Differential gene retention as an evolutionary mechanism to generate biodiversity and adaptation in yeasts

Morel, Guillaume; Sterck, Lieven; Swennen, Dominique; Marcet‐Houben, Marina; Onésime, Djamila; Levasseur, Anthony; Jacques, Noémie; Mallet, Sandrine; Couloux, Arnaud; Labadie, Karine; Amselem, Joëlle; Beckerich, Jean-Marie; Henrissat, Bernard; Peer, Yves Van de; Wincker, Patrick; Souciet, Jean-Luc; Gabaldón, Toni; Tinsley, Colin R.; Casarégola, Serge

doi:10.1038/srep11571

Cited by 56 publications

(74 citation statements)

References 121 publications

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“…Twenty-three events are novel compared to previously reported HGT cases (Rolland et al 2009;Morel et al 2015). The 24 HGT families are similar to proteins from Pezizomycotina species (10 cases), from other eukaryotes (three cases) and from bacteria (11 cases) (Supplemental Table S4).…”

Section: High-quality Reference Genomes Of the Lachancea Genusmentioning

confidence: 62%

Reconstruction of ancestral chromosome architecture and gene repertoire reveals principles of genome evolution in a model yeast genus

et al. 2016

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Reconstructing genome history is complex but necessary to reveal quantitative principles governing genome evolution. Such reconstruction requires recapitulating into a single evolutionary framework the evolution of genome architecture and gene repertoire. Here, we reconstructed the genome history of the genus Lachancea that appeared to cover a continuous evolutionary range from closely related to more diverged yeast species. Our approach integrated the generation of a high-quality genome data set; the development of AnChro, a new algorithm for reconstructing ancestral genome architecture; and a comprehensive analysis of gene repertoire evolution. We found that the ancestral genome of the genus Lachancea contained eight chromosomes and about 5173 protein-coding genes. Moreover, we characterized 24 horizontal gene transfers and 159 putative gene creation events that punctuated species diversification. We retraced all chromosomal rearrangements, including gene losses, gene duplications, chromosomal inversions and translocations at single gene resolution. Gene duplications outnumbered losses and balanced rearrangements with 1503, 929, and 423 events, respectively. Gene content variations between extant species are mainly driven by differential gene losses, while gene duplications remained globally constant in all lineages. Remarkably, we discovered that balanced chromosomal rearrangements could be responsible for up to 14% of all gene losses by disrupting genes at their breakpoints. Finally, we found that nonsynonymous substitutions reached fixation at a coordinated pace with chromosomal inversions, translocations, and duplications, but not deletions. Overall, we provide a granular view of genome evolution within an entire eukaryotic genus, linking gene content, chromosome rearrangements, and protein divergence into a single evolutionary framework.

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Section: High-quality Reference Genomes Of the Lachancea Genusmentioning

confidence: 62%

Reconstruction of ancestral chromosome architecture and gene repertoire reveals principles of genome evolution in a model yeast genus

et al. 2016

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“…This pattern is compatible either with ancient transfer from a Pezizomycotina ancestor to an ancient lineage in the CTG clade, or by simple vertical descent from their common ancestor and subsequent losses in non-CTG lineages. Such patterns of differential gene loss are not rare in Saccharomycotina (Morel et al 2015). In addition, we observed long branches separating the Saccharomycotina sequences from their Pezizomycotina counterparts.…”

Section: Resultsmentioning

confidence: 99%

Mitochondrial Carriers Link the Catabolism of Hydroxyaromatic Compounds to the Central Metabolism in Candida parapsilosis

Zeman

Neboháčová

Gérecová

et al. 2016

G3 Genes|Genomes|Genetics

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The pathogenic yeast Candida parapsilosis metabolizes hydroxyderivatives of benzene and benzoic acid to compounds channeled into central metabolism, including the mitochondrially localized tricarboxylic acid cycle, via the 3-oxoadipate and gentisate pathways. The orchestration of both catabolic pathways with mitochondrial metabolism as well as their evolutionary origin is not fully understood. Our results show that the enzymes involved in these two pathways operate in the cytoplasm with the exception of the mitochondrially targeted 3-oxoadipate CoA-transferase (Osc1p) and 3-oxoadipyl-CoA thiolase (Oct1p) catalyzing the last two reactions of the 3-oxoadipate pathway. The cellular localization of the enzymes indicates that degradation of hydroxyaromatic compounds requires a shuttling of intermediates, cofactors, and products of the corresponding biochemical reactions between cytosol and mitochondria. Indeed, we found that yeast cells assimilating hydroxybenzoates increase the expression of genes SFC1, LEU5, YHM2, and MPC1 coding for succinate/fumarate carrier, coenzyme A carrier, oxoglutarate/citrate carrier, and the subunit of pyruvate carrier, respectively. A phylogenetic analysis uncovered distinct evolutionary trajectories for sparsely distributed gene clusters coding for enzymes of both pathways. Whereas the 3-oxoadipate pathway appears to have evolved by vertical descent combined with multiple losses, the gentisate pathway shows a striking pattern suggestive of horizontal gene transfer to the evolutionarily distant Mucorales.

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“…Surprisingly, the genomes of two yeast isolates purported to be from the same species ( Geotrichum candidum isolates CLIB 918 and 3C) were placed into two different clades; G. candidum CLIB 918 (Morel et al 2015) was nested within Saccharomycotina yeasts, whereas “ G. candidum ” 3C (Polev et al 2014) was nested within the Pezizomycotina outgroup. Given its phylogenetic placement, we infer that the genome sequence of the isolate “ G. candidum ” 3C represents a misidentified Pezizomycotina species.…”

Section: Resultsmentioning

confidence: 99%

Reconstructing the Backbone of the Saccharomycotina Yeast Phylogeny Using Genome-Scale Data

Shen

Zhou

Kominek

et al. 2016

G3 Genes|Genomes|Genetics

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Understanding the phylogenetic relationships among the yeasts of the subphylum Saccharomycotina is a prerequisite for understanding the evolution of their metabolisms and ecological lifestyles. In the last two decades, the use of rDNA and multilocus data sets has greatly advanced our understanding of the yeast phylogeny, but many deep relationships remain unsupported. In contrast, phylogenomic analyses have involved relatively few taxa and lineages that were often selected with limited considerations for covering the breadth of yeast biodiversity. Here we used genome sequence data from 86 publicly available yeast genomes representing nine of the 11 known major lineages and 10 nonyeast fungal outgroups to generate a 1233-gene, 96-taxon data matrix. Species phylogenies reconstructed using two different methods (concatenation and coalescence) and two data matrices (amino acids or the first two codon positions) yielded identical and highly supported relationships between the nine major lineages. Aside from the lineage comprised by the family Pichiaceae, all other lineages were monophyletic. Most interrelationships among yeast species were robust across the two methods and data matrices. However, eight of the 93 internodes conflicted between analyses or data sets, including the placements of: the clade defined by species that have reassigned the CUG codon to encode serine, instead of leucine; the clade defined by a whole genome duplication; and the species Ascoidea rubescens. These phylogenomic analyses provide a robust roadmap for future comparative work across the yeast subphylum in the disciplines of taxonomy, molecular genetics, evolutionary biology, ecology, and biotechnology. To further this end, we have also provided a BLAST server to query the 86 Saccharomycotina genomes, which can be found at http://y1000plus.org/blast.

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Differential gene retention as an evolutionary mechanism to generate biodiversity and adaptation in yeasts

Cited by 56 publications

References 121 publications

Reconstruction of ancestral chromosome architecture and gene repertoire reveals principles of genome evolution in a model yeast genus

Reconstruction of ancestral chromosome architecture and gene repertoire reveals principles of genome evolution in a model yeast genus

Mitochondrial Carriers Link the Catabolism of Hydroxyaromatic Compounds to the Central Metabolism in Candida parapsilosis

Reconstructing the Backbone of the Saccharomycotina Yeast Phylogeny Using Genome-Scale Data

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