Publications by authors named "Marisol Sánchez-García"

11 Publications

  • Page 1 of 1

Fruiting body form, not nutritional mode, is the major driver of diversification in mushroom-forming fungi.

Proc Natl Acad Sci U S A 2020 12 30;117(51):32528-32534. Epub 2020 Nov 30.

Biology Department, Clark University, Worcester, MA 01610;

With ∼36,000 described species, Agaricomycetes are among the most successful groups of Fungi. Agaricomycetes display great diversity in fruiting body forms and nutritional modes. Most have pileate-stipitate fruiting bodies (with a cap and stalk), but the group also contains crust-like resupinate fungi, polypores, coral fungi, and gasteroid forms (e.g., puffballs and stinkhorns). Some Agaricomycetes enter into ectomycorrhizal symbioses with plants, while others are decayers (saprotrophs) or pathogens. We constructed a megaphylogeny of 8,400 species and used it to test the following five hypotheses regarding the evolution of morphological and ecological traits in Agaricomycetes and their impact on diversification: 1) resupinate forms are plesiomorphic, 2) pileate-stipitate forms promote diversification, 3) the evolution of gasteroid forms is irreversible, 4) the ectomycorrhizal (ECM) symbiosis promotes diversification, and 5) the evolution of ECM symbiosis is irreversible. The ancestor of Agaricomycetes was a saprotroph with a resupinate fruiting body. There have been 462 transitions in the examined morphologies, including 123 origins of gasteroid forms. Reversals of gasteroid forms are highly unlikely but cannot be rejected. Pileate-stipitate forms are correlated with elevated diversification rates, suggesting that this morphological trait is a key to the success of Agaricomycetes. ECM symbioses have evolved 36 times in Agaricomycetes, with several transformations to parasitism. Across the entire 8,400-species phylogeny, diversification rates of ectomycorrhizal lineages are no greater than those of saprotrophic lineages. However, some ECM lineages have elevated diversification rates compared to their non-ECM sister clades, suggesting that the evolution of symbioses may act as a key innovation at local phylogenetic scales.
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http://dx.doi.org/10.1073/pnas.1922539117DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7768725PMC
December 2020

Genomic Analysis Enlightens Agaricales Lifestyle Evolution and Increasing Peroxidase Diversity.

Mol Biol Evol 2021 04;38(4):1428-1446

Centro de Investigaciones Biológicas Margarita Salas (CIB), CSIC, Madrid, Spain.

As actors of global carbon cycle, Agaricomycetes (Basidiomycota) have developed complex enzymatic machineries that allow them to decompose all plant polymers, including lignin. Among them, saprotrophic Agaricales are characterized by an unparalleled diversity of habitats and lifestyles. Comparative analysis of 52 Agaricomycetes genomes (14 of them sequenced de novo) reveals that Agaricales possess a large diversity of hydrolytic and oxidative enzymes for lignocellulose decay. Based on the gene families with the predicted highest evolutionary rates-namely cellulose-binding CBM1, glycoside hydrolase GH43, lytic polysaccharide monooxygenase AA9, class-II peroxidases, glucose-methanol-choline oxidase/dehydrogenases, laccases, and unspecific peroxygenases-we reconstructed the lifestyles of the ancestors that led to the extant lignocellulose-decomposing Agaricomycetes. The changes in the enzymatic toolkit of ancestral Agaricales are correlated with the evolution of their ability to grow not only on wood but also on leaf litter and decayed wood, with grass-litter decomposers as the most recent eco-physiological group. In this context, the above families were analyzed in detail in connection with lifestyle diversity. Peroxidases appear as a central component of the enzymatic toolkit of saprotrophic Agaricomycetes, consistent with their essential role in lignin degradation and high evolutionary rates. This includes not only expansions/losses in peroxidase genes common to other basidiomycetes but also the widespread presence in Agaricales (and Russulales) of new peroxidases types not found in wood-rotting Polyporales, and other Agaricomycetes orders. Therefore, we analyzed the peroxidase evolution in Agaricomycetes by ancestral-sequence reconstruction revealing several major evolutionary pathways and mapped the appearance of the different enzyme types in a time-calibrated species tree.
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http://dx.doi.org/10.1093/molbev/msaa301DOI Listing
April 2021

Large-scale genome sequencing of mycorrhizal fungi provides insights into the early evolution of symbiotic traits.

Nat Commun 2020 10 12;11(1):5125. Epub 2020 Oct 12.

Université de Lorraine, Institut national de recherche pour l'agriculture, l'alimentation et l' environnement, UMR Interactions Arbres/Microorganismes, Centre INRAE Grand Est-Nancy, 54280, Champenoux, France.

Mycorrhizal fungi are mutualists that play crucial roles in nutrient acquisition in terrestrial ecosystems. Mycorrhizal symbioses arose repeatedly across multiple lineages of Mucoromycotina, Ascomycota, and Basidiomycota. Considerable variation exists in the capacity of mycorrhizal fungi to acquire carbon from soil organic matter. Here, we present a combined analysis of 135 fungal genomes from 73 saprotrophic, endophytic and pathogenic species, and 62 mycorrhizal species, including 29 new mycorrhizal genomes. This study samples ecologically dominant fungal guilds for which there were previously no symbiotic genomes available, including ectomycorrhizal Russulales, Thelephorales and Cantharellales. Our analyses show that transitions from saprotrophy to symbiosis involve (1) widespread losses of degrading enzymes acting on lignin and cellulose, (2) co-option of genes present in saprotrophic ancestors to fulfill new symbiotic functions, (3) diversification of novel, lineage-specific symbiosis-induced genes, (4) proliferation of transposable elements and (5) divergent genetic innovations underlying the convergent origins of the ectomycorrhizal guild.
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http://dx.doi.org/10.1038/s41467-020-18795-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7550596PMC
October 2020

Correction to: Brazilian fungal diversity represented by DNA markers generated over 20 years.

Braz J Microbiol 2020 Dec;51(4):2181

Biology Department, Clark University, Worcester, MA, 01610, USA.

Due to a processing error, there was a mistake in Table 3. The first entry in the right column should read 109. The corrected table is given below.
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http://dx.doi.org/10.1007/s42770-020-00299-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7688807PMC
December 2020

Building de novo reference genome assemblies of complex eukaryotic microorganisms from single nuclei.

Sci Rep 2020 Jan 28;10(1):1303. Epub 2020 Jan 28.

Department of Ecology and Genetics, Evolutionary Biology, Uppsala University, Uppsala, Sweden.

The advent of novel sequencing techniques has unraveled a tremendous diversity on Earth. Genomic data allow us to understand ecology and function of organisms that we would not otherwise know existed. However, major methodological challenges remain, in particular for multicellular organisms with large genomes. Arbuscular mycorrhizal (AM) fungi are important plant symbionts with cryptic and complex multicellular life cycles, thus representing a suitable model system for method development. Here, we report a novel method for large scale, unbiased nuclear sorting, sequencing, and de novo assembling of AM fungal genomes. After comparative analyses of three assembly workflows we discuss how sequence data from single nuclei can best be used for different downstream analyses such as phylogenomics and comparative genomics of single nuclei. Based on analysis of completeness, we conclude that comprehensive de novo genome assemblies can be produced from six to seven nuclei. The method is highly applicable for a broad range of taxa, and will greatly improve our ability to study multicellular eukaryotes with complex life cycles.
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http://dx.doi.org/10.1038/s41598-020-58025-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6987183PMC
January 2020

Brazilian fungal diversity represented by DNA markers generated over 20 years.

Braz J Microbiol 2020 Jun 11;51(2):729-749. Epub 2019 Dec 11.

Biology Department, Clark University, Worcester, MA, 01610, USA.

Molecular techniques using fungal DNA barcoding (ITS) and other markers have been key to identifying the biodiversity of different geographic areas, mainly in megadiverse countries. Here, we provide an overview of the fungal diversity in Brazil based on DNA markers of phylogenetic importance generated since 1996. We retrieved fungal sequences of ITS, LSU, SSU, tef1-α, β-tubulin, rpb1, rpb2, actin, chitin synthase, and ATP6 from GenBank using different field keywords that indicated their origin in Brazil. A total of 19,440 sequences were recovered. ITS is the most representative marker (11,209 sequences), with 70.1% belonging to Ascomycota, 18.6% Basidiomycota, 10.2% unidentified, 1.1% Mucoromycota, two sequences of Olpidium bornovanus (Fungi incertae sedis), one sequence of Blastocladiomycota (Allomyces arbusculus), and one sequence of Chytridiomycota (Batrachochytrium dendrobatidis). Considering the sequences of all selected markers, only the phyla Cryptomycota and Entorrhizomycota were not represented. Based on ITS, using a cutoff of 98%, all sequences comprise 3047 OTUs, with the majority being Ascomycota (2088 OTUs) and Basidiomycota (681 OTUs). Previous numbers based mainly on morphological and bibliographical data revealed 5264 fungal species from Brazil, with a predominance of Basidiomycota (2741 spp.) and Ascomycota (1881 spp.). The unidentified ITS sequences not assigned to a higher taxonomic level represent 1.61% of all ITS sequences sampled and correspond to 38 unknown class-level lineages (75% cutoff). A maximum likelihood phylogeny based on LSU illustrates the fungal classes occurring in Brazil.
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http://dx.doi.org/10.1007/s42770-019-00206-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7203393PMC
June 2020

Megaphylogeny resolves global patterns of mushroom evolution.

Nat Ecol Evol 2019 04 18;3(4):668-678. Epub 2019 Mar 18.

Synthetic and Systems Biology Unit, Biological Research Centre, Hungarian Academy of Sciences, Szeged, Hungary.

Mushroom-forming fungi (Agaricomycetes) have the greatest morphological diversity and complexity of any group of fungi. They have radiated into most niches and fulfil diverse roles in the ecosystem, including wood decomposers, pathogens or mycorrhizal mutualists. Despite the importance of mushroom-forming fungi, large-scale patterns of their evolutionary history are poorly known, in part due to the lack of a comprehensive and dated molecular phylogeny. Here, using multigene and genome-based data, we assemble a 5,284-species phylogenetic tree and infer ages and broad patterns of speciation/extinction and morphological innovation in mushroom-forming fungi. Agaricomycetes started a rapid class-wide radiation in the Jurassic, coinciding with the spread of (sub)tropical coniferous forests and a warming climate. A possible mass extinction, several clade-specific adaptive radiations and morphological diversification of fruiting bodies followed during the Cretaceous and the Paleogene, convergently giving rise to the classic toadstool morphology, with a cap, stalk and gills (pileate-stipitate morphology). This morphology is associated with increased rates of lineage diversification, suggesting it represents a key innovation in the evolution of mushroom-forming fungi. The increase in mushroom diversity started during the Mesozoic-Cenozoic radiation event, an era of humid climate when terrestrial communities dominated by gymnosperms and reptiles were also expanding.
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http://dx.doi.org/10.1038/s41559-019-0834-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6443077PMC
April 2019

Guyanagarika, a new ectomycorrhizal genus of Agaricales from the Neotropics.

Fungal Biol 2016 12 20;120(12):1540-1553. Epub 2016 Aug 20.

Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996, USA.

A new genus and three new species of Agaricales are described from the Pakaraima Mountains of Guyana in the central Guiana Shield. All three of these new species fruit on the ground in association with species of the ectomycorrhizal (ECM) tree genus Dicymbe (Fabaceae subfam. Caesalpinioideae) and one species has been shown to form ectomycorrhizas. Multi-locus molecular phylogenetic analyses place Guyanagarika gen. nov. within the Catathelasma clade, a lineage in the suborder Tricholomatineae of the Agaricales. We formally recognize this 'Catathelasma clade' as an expanded family Catathelasmataceae that includes the genera Callistosporium, Catathelasma, Guyanagarika, Macrocybe, Pleurocollybia, and Pseudolaccaria. Within the Catathelasmataceae, Catathelasma and Guyanagarika represent independent origins of the ectomycorrhizal habit. Guyanagarika is the first documented case of an ECM Agaricales genus known only from the Neotropics.
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http://dx.doi.org/10.1016/j.funbio.2016.08.005DOI Listing
December 2016

Is the switch to an ectomycorrhizal state an evolutionary key innovation in mushroom-forming fungi? A case study in the Tricholomatineae (Agaricales).

Evolution 2017 01 11;71(1):51-65. Epub 2016 Nov 11.

Department of Ecology and Evolutionary Biology, University of Tennessee, 569 Dabney Hall, Knoxville, Tennessee, 37996-1610.

Although fungi are one of the most diverse groups of organisms, little is known about the processes that shape their high taxonomic diversity. This study focuses on evolution of ectomycorrhizal (ECM) mushroom-forming fungi, symbiotic associates of many trees and shrubs, in the suborder Tricholomatineae of the Agaricales. We used the BiSSE model and BAMM to test the hypothesis that the ECM habit represents an evolutionary key innovation that allowed the colonization of new niches followed by an increase in diversification rate. Ancestral state reconstruction (ASR) supports the ancestor of the Tricholomatineae as non-ECM. We detected two diversification rate increases in the genus Tricholoma and the Rhodopolioid clade of the genus Entoloma. However, no increases in diversification were detected in the four other ECM clades of Tricholomatineae. We suggest that diversification of Tricholoma was not only due to the evolution of the ECM lifestyle, but also to the expansion and dominance of its main hosts and ability to associate with a variety of hosts. Diversification in the Rhodopolioid clade could be due to the unique combination of spore morphology and ECM habit. The spore morphology may represent an exaptation that aided spore dispersal and colonization. This is the first study to investigate rate shifts across a phylogeny that contains both non-ECM and ECM lineages.
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http://dx.doi.org/10.1111/evo.13099DOI Listing
January 2017

Into and out of the tropics: global diversification patterns in a hyperdiverse clade of ectomycorrhizal fungi.

Mol Ecol 2016 01 19;25(2):630-47. Epub 2016 Jan 19.

Department of Ecology and Evolutionary Biology, University of Tennessee, 332 Hesler Biology Building, Knoxville, TN, 37996-1610, USA.

Ectomycorrhizal (ECM) fungi, symbiotic mutualists of many dominant tree and shrub species, exhibit a biogeographic pattern counter to the established latitudinal diversity gradient of most macroflora and fauna. However, an evolutionary basis for this pattern has not been explicitly tested in a diverse lineage. In this study, we reconstructed a mega-phylogeny of a cosmopolitan and hyperdiverse genus of ECM fungi, Russula, sampling from annotated collections and utilizing publically available sequences deposited in GenBank. Metadata from molecular operational taxonomic unit cluster sets were examined to infer the distribution and plant association of the genus. This allowed us to test for differences in patterns of diversification between tropical and extratropical taxa, as well as how their associations with different plant lineages may be a driver of diversification. Results show that Russula is most species-rich at temperate latitudes and ancestral state reconstruction shows that the genus initially diversified in temperate areas. Migration into and out of the tropics characterizes the early evolution of the genus, and these transitions have been frequent since this time. We propose the 'generalized diversification rate' hypothesis to explain the reversed latitudinal diversity gradient pattern in Russula as we detect a higher net diversification rate in extratropical lineages. Patterns of diversification with plant associates support host switching and host expansion as driving diversification, with a higher diversification rate in lineages associated with Pinaceae and frequent transitions to association with angiosperms.
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http://dx.doi.org/10.1111/mec.13506DOI Listing
January 2016