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

Genome research | 2016

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.

Pubmed ID: 27247244 RIS Download

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RefSeq (tool)

RRID:SCR_003496

Collection of curated, non-redundant genomic DNA, transcript RNA, and protein sequences produced by NCBI. Provides a reference for genome annotation, gene identification and characterization, mutation and polymorphism analysis, expression studies, and comparative analyses. Accessed through the Nucleotide and Protein databases.

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European Nucleotide Archive (ENA) (tool)

RRID:SCR_006515

Public archive providing a comprehensive record of the world''''s nucleotide sequencing information, covering raw sequencing data, sequence assembly information and functional annotation. All submitted data, once public, will be exchanged with the NCBI and DDBJ as part of the INSDC data exchange agreement. The European Nucleotide Archive (ENA) captures and presents information relating to experimental workflows that are based around nucleotide sequencing. A typical workflow includes the isolation and preparation of material for sequencing, a run of a sequencing machine in which sequencing data are produced and a subsequent bioinformatic analysis pipeline. ENA records this information in a data model that covers input information (sample, experimental setup, machine configuration), output machine data (sequence traces, reads and quality scores) and interpreted information (assembly, mapping, functional annotation). Data arrive at ENA from a variety of sources including submissions of raw data, assembled sequences and annotation from small-scale sequencing efforts, data provision from the major European sequencing centers and routine and comprehensive exchange with their partners in the International Nucleotide Sequence Database Collaboration (INSDC). Provision of nucleotide sequence data to ENA or its INSDC partners has become a central and mandatory step in the dissemination of research findings to the scientific community. ENA works with publishers of scientific literature and funding bodies to ensure compliance with these principles and to provide optimal submission systems and data access tools that work seamlessly with the published literature. ENA is made up of a number of distinct databases that includes the EMBL Nucleotide Sequence Database (Embl-Bank), the newly established Sequence Read Archive (SRA) and the Trace Archive. The main tool for downloading ENA data is the ENA Browser, which is available through REST URLs for easy programmatic use. All ENA data are available through the ENA Browser. Note: EMBL Nucleotide Sequence Database (EMBL-Bank) is entirely included within this resource.

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Celera assembler (tool)

RRID:SCR_010750

A de novo whole-genome shotgun (WGS) DNA sequence assembler.

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tRNAscan-SE (tool)

RRID:SCR_010835

Web server to search for tRNA genes in genomic sequence. If you would like to run tRNAscan-SE locally, you can get the UNIX source code (gzip''d tar file).

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Newbler (tool)

RRID:SCR_011916

A software package for de novo DNA sequence assembly.

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ProtTest (tool)

RRID:SCR_014628

Web-based software used for the selection of best-fit models of protein evolution.

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PAML (tool)

RRID:SCR_014932

Package of programs for phylogenetic analyses of DNA or protein sequences using maximum likelihood. PAML estimates parameters and tests hypotheses to study the evolutionary process from a phylogenetic tree.

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Genome Resources for Yeast Chromosomes (tool)

RRID:SCR_015005

Database which provides annotated sequence data for the genomes of basidio and ascomycete yeasts. The resources provided include genetic element pages, data sets for downloading, quick and advanced searches, facilities for BLAST comparisons, and a genome browser powered by JBrowse from GMOD.

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tRNAscan-SE (tool)

RRID:SCR_008637

Web server to search for tRNA genes in genomic sequence. If you would like to run tRNAscan-SE locally, you can get the UNIX source code (gzip''d tar file).

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