A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes

By Eugene V. Koonin, N. Fedorova, John D. Jackson, A. Jacobs, D. M. Krylov, Kira S. Makarova, Raja Mazumder, S. Mekhedov, Anastasia N. Nikolskaya, B. S. Rao and 8 more. Genome Biology, 2004

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BackgroundSequencing the genomes of multiple, taxonomically diverse eukaryotes enables in-depth comparative-genomic analysis which is expected to help in reconstructing ancestral eukaryotic genomes and major events in eukaryotic evolution and in making functional predictions for currently uncharacterized conserved genes.ResultsWe examined functional and evolutionary patterns in the recently constructed set of 5,873 clusters of predicted orthologs (eukaryotic orthologous groups or KOGs) from seven eukaryotic genomes: Caenorhabditis elegans, Drosophila melanogaster, Homo sapiens, Arabidopsis thaliana, Saccharomyces cerevisiae, Schizosaccharomyces pombe and Encephalitozoon cuniculi. Conservation of KOGs through the phyletic range of eukaryotes strongly correlates with their functions and with the effect of gene knockout on the organism's viability. The approximately 40% of KOGs that are represented in six or seven species are enriched in proteins responsible for housekeeping functions, particularly translation and RNA processing. These conserved KOGs are often essential for survival and might approximate the minimal set of essential eukaryotic genes. The 131 single-member, pan-eukaryotic KOGs we identified were examined in detail. For around 20 that remained uncharacterized, functions were predicted by in-depth sequence analysis and examination of genomic context. Nearly all these proteins are subunits of known or predicted multiprotein complexes, in agreement with the balance hypothesis of evolution of gene copy number. Other KOGs show a variety of phyletic patterns, which points to major contributions of lineage-specific gene loss and the 'invention' of genes new to eukaryotic evolution. Examination of the sets of KOGs lost in individual lineages reveals co-elimination of functionally connected genes. Parsimonious scenarios of eukaryotic genome evolution and gene sets for ancestral eukaryotic forms were reconstructed. The gene set of the last common ancestor of the crown group consists of 3,413 KOGs and largely includes proteins involved in genome replication and expression, and central metabolism. Only 44% of the KOGs, mostly from the reconstructed gene set of the last common ancestor of the crown group, have detectable homologs in prokaryotes; the remainder apparently evolved via duplication with divergence and invention of new genes.ConclusionsThe KOG analysis reveals a conserved core of largely essential eukaryotic genes as well as major diversification and innovation associated with evolution of eukaryotic genomes. The results provide quantitative support for major trends of eukaryotic evolution noticed previously at the qualitative level and a basis for detailed reconstruction of evolution of eukaryotic genomes and biology of ancestral forms.

Subfields: Genetics, Molecular Biology, Plant Science

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Citations in the corpus

Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi (2014, methodology): “We were able to assign functions from the Eukaryotic Clusters of Orthologs (KOG) (48) to 38% of Basidiomycota proteins (compared with 43% in Ascomycota); 74% of core proteins in both Basidiomycota and Ascomycota; and 17% of Basidiomycota-specific proteins (23% in Ascomycota) (Fig.”
The Genome Portal of the Department of Energy Joint Genome Institute (2011, methodology): “KOG proﬁle summarizes functional annotations of genes according to this classi-ﬁcation and allows comparison of gene counts in each category between related genomes (last two columns).”
MycoCosm portal: gearing up for 1000 fungal genomes (2013, background): “Additionally, summaries listing numbers of genes by category in the GO, KEGG and KOG classiﬁcations are accessible from the portal menu, and can be compared with other selected genomes to explore gene family expansions and contractions across genomes.”
Phytozome: a comparative platform for green plant genomics (2011, methodology): “Protein-coding genes from both JGI and non-JGI genomes are then assigned PFAM domains (26), KEGG enzyme classification and KEGG Orthology assignment (27), KOG assignment (28) and Panther classification (29).”
Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus (2005, methodology): “…in the A.fumigatus genome were identiﬁed by BLASTp search against 131 single-member KOGs (eukaryotic orthologous groups) representing a conserved core of largely essential eukaryotic genes compiled by analysis of seven diverse, completely sequenced eukaryotic genomes 15 (Supplementary Table S4).”
Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma (2011, methodology): “All predicted gene models were functionally annotated by homology to annotated genes from a NCBI nonredundant set and classified according to Gene Ontology [51], eukaryotic orthologous groups (KOGs) [52], and Kyoto Encyclopedia of Genes and Genomes (KEGG) metabolic pathways [53].”
Insights into Land Plant Evolution Garnered from the Marchantia polymorpha Genome. (2017, methodology): “KOGs found in M. polymorpha, but not in other land plants, are often homologous with fungal genes or related tomobile elements, suggestive of horizontal gene transfer.”
Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis (2013, methodology): “We confirm that none of the MATA-HMG genes are located in close proximity to orthologs of genes known to compose the MAT locus of other fungi, and that six scaffolds harbor MATA-HMGs that are repeated in tandem (31).”