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Extensive gene flow over Europe and possible speciation over Eurasia in the ectomycorrhizal basidiomycete Laccaria amethystina complex

Identifieur interne : 000B43 ( Istex/Corpus ); précédent : 000B42; suivant : 000B44

Extensive gene flow over Europe and possible speciation over Eurasia in the ectomycorrhizal basidiomycete Laccaria amethystina complex

Auteurs : Lucie Vincenot ; Kazuhide Nara ; Christopher Sthultz ; Jessy Labbé ; Marie-Pierre Dubois ; Leho Tedersoo ; Francis Martin ; Marc-André Selosse

Source :

RBID : ISTEX:EE5DD48A4239CA97D06A784BA37D7BE0DFFA57F3

English descriptors

Abstract

Biogeographical patterns and large‐scale genetic structure have been little studied in ectomycorrhizal (EM) fungi, despite the ecological and economic importance of EM symbioses. We coupled population genetics and phylogenetic approaches to understand spatial structure in fungal populations on a continental scale. Using nine microsatellite markers, we characterized gene flow among 16 populations of the widespread EM basidiomycete Laccaria amethystina over Europe (i.e. over 2900 km). We also widened our scope to two additional populations from Japan (104 km away) and compared them with European populations through microsatellite markers and multilocus phylogenies, using three nuclear genes (NAR, G6PD and ribosomal DNA) and two mitochondrial ribosomal genes. European L. amethystina populations displayed limited differentiation (average FST = 0.041) and very weak isolation by distance (IBD). This panmictic European pattern may result from effective aerial dispersal of spores, high genetic diversity in populations and mutualistic interactions with multiple hosts that all facilitate migration. The multilocus phylogeny based on nuclear genes confirmed that Japanese and European specimens were closely related but clustered on a geographical basis. By using microsatellite markers, we found that Japanese populations were strongly differentiated from the European populations (FST = 0.416), more than expected by extrapolating the European pattern of IBD. Population structure analyses clearly separated the populations into two clusters, i.e. European and Japanese clusters. We discuss the possibility of IBD in a continuous population (considering some evidence for a ring species over the Northern Hemisphere) vs. an allopatric speciation over Eurasia, making L. amethystina a promising model of intercontinental species for future studies.

Url:
DOI: 10.1111/j.1365-294X.2011.05392.x

Links to Exploration step

ISTEX:EE5DD48A4239CA97D06A784BA37D7BE0DFFA57F3

Le document en format XML

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<p>Biogeographical patterns and large‐scale genetic structure have been little studied in ectomycorrhizal (EM) fungi, despite the ecological and economic importance of EM symbioses. We coupled population genetics and phylogenetic approaches to understand spatial structure in fungal populations on a continental scale. Using nine microsatellite markers, we characterized gene flow among 16 populations of the widespread EM basidiomycete Laccaria amethystina over Europe (i.e. over 2900 km). We also widened our scope to two additional populations from Japan (104 km away) and compared them with European populations through microsatellite markers and multilocus phylogenies, using three nuclear genes (NAR, G6PD and ribosomal DNA) and two mitochondrial ribosomal genes. European L. amethystina populations displayed limited differentiation (average FST = 0.041) and very weak isolation by distance (IBD). This panmictic European pattern may result from effective aerial dispersal of spores, high genetic diversity in populations and mutualistic interactions with multiple hosts that all facilitate migration. The multilocus phylogeny based on nuclear genes confirmed that Japanese and European specimens were closely related but clustered on a geographical basis. By using microsatellite markers, we found that Japanese populations were strongly differentiated from the European populations (FST = 0.416), more than expected by extrapolating the European pattern of IBD. Population structure analyses clearly separated the populations into two clusters, i.e. European and Japanese clusters. We discuss the possibility of IBD in a continuous population (considering some evidence for a ring species over the Northern Hemisphere) vs. an allopatric speciation over Eurasia, making L. amethystina a promising model of intercontinental species for future studies.</p>
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<copyright>© 2011 Blackwell Publishing Ltd</copyright>
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<correspondenceTo>Lucie Vincenot, Fax: (+39 0461650872); E‐mail:
<email>lucie.vincenot@cefe.cnrs.fr</email>
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<unparsedEditorialHistory>Received 11 July 2011; revision received 27 October 2011; accepted 1 November 2011</unparsedEditorialHistory>
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<title type="main">Extensive gene flow over Europe and possible speciation over Eurasia in the ectomycorrhizal basidiomycete
<i>Laccaria amethystina</i>
complex</title>
<title type="shortAuthors">L. VINCENOT
<i>ET AL.</i>
</title>
<title type="short">EURASIAN POPULATION GENETICS OF
<i>LACCARIA AMETHYSTINA</i>
</title>
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<p>
<b>Fig. S1</b>
Structure diagram of European and Japanese populations, based on the software Structure 2.2 for
<i>K = </i>
2 clusters.</p>
<p>
<b>Fig. S2</b>
Bayesian phylogram of
<i>Laccaria</i>
spp. using ITS sequences from this study, Unite and GenBank (138 taxa, 622 characters).</p>
<p>
<b>Fig. S3</b>
Alignment of ITS sequences from
<i>L. amethystina</i>
and
<i>L. amethysteo‐occidentalis</i>
.</p>
<p>
<b>Fig. S4</b>
Unrooted Bayesian phylograms of
<i>L. amethystina</i>
in Europe and Japan for two mitochondrial ribosomal genes,
<i>SrRNA</i>
(a, 29 taxa, 477 characters) and
<i>LrRNA</i>
(b, 37 taxa, 410 characters).</p>
<p>
<b>Data S1</b>
Microsatellites diploid genotypes for 667 individuals in 18
<i>L. amethystina</i>
populations, 9 microsatellites loci</p>
<p>
<b>Data S2</b>
Genbank accession numbers for sequences of 5 coding or non‐coding loci, on purpose of phylogenetic analysis. Associated phylogenetic trees are available on TREEBASE, study accessions no.11481, 11482, 11483, 11484, 11485, 11486, 11487I have also attached the PDF for reference.</p>
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<p>Biogeographical patterns and large‐scale genetic structure have been little studied in ectomycorrhizal (EM) fungi, despite the ecological and economic importance of EM symbioses. We coupled population genetics and phylogenetic approaches to understand spatial structure in fungal populations on a continental scale. Using nine microsatellite markers, we characterized gene flow among 16 populations of the widespread EM basidiomycete
<i>Laccaria amethystina</i>
over Europe (i.e. over 2900 km). We also widened our scope to two additional populations from Japan (10
<sup>4</sup>
 km away) and compared them with European populations through microsatellite markers and multilocus phylogenies, using three nuclear genes (
<i>NAR</i>
,
<i>G6PD</i>
and ribosomal DNA) and two mitochondrial ribosomal genes. European
<i>L. amethystina</i>
populations displayed limited differentiation (average
<i>F</i>
<sub>ST</sub>
 = 0.041) and very weak isolation by distance (IBD). This panmictic European pattern may result from effective aerial dispersal of spores, high genetic diversity in populations and mutualistic interactions with multiple hosts that all facilitate migration. The multilocus phylogeny based on nuclear genes confirmed that Japanese and European specimens were closely related but clustered on a geographical basis. By using microsatellite markers, we found that Japanese populations were strongly differentiated from the European populations (
<i>F</i>
<sub>ST</sub>
 = 0.416), more than expected by extrapolating the European pattern of IBD. Population structure analyses clearly separated the populations into two clusters, i.e. European and Japanese clusters. We discuss the possibility of IBD in a continuous population (considering some evidence for a ring species over the Northern Hemisphere) vs. an allopatric speciation over Eurasia, making
<i>L. amethystina</i>
a promising model of intercontinental species for future studies.</p>
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<p> Present address: Sustainable Agro‐Ecosystems and Bioresources, Fondazione Edmund Mach‐IASMA, via Edmund Mach 1, 38100 San Michele all’Adige, Italy</p>
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<abstract lang="en">Biogeographical patterns and large‐scale genetic structure have been little studied in ectomycorrhizal (EM) fungi, despite the ecological and economic importance of EM symbioses. We coupled population genetics and phylogenetic approaches to understand spatial structure in fungal populations on a continental scale. Using nine microsatellite markers, we characterized gene flow among 16 populations of the widespread EM basidiomycete Laccaria amethystina over Europe (i.e. over 2900 km). We also widened our scope to two additional populations from Japan (104 km away) and compared them with European populations through microsatellite markers and multilocus phylogenies, using three nuclear genes (NAR, G6PD and ribosomal DNA) and two mitochondrial ribosomal genes. European L. amethystina populations displayed limited differentiation (average FST = 0.041) and very weak isolation by distance (IBD). This panmictic European pattern may result from effective aerial dispersal of spores, high genetic diversity in populations and mutualistic interactions with multiple hosts that all facilitate migration. The multilocus phylogeny based on nuclear genes confirmed that Japanese and European specimens were closely related but clustered on a geographical basis. By using microsatellite markers, we found that Japanese populations were strongly differentiated from the European populations (FST = 0.416), more than expected by extrapolating the European pattern of IBD. Population structure analyses clearly separated the populations into two clusters, i.e. European and Japanese clusters. We discuss the possibility of IBD in a continuous population (considering some evidence for a ring species over the Northern Hemisphere) vs. an allopatric speciation over Eurasia, making L. amethystina a promising model of intercontinental species for future studies.</abstract>
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<note type="content"> Fig. S1 Structure diagram of European and Japanese populations, based on the software Structure 2.2 for K = 2 clusters. Fig. S2 Bayesian phylogram of Laccaria spp. using ITS sequences from this study, Unite and GenBank (138 taxa, 622 characters). Fig. S3 Alignment of ITS sequences from L. amethystina and L. amethysteo‐occidentalis. Fig. S4 Unrooted Bayesian phylograms of L. amethystina in Europe and Japan for two mitochondrial ribosomal genes, SrRNA (a, 29 taxa, 477 characters) and LrRNA (b, 37 taxa, 410 characters). Data S1 Microsatellites diploid genotypes for 667 individuals in 18 L. amethystina populations, 9 microsatellites loci Data S2 Genbank accession numbers for sequences of 5 coding or non‐coding loci, on purpose of phylogenetic analysis. Associated phylogenetic trees are available on TREEBASE, study accessions no.11481, 11482, 11483, 11484, 11485, 11486, 11487I have also attached the PDF for reference. Fig. S1 Structure diagram of European and Japanese populations, based on the software Structure 2.2 for K = 2 clusters. Fig. S2 Bayesian phylogram of Laccaria spp. using ITS sequences from this study, Unite and GenBank (138 taxa, 622 characters). Fig. S3 Alignment of ITS sequences from L. amethystina and L. amethysteo‐occidentalis. Fig. S4 Unrooted Bayesian phylograms of L. amethystina in Europe and Japan for two mitochondrial ribosomal genes, SrRNA (a, 29 taxa, 477 characters) and LrRNA (b, 37 taxa, 410 characters). Data S1 Microsatellites diploid genotypes for 667 individuals in 18 L. amethystina populations, 9 microsatellites loci Data S2 Genbank accession numbers for sequences of 5 coding or non‐coding loci, on purpose of phylogenetic analysis. Associated phylogenetic trees are available on TREEBASE, study accessions no.11481, 11482, 11483, 11484, 11485, 11486, 11487I have also attached the PDF for reference. Fig. S1 Structure diagram of European and Japanese populations, based on the software Structure 2.2 for K = 2 clusters. Fig. S2 Bayesian phylogram of Laccaria spp. using ITS sequences from this study, Unite and GenBank (138 taxa, 622 characters). Fig. S3 Alignment of ITS sequences from L. amethystina and L. amethysteo‐occidentalis. Fig. S4 Unrooted Bayesian phylograms of L. amethystina in Europe and Japan for two mitochondrial ribosomal genes, SrRNA (a, 29 taxa, 477 characters) and LrRNA (b, 37 taxa, 410 characters). Data S1 Microsatellites diploid genotypes for 667 individuals in 18 L. amethystina populations, 9 microsatellites loci Data S2 Genbank accession numbers for sequences of 5 coding or non‐coding loci, on purpose of phylogenetic analysis. Associated phylogenetic trees are available on TREEBASE, study accessions no.11481, 11482, 11483, 11484, 11485, 11486, 11487I have also attached the PDF for reference. Fig. S1 Structure diagram of European and Japanese populations, based on the software Structure 2.2 for K = 2 clusters. Fig. S2 Bayesian phylogram of Laccaria spp. using ITS sequences from this study, Unite and GenBank (138 taxa, 622 characters). Fig. S3 Alignment of ITS sequences from L. amethystina and L. amethysteo‐occidentalis. Fig. S4 Unrooted Bayesian phylograms of L. amethystina in Europe and Japan for two mitochondrial ribosomal genes, SrRNA (a, 29 taxa, 477 characters) and LrRNA (b, 37 taxa, 410 characters). Data S1 Microsatellites diploid genotypes for 667 individuals in 18 L. amethystina populations, 9 microsatellites loci Data S2 Genbank accession numbers for sequences of 5 coding or non‐coding loci, on purpose of phylogenetic analysis. Associated phylogenetic trees are available on TREEBASE, study accessions no.11481, 11482, 11483, 11484, 11485, 11486, 11487I have also attached the PDF for reference. Fig. S1 Structure diagram of European and Japanese populations, based on the software Structure 2.2 for K = 2 clusters. Fig. S2 Bayesian phylogram of Laccaria spp. using ITS sequences from this study, Unite and GenBank (138 taxa, 622 characters). Fig. S3 Alignment of ITS sequences from L. amethystina and L. amethysteo‐occidentalis. Fig. S4 Unrooted Bayesian phylograms of L. amethystina in Europe and Japan for two mitochondrial ribosomal genes, SrRNA (a, 29 taxa, 477 characters) and LrRNA (b, 37 taxa, 410 characters). Data S1 Microsatellites diploid genotypes for 667 individuals in 18 L. amethystina populations, 9 microsatellites loci Data S2 Genbank accession numbers for sequences of 5 coding or non‐coding loci, on purpose of phylogenetic analysis. Associated phylogenetic trees are available on TREEBASE, study accessions no.11481, 11482, 11483, 11484, 11485, 11486, 11487I have also attached the PDF for reference. Fig. S1 Structure diagram of European and Japanese populations, based on the software Structure 2.2 for K = 2 clusters. Fig. S2 Bayesian phylogram of Laccaria spp. using ITS sequences from this study, Unite and GenBank (138 taxa, 622 characters). Fig. S3 Alignment of ITS sequences from L. amethystina and L. amethysteo‐occidentalis. Fig. S4 Unrooted Bayesian phylograms of L. amethystina in Europe and Japan for two mitochondrial ribosomal genes, SrRNA (a, 29 taxa, 477 characters) and LrRNA (b, 37 taxa, 410 characters). Data S1 Microsatellites diploid genotypes for 667 individuals in 18 L. amethystina populations, 9 microsatellites loci Data S2 Genbank accession numbers for sequences of 5 coding or non‐coding loci, on purpose of phylogenetic analysis. 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