Abstract
Novel, large-scale structural mutations were previously discovered during the cultivation of engineered Saccharomyces cerevisiae strains in which essential tRNA synthetase genes were replaced by their orthologs from the distantly related yeast Yarrowia lipolytica. Among those were internal segmental amplifications forming giant chromosomes as well as complex segmental rearrangements associated with massive amplifications at an unselected short locus. The formation of such novel structures, whose stability is high enough to propagate over multiple generations, involved short repeated sequences dispersed in the genome (as expected), but also novel junctions between unrelated sequences likely triggered by accidental template switching within replication forks. Using the same evolutionary protocol, we now describe yet another type of major structural mutation in the yeast genome, the formation of neochromosomes, with functional centromeres and telomeres, made of extra copies of very long chromosomal segments ligated together in novel arrangements. The novel junctions occurred between short repeated sequences dispersed in the genome. They first resulted in the formation of an instable neochromosome present in a single copy in the diploid cells, followed by its replacement by a shorter, partially palindromic neochromosome present in two copies, whose stability eventually increased the chromosome number of the diploid strains harboring it.
Highlights
The total number of chromosomes forming the nuclear genome of eukaryotes often differs between related species
Using the experimental evolutionary set up previously described [11], we show the recurrent formation of neochromosomes during the evolution of diploid S. cerevisiae strains in which both copies of the KRS1 gene (YDR037w) encoding the class II lysine-tRNA synthetase have been replaced by their ortholog (YAL0F16291g) from the very distantly related yeast Y. lipolytica
The generation time of BYAT5810 is more than four times longer than that of the wild-type, consistent with the fact that the Y. lipolitica gene YALI0F16291g is a poor orthologous replacement of the S. cerevisiae KRS1 gene resulting in an insufficient pool of lysine-charged tRNA molecules in yeast cells [11]
Summary
The total number of chromosomes forming the nuclear genome of eukaryotes often differs between related species. In the budding yeasts of the Saccharomycetaceae family, the haploid number of chromosomes varies between 6 for Kluyveromyces lactis and 8 for Lachancea thermotolerans, two species of the KLE protoploïd clade [3] or between 10 for Nakaseomyces castelli and 16 for Saccharomyces cerevisiae, two species of the post genome duplication clade [4]. By comparing yeast genome sequences, it was shown that, during evolution, the chromosome number decreases principally by telomere-to-telomere fusion between two chromosomes with the concomitant disappearance of one centromere [5]. No precise mechanism has been identified yet to increase chromosome numbers, if one excepts whole-genome duplication
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