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Rhizopogon confusus sp. nov., a correct name for a fungus previously recorded in Central Europe as the North American Rhizopogon salebrosus

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Abstract

Rhizopogon salebrosus, a common species found in western North America, has been recently considered an invasive species in Europe, based on ITS rDNA sequence records from ectomycorrhizal root tips. We collected in montane and submontane coniferous forests (both plantations and unmanaged forests) in the Czech Republic and Slovakia basidiocarps of a species with morphology similar to R. salebrosus. Analysis of sequences of ITS rDNA showed that our collections together with further records from Europe belonged into the R. salebrosus species group. In contrary, they formed a well-supported clade based on analysis of a gene for RNA polymerase II second largest subunit and one anonymous nuclear locus developed for better resolution in the R. salebrosus species group. Evidence from the three genes and distinct phenotypic characteristics show that the European collections represent a novel species within R. salebrosus species group that is described herein as R. confusus. Host affinity of R. confusus, its native presence in Europe and implications for the presumed invasion of R. salebrosus in Europe are discussed.

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Data availability

Sequences were submitted in GenBank and voucher specimens are deposited in herbaria.

References

  • Abadi S, Azouri D, Pupko T, Mayrose I (2019) Model selection may not be a mandatory step for phylogeny reconstruction. Nat Commun 10(1):934. https://doi.org/10.1038/s41467-019-08822-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215(2):403–410

    Article  CAS  Google Scholar 

  • Bidartondo MI, Bruns TD (2002) Fine-level mycorrhizal specificity in the Monotropoideae (Ericaceae): specificity for fungal species group. Mol Ecol 11:557–569

    Article  CAS  Google Scholar 

  • Chapela IH, Osher LJ, Horton TR, Henn MR (2001) Ectomycorrhizal fungi introduced with exotic pine plantations induce soil carbon depletion. Soil Biol Biochem 33:1733–1740

    Article  CAS  Google Scholar 

  • Cowden CC, Peterson CJ (2013) Annual and seasonal dynamics of ectomycorrhizal fungi colonizing white pine (Pinus strobus) seedlings following catastrophic windthrow in northern Georgia, USA. Can J For Res 43(3):215–223. https://doi.org/10.1139/cjfr-2012-0410

    Article  Google Scholar 

  • Deckerová H (2015) Rhizopogon villosulus – a hypogeous species new to the Czech Republic. Mykol Listy 130:26–32

    Google Scholar 

  • Dowie NJ (2019) Cryptic ecological specificity linked to species divergence in a co-phylogeographic evaluation of a tripartite symbiosis (an achlorophyllous plant, ectomycorrhizal fungi, and conifers), Ph.D. Thesis, University of Wyoming

  • Dowie NJ, Hemenway JJ, Trowbridge SM, Miller SL (2011) Mycobiont overlap between two mycoheterotrophic genera of Monotropoideae (Pterospora andromedea and Sarcodes sanguinea) found in the Greater Yellowstone Ecosystem. Symbiosis 54(1):29–36

    Article  Google Scholar 

  • Dowie NJ, Hemenway JJ, Miller SL (2012) Identity, genetic lineages and putative hybrids of an obligate mycobiont associated with the mycoheterotrophic plant Pterospora andromedea in the south-central Rocky Mountains. Funct Ecol 5(2):137–146

    Article  Google Scholar 

  • Dowie NJ, Grubisha LC, Trowbridge SM, Klooster MR, Miller SL (2016) Variability of ecological and autotrophic host specificity in a mycoheterotrophic system: Pterospora andromedea and associated fungal and conifer hosts. Funct Ecol 20:97–107. https://doi.org/10.1016/j.funeco.2015.11.005

    Article  Google Scholar 

  • Dowie NJ, Grubisha LC, Burton BA, Klooster MR, Miller SL (2017) Increased phylogenetic resolution within the ecologically important Rhizopogon subgenus Amylopogon using 10 anonymous nuclear loci. Mycologia 109(1):35–45

    Article  CAS  Google Scholar 

  • Forin N, Nigris S, Voyron S, Girlanda M, Vizzini A, Casadoro G, Baldan B (2018) Next generation sequencing of ancient fungal specimens: the case of the Saccardo mycological herbarium. Front Ecol Evol 6(129):19. https://doi.org/10.3389/fevo.2018.00129

    Article  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  Google Scholar 

  • Gernandt DS, López GG, García SO, Aaron L (2005) Phylogeny and classification of Pinus. Taxon 54(1):29–42

    Article  Google Scholar 

  • Grubisha LC, Trappe JM, Molina R, Spatafora JW (2002) Biology of the ectomycorrhizal genus Rhizopogon. VI. Re-examination of infrageneric relationships inferred from phylogenetic analyses of ITS sequences. Mycologia 94(4):607–619

    Article  Google Scholar 

  • Grubisha LC, Bergemann SE, Bruns TD (2007) Host islands within the California Northern Channel Islands create fine-scale genetic structure in two sympatric species of the symbiotic ectomycorrhizal fungus Rhizopogon. Mol Ecol 16:1811–1822

    Article  Google Scholar 

  • Grubisha LC, Dowie NJ, Miller SL, Hazard C, Trowbridge SM, Horton TR, Klooster MR (2014) Rhizopogon kretzerae sp. nov.: the rare fungal symbiont in the tripartite system with Pterospora andromedea and Pinus strobus. Botany 92(7):527–534. https://doi.org/10.1139/cjb-2013-0309

    Article  CAS  Google Scholar 

  • Hazard C, Lilleskov EA, Horton TR (2012) Is rarity of pinedrops (Pterospora andromedea) in eastern North America linked to rarity of its unique fungal symbiont? Mycorrhiza 22(5):393–402. https://doi.org/10.1007/s00572-011-0414-y

    Article  PubMed  Google Scholar 

  • Hynson NA, Merckx VSFT, Perry BA, Treseder KK (2013) Identities and distributions of the co-invading ectomycorrhizal fungal symbionts of exotic pines in the Hawaiian Islands. Biol Invasions 15(11):2373–2385. https://doi.org/10.1007/s10530-013-0458-3

    Article  Google Scholar 

  • Kohout P, Sýkorová Z, Bahram M, Hadincová V, Albrechtová J, Tedersoo L, Vohník M (2011) Ericaceous dwarf shrubs affect ectomycorrhizal fungal community of the invasive Pinus strobus and native Pinus sylvestris in a pot experiment. Mycorrhiza 21(5):403–412. https://doi.org/10.1007/s00572-010-0350-2

    Article  PubMed  Google Scholar 

  • Kreisel H (2001) Checklist of the gasteral and secotioid Basidiornycetes of Europe, Africa, and the Middle East. Österr Z Pilzkd 10:213–313

    Google Scholar 

  • Krpata D, Mühlmann O, Kuhnert R, Ladurner H, Göbl F, Peintner U (2007) High diversity of ectomycorrhizal fungi associated with Arctostaphylos uva-ursi in subalpine and alpine zones: Potential inoculum for afforestation. For Ecol Manag 250(3):167–175. https://doi.org/10.1016/j.foreco.2007.05.012

    Article  Google Scholar 

  • Li LIN, Zhao Y, Zhou D, Yu F, Zheng L, Wang YUN, Zhang X, Duan Z, Zhao X, He Z, Li S (2016) Three new species of Rhizopogon from Southwest China. Phytotaxa 282(2):151–163. https://doi.org/10.11646/phytotaxa.282.2.7

    Article  Google Scholar 

  • Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Mol Biol Evol 16(12):1799–1808

    Article  CAS  Google Scholar 

  • Martín MP (1996) The genus Rhizopogon in Europe, vol 5. Societat Catalana de Micologia

    Google Scholar 

  • Martín MP (2001) Chorologic database of European Rhizopogon species. Mycotaxon 78:191–244

    Google Scholar 

  • Massicotte HB, Melville LH, Peterson RL, Molina R (1999) Biology of the ectomycorrhizal fungal genus, Rhizopogon - IV. Comparative morphology and anatomy of ectomycorrhizas synthesized between several Rhizopogon species on Ponderosa pine (Pinus ponderosa). New Phytol 142:355–370

    Article  Google Scholar 

  • Mujic AB, Huang B, Chen M-J, Wang P-H, Gernandt DG, Hosaka K, Spatafora JW (2019) Out of western North America: Evolution of the Rhizopogon-Pseudotsuga symbiosis inferred by genome-scale sequence typing. Funct Ecol 39:12–25

    Article  Google Scholar 

  • Nguyen NH, Hynson NA, Bruns TD (2012) Stayin' alive: survival of mycorrhizal fungal propagules from 6-yr-old forest soil. Funct Ecol 5(6):741–746. https://doi.org/10.1016/j.funeco.2012.05.006

    Article  Google Scholar 

  • Okuda Y, Shimomura N, Funato C, Nagasawa E, Matsumoto T (2013) Genetic variation among natural isolates of the ectomycorrhizal hypogenous fungus, Rhizopogon roseolus from Japanese pine forests inferred using AFLP markers. Mycoscience 54:13–18

    Article  Google Scholar 

  • Pietras M, Kolanowska M (2019) Predicted potential occurrence of the North American false truffle Rhizopogon salebrosus in Europe. Funct Ecol 39:225–230. https://doi.org/10.1016/j.funeco.2018.12.002

    Article  Google Scholar 

  • Policelli N, Bruns TD, Vilgalys R, Nunez MA (2019) Suilloid fungi as global drivers of pine invasions. New Phytol 222 (2):714–725. https://doi.org/10.1111/nph.15660

  • Rainer G, Kuhnert R, Unterholzer M, Dresch P, Gruber A, Peintner U (2015) Host-specialist dominated ectomycorrhizal communities of Pinus cembra are not affected by temperature manipulation. J Fungi 1(1):55–75

    Article  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542. https://doi.org/10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith AH, Zeller S (1966) A preliminary account of the North American species of Rhizopogon. Mem N Y Bot Gard 14(2):1–178

    Google Scholar 

  • Sulzbacher MA, Grebenc T, Garcia MA, Silva BD, Silveira A, Antoniolli ZI, Marinho P, Munzenberger B, Telleria MT, Baseia IG, Martín MP (2016) Molecular and morphological analyses confirm Rhizopogon verii as a widely distributed ectomycorrhizal false truffle in Europe, and its presence in South America. Mycorrhiza 26(5):377–388. https://doi.org/10.1007/s00572-015-0678-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Trappe JM, Evans F (2007) Field guide to North American truffles: hunting, identifying, and enjoying the world's most prized fungi. Ten Speed Press

    Google Scholar 

  • Urcelay C, Longo S, Geml J, Tecco PA, Nouhra E (2017) Co-invasive exotic pines and their ectomycorrhizal symbionts show capabilities for wide distance and altitudinal range expansion. Funct Ecol 25:50–58. https://doi.org/10.1016/j.funeco.2016.11.002

    Article  Google Scholar 

  • Valda S (2011) Contribution to the knowledge of our hypogeous fungi – Part II: Basidiomycota. Mykol Listy 117:10–27

    Google Scholar 

  • Vlk L, Tedersoo L, Antl T, Větrovský T, Abarenkov K, Pergl J, Albrechtová J, Vosátka M, Baldrian P, Pyšek P, Kohout P (2020) Alien ectomycorrhizal plants differ in their ability to interact with co-introduced and native ectomycorrhizal fungi in novel sites. ISME J 14(9):2336–2346. https://doi.org/10.1038/s41396-020-0692-5

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang L, Otgonsuren B, Godbold DL (2017) Mycorrhizas and soil ecosystem function of co-existing woody vegetation islands at the alpine tree line. Plant Soil 411:467–481. https://doi.org/10.1007/s11104-016-3047-2

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns TD, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

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Acknowledgements

Special thanks are due to Jan Holec (PRM), Vladimír Antonín (BRNM), and Tereza Tejklová (HR) for arranging the loans and to Petra Veselá and Martina Vašutová for sharing their photos and data.

Funding

OK was supported by Institutional Support for Science and Research of the Ministry of Education, Youth and Sports and Ministry of Agriculture of the Czech Republic. VK was supported by the Scientific Grant Agency of the Ministry of Education, Science, Research and Sport of the Slovak Republic (Project No. VEGA 1/0295/20).

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All authors contributed to the study conception and identification of collected material. Material preparation and collection were performed by S. Valda, J. Gaisler, and V. Kunca; molecular data were obtained and analysed by O. Koukol and interpreted by O. Koukol and N. Dowie. The first draft of the manuscript was written by O. Koukol and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Ondřej Koukol.

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Section Editor: Zhu-Liang Yang

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Supplementary information

Online Resource 1:

Alignment of ITS rDNA in the .nex format. (NEX 44 kb)

Online Resource 2:

Alignment of RPB2 in the .nex format. (NEX 25 kb)

Online Resource 3:

Alignment of RAanl1 in the .nex format. (NEX 26 kb)

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Koukol, O., Valda, S., Gaisler, J. et al. Rhizopogon confusus sp. nov., a correct name for a fungus previously recorded in Central Europe as the North American Rhizopogon salebrosus. Mycol Progress 21, 49 (2022). https://doi.org/10.1007/s11557-022-01777-1

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  • DOI: https://doi.org/10.1007/s11557-022-01777-1

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