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PMID: 14759257 Published · ppublish English Journal Article

A comprehensive evolutionary classification of proteins encoded in complete eukaryotic genomes.

Genome biology ·Vol. 5 ·No. 2 ·2004-00-00 ·Pages R7

Koonin EV, Fedorova ND, Jackson JD, Jacobs AR, Krylov DM, Makarova KS, Mazumder R, Mekhedov SL, Nikolskaya AN, Rao BS, Rogozin IB, Smirnov S, Sorokin AV, Sverdlov AV, Vasudevan S, Wolf YI, Yin JJ, Natale DA

Abstract

Sequencing 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. We 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. The 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.

MeSH Terms
Animals Caenorhabditis elegans/genetics Eukaryotic Cells/classification Evolution, Molecular Gene Deletion Genome Humans Phylogeny Prokaryotic Cells/classification Protein Structure, Tertiary Proteins/classification,genetics,physiology Sequence Analysis, Protein Yeasts/genetics
Chemicals
Proteins
Authors & Affiliations
18 authors, click to expand affiliations / ORCID
Koonin Eugene V
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894, USA. koonin@ncbi.nlm.nih.gov
Fedorova Natalie D
Jackson John D
Jacobs Aviva R
Krylov Dmitri M
Makarova Kira S
Mazumder Raja
Mekhedov Sergei L
Nikolskaya Anastasia N
Rao B Sridhar
Rogozin Igor B
Smirnov Sergei
Sorokin Alexander V
Sverdlov Alexander V
Vasudevan Sona
Wolf Yuri I
Yin Jodie J
Natale Darren A
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Article Info
Journal
Genome biology
Abbr.
Genome Biol
ISSN
1474-760X
DOI
10.1186/gb-2004-5-2-r7
Email
koonin@ncbi.nlm.nih.gov
Published
2004-00-00
Epub
2004-00-15
Pages
R7
Language
English
Region
England
NLM ID
100960660
PMCID
PMC395751
Subset
IM
External Links
PubMed source DOI: 10.1186/gb-2004-5-2-r7 PMC Full Text View journal details
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