Lineage-specific loss and divergence of functionally linked genes in eukaryotes

Abstract

By comparing 4,344 protein sequences from fission yeast Schizosaccharomyces pombe with all available eukaryotic sequences, we identified those genes that are conserved in S. pombe and nonfungal eukaryotes but are missing or highly diverged in the baker's yeast Saccharomyces cerevisiae. Since the radiation from the common ancestor with S. pombe, S. cerevisiae appears to have lost about 300 genes, and about 300 more genes have diverged by far beyond expectation. The most notable feature of the set of genes lost in S. cerevisiae is the coelimination of functionally connected groups of proteins, such as the signalosome and the spliceosome components. We predict similar coelimination of the components of the posttranscriptional gene-silencing system that includes the recently identified RNA-dependent RNA polymerase. Because one of the functions of posttranscriptional silencing appears to be ''taming'' of retrotransposons, the loss of this system in yeast could have triggered massive retrotransposition, resulting in elimination of introns and subsequent loss of spliceosome components that become dispensable. As the genome database grows, systematic analysis of coordinated gene loss may become a general approach for predicting new components of functional systems or even defining previously unknown functional complexes.A major outcome of the recent advances in comparative genomics is the realization of the major role of horizontal gene transfer and lineage-specific gene loss in the evolution of prokaryotes (1-4). These phenomena appear to account largely for the remarkable diversity of the prokaryotic gene repertoires. The likelihood of horizontal gene transfer between eukaryotes, at least multicellular ones, is low because, for a gene to be laterally transferred, it must enter the germ line. In contrast, there is no such restriction for gene loss. The dramatic variation in the number of genes among eukaryotes, in some cases even between rather closely related species-yeast Saccharomyces cerevisiae, for example, has about 6,000 genes compared with at least 8,000-9,000 in multicellular ascomycetes such as Aspergillus (5)-suggests that, along with proliferation of gene families (6), lineage-specific gene loss could have been important in eukaryotic evolution.The two yeasts, S. cerevisiae and Schizosaccharomyces pombe, are probably the optimal current choice of genomes to compare with the aim of estimating the number of lost genes. The genome of S. cerevisiae, arguably the best-studied eukaryote in terms of gene functions (6), has been completed (7), and for S. pombe, up to 70% of the genome sequence is available. For estimating gene loss, it is critical to have assurance that (nearly) all genes in the analyzed genome have been identified; S. cerevisiae is the only eukaryotic genome for which such confidence exists, particularly because of the paucity of introns, which facilitates gene detection. The two yeast species are close enough so that direct counterparts among their genes [orthologs (8)] are readily identifiable b...

Histone H3-variant Cse4-induced positive DNA supercoiling in the yeast plasmid has implications for a plasmid origin of a chromosome centromere

“…In contrast, the S. cerevisiae point centromere is quite short (∼125 bp), genetically defined, and has a characteristic tripartite DNA organization (40,41). Point centromeres are unique to members of the Saccharomycetaceae fungal lineage that have lost all or nearly all of the protein components of the RNAi and heterochromatin machineries (42). This lineage also stands apart from the rest of eukaryotes in harboring autonomously replicating plasmids analogous to the 2-μm plasmid.…”

Accelerated Evolutionary Rate May Be Responsible for the Emergence of Lineage-Specific Genes in Ascomycota

“…Genes with the same phylogenetic distribution may have linked functions (Aravind et al 2000;Marcotte et al 1999;Pellegrini et al 1999). If we use lineage specificity (LS) to measure the degree of phylogenetic distribution, genes with higher levels of LS are found only in a smaller group of species that diverge from a certain point in a species tree.…”

“…In the case of formation from random ORFs it is unlikely that such a protein would be functional. A second option is gene loss (Aravind et al 2000;Krylov et al 2003). However it is relatively unlikely that a gene would be lost in all but one lineage (Domazet-Loso and Tautz 2003) and this may not explain most orphan or lineage-specific genes.…”

A de novo originated gene depresses budding yeast mating pathway and is repressed by the protein encoded by its antisense strand

“…This transcriptional suppression is instead probably due to the RNA or protein of ADF1 present in the cells. In view of the absence of RNAi machinery in S. cerevisiae [3], it is more likely that the repression occurred at the protein level. Subcellular localization of the Adf1p provides further support for a role as a transcription factor.…”

“…Studies in various organisms revealed that antisense transcripts are involved in degradation of the corresponding sense transcripts (RNA interference) [2]. However, in Saccharomyces cerevisiae, components of the RNAi machinery are absent [3], and antisense repression can be mediated by transcription interference (TI) or histone deacetylation. TI was thought to be an unavoidable suppressive consequence of two convergent promoters directing transcripts that overlap for at least part of their sequences [4].…”