Molecular phylogenetics of porcini mushrooms (Boletus section Boletus)

Bryn T. M. Dentinger* (Corresponding Author), Joseph F. Ammirati, Ernst E. Both, Dennis E. Desjardin, Roy E. Halling, Terry W. Henkel, Pierre-Arthur Moreau, Eiji Nagasawa, Kasem Soytong, Andy F. Taylor, Roy Watling, Jean-Marc Moncalvo, David J. McLaughlin

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

137 Citations (Scopus)

Abstract

Porcini (Boletus section Boletus: Boletaceae: Boletineae: Boletales) are a conspicuous group of wild, edible mushrooms characterized by fleshy fruiting bodies with a poroid hymenophore that is "stuffed" with white hyphae when young. Their reported distribution is with ectomycorrhizal plants throughout the Northern Hemisphere. Little progress has been made on the systematics of this group using modern molecular phylogenetic tools because sampling has been limited primarily to European species and the genes employed were insufficient to resolve the phylogeny. We examined the evolutionary history of porcini by using a global geographic sampling of most known species, new discoveries from little explored areas, and multiple genes. We used 78 sequences from the fast-evolving nuclear internal transcribed spacers and are able to recognize 18 reciprocally monophyletic species. To address whether or not porcini form a monophyletic group, we compiled a broadly sampled dataset of 41 taxa, including other members of the Boletineae, and used separate and combined phylogenetic analysis of sequences from the nuclear large subunit ribosomal DNA, the largest subunit of RNA polymerase II, and the mitochondrial ATPase subunit six gene. Contrary to previous studies, our separate and combined phylogenetic analyses support the monophyly of porcini. We also report the discovery of two taxa that expand the known distribution of porcini to Australia and Thailand and have ancient phylogenetic connections to the rest of the group. A relaxed molecular clock analysis with these new taxa dates the origin of porcini to between 42 and 54 million years ago, coinciding with the initial diversification of angiosperms, during the Eocene epoch when the climate was warm and humid. These results reveal an unexpected diversity, distribution, and ancient origin of a group of commercially valuable mushrooms that may provide an economic incentive for conservation and support the hypothesis of a tropical origin of the ectomycorrhizal symbiosis. (C) 2010 Elsevier Inc. All rights reserved.

Original languageEnglish
Pages (from-to)1276-1292
Number of pages17
JournalMolecular Phylogenetics and Evolution
Volume57
Issue number3
Early online date21 Oct 2010
DOIs
Publication statusPublished - Dec 2010

Bibliographical note

Acknowledgments
BTMD would especially like to thank Iris Charvat, Scott Lanyon, Rachel Mason Dentinger, George Weiblen, and Robert Zink for their keen insight and advice during the course of this study. Tom Bruns and Ankie Camacho are gratefully acknowledged for sharing unpublished data early in this project that were instrumental to its development and to Tom Bruns and Xiang-Hua Wang for providing valuable material used in this study. The authors gratefully appreciate comments from two anonymous reviewers and specimens and information provided by Mohamed Abourouh, David Arora, Robert Fogel, Josh Grinath, James Groth, Jeffrey Klemens, Christophe Lécuru, Daniel Mousain, and Tim Whitfeld. BTMD is grateful to the University of Michigan Biological Station, Mountain Lake Biological Station, Ouachita Mountains Biological Station, and especially Rytas Vilgalys, Jason Thacker, and Tim James for hosting him during his 2003 collecting expedition. BTMD also thanks The Quetzal Education and Research Center (especially Zana Finkenbinder), INBIO (especially Milagro Mata), Julieta Carranza (University of Costa Rica) and Roger Blanco Segura for help with depositing specimens and securing permits for work in Costa Rica. We thank the Minnesota Supercomputing Institute for Advanced Computational Research and Victor Hanson-Smith and the Thornton Lab at the University of Oregon for access to computing resources. The contribution of K.S. and King Mongkut’s Institute of Technology in providing Roy Halling with a Material Transfer Agreement to study Thai bolete specimens is gratefully appreciated. PAM thanks the Office de l’Environnement de la Corse for facilitating fieldwork in Corsica and REH is supported by NSF Grants DEB-0414665 and DEB-9972018. Portions of this research were supported by the Mycological Society of America Backus Award, North American Mycological Association Memorial Fellowship, three fellowships from the University of Minnesota Graduate School (Alexander and Lydia Anderson Fellowship, Carolyn Crosby Fellowship, Doctoral Dissertation Fellowship), and a Simons Fellowship in Systematic Biology and Dayton and Wilkie Natural History Funds from the Bell Museum of Natural History to BTMD, NSF Grant EF-0228671 to D.J.M., and NSERC and Genome Canada funds for the Canadian Barcode of Life Network to J.M.M.

Keywords

  • ectomycorrhizal fungi
  • partial veil
  • stuffed pores
  • synapomorphy
  • biogeography
  • inference
  • molecular systematics
  • ITS
  • species complex
  • boletales
  • RPB1
  • mixed models
  • molecular clock
  • long-distance dispersal
  • sustainable non-timber forest product
  • systematics
  • identification
  • conservation
  • basidiomycota
  • edulis
  • high-throughput
  • evolution
  • ATP6

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