogeous fruitbodies. Their biodiversity, host associations and geographical distributions are not well documented. ITS rDNA sequences of Tuber are commonly recovered from molecular surveys of fungal communities, but most remain insufficiently identified making it difficult to determine whether these sequences represent conspecific or novel taxa. In this meta-analysis, over 2000 insufficiently identified Tuber sequences from 76 independent studies were analysed within a phylogenetic framework. Species ranges, host associates, geographical distributions and intra- and interspecific ITS variability were assessed. Over 99% of the insufficiently identified Tuber sequences grouped within clades composed of species with little culinary value (Maculatum, Puberulum and Rufum). Sixty-four novel phylotypes were distinguished including 36 known only from ectomycorrhizae or soil. Most species of Tuber showed 1-3% intraspecific ITS variability and >4% interspecific ITS sequence variation. We found 123 distinct phylotypes based on 96% ITS sequence similarity and estimated that Tuber contains a minimum of 180 species. Based on this meta-analysis, species in Excavatum, Maculatum and Rufum clades exhibit preference for angiosperm hosts, whereas those in the Gibbosum clade are preferential towards gymnosperms. Sixteen Tuber species (>13% of the known diversity) have putatively been introduced to continents or islands outside their native range. © 2010 Blackwell Publishing Ltd.
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              Correspondence Analysis of Incidence and Abundance Data: Properties in Terms of a Unimodal Response Model

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                Author and article information

                Contributors
                gryndler@biomed.cas.cz
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                07 May 2017
                June 2017
                : 7
                : 12 ( doiID: 10.1002/ece3.2017.7.issue-12 )
                : 4275-4288
                Affiliations
                [ 1 ] Faculty of SciencesJan Evangelista Purkyně University in Ústí nad Labem Ústí nad LabemCzech Republic
                [ 2 ] Laboratory of Fungal Biology Institute of MicrobiologyAcademy of Sciences of the Czech Republic PragueCzech Republic
                [ 3 ] Faculty of ScienceUniversity of South Bohemia České BudějoviceCzech Republic
                Author notes
                [* ] Correspondence

                Milan Gryndler, Faculty of Sciences, Jan Evangelista Purkyně University in Ústí nad Labem, Ústí nad Labem, Czech Republic.

                Email: gryndler@ 123456biomed.cas.cz

                Article
                ECE33017
                10.1002/ece3.3017
                5478065
                © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 4, Tables: 5, Pages: 14, Words: 10874
                Product
                Funding
                Funded by: Grantová Agentura České Republiky
                Award ID: 14‐36079G
                Award ID: P504/10/0382
                Funded by: Ministerstvo Školství, Mládeže a Tělovýchovy
                Award ID: LM2015073
                Award ID: RVO61388971
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece33017
                June 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.1.1 mode:remove_FC converted:20.06.2017

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