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Comparative phylogenies and host specialization in the alder ectomycorrhizal fungi Alnicola, Alpova and Lactarius (Basidiomycota) in Europe.

Rochet J, Moreau PA, Manzi S, Gardes M - BMC Evol. Biol. (2011)

Bottom Line: Alnus.Alnus to A. alnobetula are found in most lineages of Alnicola (at least four times), Alpova (twice) and Lactarius (once), but they do not represent such a common event as could be expected by geographic proximity of trees from the two subgenera.However, active or very recent host extensions clearly occurred in Corsica, where some fungi usually associated with Alnus glutinosa on mainland Europe locally extend there to A. alnobetula subsp. suaveolens without significant genetic or morphological deviation.

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Affiliation: Laboratoire Evolution et Diversité Biologique, Université de Toulouse, UPS, UMR 5174 EDB, 118 route de Narbonne, 31062 Toulouse Cedex 4, France.

ABSTRACT

Background: Mycorrhizal fungi form intimate associations with their host plants that constitute their carbon resource and habitat. Alnus spp. (Betulaceae) are known to host an exceptional species-poor and specialized ectomycorrhizal (ECM) fungal community compared to other tree species, but the host-specificity pattern and its significance in terms of fungal diversification and speciation remain poorly documented. The degree of parallel speciation, host switching, and patterns of biogeography were explored in the historical associations between alders and three ECM taxa of Basidiomycetes: Alnicola (Agaricales), Alpova (Boletales), and Lactarius (Russulales). The aim was to develop an evolutionary framework on host specificity and diversification of Basidiomycetes in this highly specialized plant-fungus symbiosis.

Results: Sporocarps of Alnicola (220), Lactarius (61) and Alpova (29) were collected from stands of the four European alder species (A. alnobetula including the endemic subsp. suaveolens in Corsica, A. cordata, A. glutinosa, A. incana) in Western Europe (mainly in France and Austria), from 1995 to 2009. Specimens were morphologically identified to the species level. From these, 402 sequences of four DNA regions (ITS, rpb2, gpd, and the V9 domain of the mit-SSU rDNA) were successfully obtained and analyzed in addition with 89 sequences available in GenBank and UNITE databases. Phylogenetic analyses were conducted on all sequence data sets (individual and combined) using maximum likelihood reconstruction and Bayesian inference. Fungal phylogenies are compared and discussed in relation to the host, with a focus on species boundaries by associating taxonomic, systematic and molecular information.

Conclusions: Patterns of host specificity and phylogenies of Alnicola and Lactarius suggest coevolution as a basal factor of speciation in relation with the subgeneric diversification of Alnus, possibly due to the very selective pressure of the host. A second element of the historical associations between Alnus and its fungal symbionts is a host-dependent speciation (radiation without host change), here observed in Alnicola and Alpova in relation with Alnus subgen. Alnus. Finally host shifts from Alnus subgen. Alnus to A. alnobetula are found in most lineages of Alnicola (at least four times), Alpova (twice) and Lactarius (once), but they do not represent such a common event as could be expected by geographic proximity of trees from the two subgenera. However, active or very recent host extensions clearly occurred in Corsica, where some fungi usually associated with Alnus glutinosa on mainland Europe locally extend there to A. alnobetula subsp. suaveolens without significant genetic or morphological deviation.

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Phylogenetic reconstruction of the Alnicola sect. Alnicola lineage (Hymenogastraceae) by concatenate analysis (ITS, GPD, RPB2, V9), showing putative evolutional events in relation with host specificity. Red: species associated with Alnus sect. Alnus. Green: species associated with Alnus sect. Alnobetula. Green star shows putative basal association with Alnus alnobetula (possible co-speciation). Arrows show events of speciation associated with host specificity; red arrow: host-dependent radiation with Alnus subgen. Alnus; green arrow: host shifts from Alnus subgen. Alnus to A. alnobetula.
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Figure 2: Phylogenetic reconstruction of the Alnicola sect. Alnicola lineage (Hymenogastraceae) by concatenate analysis (ITS, GPD, RPB2, V9), showing putative evolutional events in relation with host specificity. Red: species associated with Alnus sect. Alnus. Green: species associated with Alnus sect. Alnobetula. Green star shows putative basal association with Alnus alnobetula (possible co-speciation). Arrows show events of speciation associated with host specificity; red arrow: host-dependent radiation with Alnus subgen. Alnus; green arrow: host shifts from Alnus subgen. Alnus to A. alnobetula.

Mentions: Because the datasets of the four genes were highly congruent, a combined analysis was conducted on a 2743 bases long alignment, obtained by concatenation of all genes for each sampled morphospecies, with a Bayesian approach (Figure 2, 3, 4). Alnicola geraniolens Courtec., which belongs to Alnicola sect. Amarescens [33] (not associated with Alnus) was taken as an outgroup [32]. Alnicola cholea Kühner, in sect. Cholea P.A. Moreau [35], a more distant species not associated with Alnus, was also tested as outgroup but gave a weaker resolution on some branches (not shown). Although species relationships are still not completely resolved even when data from additional genes are included, the same fourteen species are clearly identified in all the analyses (each gene separately or the concatenated dataset), likely representing independently evolved lineages (Figure 2). The low sequence divergence and lack of phylogenetic resolution including with the combined gene dataset, suggests a fast radiation of these species in a short geological time.


Comparative phylogenies and host specialization in the alder ectomycorrhizal fungi Alnicola, Alpova and Lactarius (Basidiomycota) in Europe.

Rochet J, Moreau PA, Manzi S, Gardes M - BMC Evol. Biol. (2011)

Phylogenetic reconstruction of the Alnicola sect. Alnicola lineage (Hymenogastraceae) by concatenate analysis (ITS, GPD, RPB2, V9), showing putative evolutional events in relation with host specificity. Red: species associated with Alnus sect. Alnus. Green: species associated with Alnus sect. Alnobetula. Green star shows putative basal association with Alnus alnobetula (possible co-speciation). Arrows show events of speciation associated with host specificity; red arrow: host-dependent radiation with Alnus subgen. Alnus; green arrow: host shifts from Alnus subgen. Alnus to A. alnobetula.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3045908&req=5

Figure 2: Phylogenetic reconstruction of the Alnicola sect. Alnicola lineage (Hymenogastraceae) by concatenate analysis (ITS, GPD, RPB2, V9), showing putative evolutional events in relation with host specificity. Red: species associated with Alnus sect. Alnus. Green: species associated with Alnus sect. Alnobetula. Green star shows putative basal association with Alnus alnobetula (possible co-speciation). Arrows show events of speciation associated with host specificity; red arrow: host-dependent radiation with Alnus subgen. Alnus; green arrow: host shifts from Alnus subgen. Alnus to A. alnobetula.
Mentions: Because the datasets of the four genes were highly congruent, a combined analysis was conducted on a 2743 bases long alignment, obtained by concatenation of all genes for each sampled morphospecies, with a Bayesian approach (Figure 2, 3, 4). Alnicola geraniolens Courtec., which belongs to Alnicola sect. Amarescens [33] (not associated with Alnus) was taken as an outgroup [32]. Alnicola cholea Kühner, in sect. Cholea P.A. Moreau [35], a more distant species not associated with Alnus, was also tested as outgroup but gave a weaker resolution on some branches (not shown). Although species relationships are still not completely resolved even when data from additional genes are included, the same fourteen species are clearly identified in all the analyses (each gene separately or the concatenated dataset), likely representing independently evolved lineages (Figure 2). The low sequence divergence and lack of phylogenetic resolution including with the combined gene dataset, suggests a fast radiation of these species in a short geological time.

Bottom Line: Alnus.Alnus to A. alnobetula are found in most lineages of Alnicola (at least four times), Alpova (twice) and Lactarius (once), but they do not represent such a common event as could be expected by geographic proximity of trees from the two subgenera.However, active or very recent host extensions clearly occurred in Corsica, where some fungi usually associated with Alnus glutinosa on mainland Europe locally extend there to A. alnobetula subsp. suaveolens without significant genetic or morphological deviation.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratoire Evolution et Diversité Biologique, Université de Toulouse, UPS, UMR 5174 EDB, 118 route de Narbonne, 31062 Toulouse Cedex 4, France.

ABSTRACT

Background: Mycorrhizal fungi form intimate associations with their host plants that constitute their carbon resource and habitat. Alnus spp. (Betulaceae) are known to host an exceptional species-poor and specialized ectomycorrhizal (ECM) fungal community compared to other tree species, but the host-specificity pattern and its significance in terms of fungal diversification and speciation remain poorly documented. The degree of parallel speciation, host switching, and patterns of biogeography were explored in the historical associations between alders and three ECM taxa of Basidiomycetes: Alnicola (Agaricales), Alpova (Boletales), and Lactarius (Russulales). The aim was to develop an evolutionary framework on host specificity and diversification of Basidiomycetes in this highly specialized plant-fungus symbiosis.

Results: Sporocarps of Alnicola (220), Lactarius (61) and Alpova (29) were collected from stands of the four European alder species (A. alnobetula including the endemic subsp. suaveolens in Corsica, A. cordata, A. glutinosa, A. incana) in Western Europe (mainly in France and Austria), from 1995 to 2009. Specimens were morphologically identified to the species level. From these, 402 sequences of four DNA regions (ITS, rpb2, gpd, and the V9 domain of the mit-SSU rDNA) were successfully obtained and analyzed in addition with 89 sequences available in GenBank and UNITE databases. Phylogenetic analyses were conducted on all sequence data sets (individual and combined) using maximum likelihood reconstruction and Bayesian inference. Fungal phylogenies are compared and discussed in relation to the host, with a focus on species boundaries by associating taxonomic, systematic and molecular information.

Conclusions: Patterns of host specificity and phylogenies of Alnicola and Lactarius suggest coevolution as a basal factor of speciation in relation with the subgeneric diversification of Alnus, possibly due to the very selective pressure of the host. A second element of the historical associations between Alnus and its fungal symbionts is a host-dependent speciation (radiation without host change), here observed in Alnicola and Alpova in relation with Alnus subgen. Alnus. Finally host shifts from Alnus subgen. Alnus to A. alnobetula are found in most lineages of Alnicola (at least four times), Alpova (twice) and Lactarius (once), but they do not represent such a common event as could be expected by geographic proximity of trees from the two subgenera. However, active or very recent host extensions clearly occurred in Corsica, where some fungi usually associated with Alnus glutinosa on mainland Europe locally extend there to A. alnobetula subsp. suaveolens without significant genetic or morphological deviation.

Show MeSH