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...

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Autores principales: Gregory Bonito, Matthew E Smith, Michael Nowak, Rosanne A Healy, Gonzalo Guevara, Efren Cázares, Akihiko Kinoshita, Eduardo R Nouhra, Laura S Domínguez, Leho Tedersoo, Claude Murat, Yun Wang, Baldomero Arroyo Moreno, Donald H Pfister, Kazuhide Nara, Alessandra Zambonelli, James M Trappe, Rytas Vilgalys
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spelling oai:doaj.org-article:86baaa01617f4c2b9988375a610e41eb2021-11-18T08:02:54ZHistorical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage.1932-620310.1371/journal.pone.0052765https://doaj.org/article/86baaa01617f4c2b9988375a610e41eb2013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23300990/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203Truffles 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.Gregory BonitoMatthew E SmithMichael NowakRosanne A HealyGonzalo GuevaraEfren CázaresAkihiko KinoshitaEduardo R NouhraLaura S DomínguezLeho TedersooClaude MuratYun WangBaldomero Arroyo MorenoDonald H PfisterKazuhide NaraAlessandra ZambonelliJames M TrappeRytas VilgalysPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 8, Iss 1, p e52765 (2013)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Gregory Bonito
Matthew E Smith
Michael Nowak
Rosanne A Healy
Gonzalo Guevara
Efren Cázares
Akihiko Kinoshita
Eduardo R Nouhra
Laura S Domínguez
Leho Tedersoo
Claude Murat
Yun Wang
Baldomero Arroyo Moreno
Donald H Pfister
Kazuhide Nara
Alessandra Zambonelli
James M Trappe
Rytas Vilgalys
Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage.
description 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.
format article
author Gregory Bonito
Matthew E Smith
Michael Nowak
Rosanne A Healy
Gonzalo Guevara
Efren Cázares
Akihiko Kinoshita
Eduardo R Nouhra
Laura S Domínguez
Leho Tedersoo
Claude Murat
Yun Wang
Baldomero Arroyo Moreno
Donald H Pfister
Kazuhide Nara
Alessandra Zambonelli
James M Trappe
Rytas Vilgalys
author_facet Gregory Bonito
Matthew E Smith
Michael Nowak
Rosanne A Healy
Gonzalo Guevara
Efren Cázares
Akihiko Kinoshita
Eduardo R Nouhra
Laura S Domínguez
Leho Tedersoo
Claude Murat
Yun Wang
Baldomero Arroyo Moreno
Donald H Pfister
Kazuhide Nara
Alessandra Zambonelli
James M Trappe
Rytas Vilgalys
author_sort Gregory Bonito
title Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage.
title_short Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage.
title_full Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage.
title_fullStr Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage.
title_full_unstemmed Historical biogeography and diversification of truffles in the Tuberaceae and their newly identified southern hemisphere sister lineage.
title_sort historical biogeography and diversification of truffles in the tuberaceae and their newly identified southern hemisphere sister lineage.
publisher Public Library of Science (PLoS)
publishDate 2013
url https://doaj.org/article/86baaa01617f4c2b9988375a610e41eb
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