Abstract
The whole-genome duplication (WGD) that occurred during yeast evolution changed the basal number of chromosomes from 8 to 16. However, the number of chromosomes in post-WGD species now ranges between 10 and 16, and the number in non-WGD species (Zygosaccharomyces, Kluyveromyces, Lachancea, and Ashbya) ranges between 6 and 8. To study the mechanism by which chromosome number changes, we traced the ancestry of centromeres and telomeres in each species. We observe only two mechanisms by which the number of chromosomes has decreased, as indicated by the loss of a centromere. The most frequent mechanism, seen 8 times, is telomere-to-telomere fusion between two chromosomes with the concomitant death of one centromere. The other mechanism, seen once, involves the breakage of a chromosome at its centromere, followed by the fusion of the two arms to the telomeres of two other chromosomes. The only mechanism by which chromosome number has increased in these species is WGD. Translocations and inversions have cycled telomere locations, internalizing some previously telomeric genes and creating novel telomeric locations. Comparison of centromere structures shows that the length of the CDEII region is variable between species but uniform within species. We trace the complete rearrangement history of the Lachancea kluyveri genome since its common ancestor with Saccharomyces and propose that its exceptionally low level of rearrangement is a consequence of the loss of the non-homologous end joining (NHEJ) DNA repair pathway in this species.
Highlights
Centromeres and telomeres are essential genetic and structural elements of eukaryotic chromosomes
By inferring ancestral genome structures, we examine the changes in location of centromeres and telomeres, key elements that biologically define chromosomes
We trace an evolutionary path between existing centromeres and telomeres to those in the ancestral genomes, allowing us to identify the specific evolutionary events that caused changes in chromosome number
Summary
Centromeres and telomeres are essential genetic and structural elements of eukaryotic chromosomes. Centromeres in all eukaryotes are the site at which the kinetochore forms and is attached to spindle microtubules, which segregate sister chromosomes to opposite poles of a dividing cell during anaphase I of meiosis, and sister chromatids during mitosis and anaphase II of meiosis. They play a role in the pairing of homologous chromosomes during meiosis [5]. Yeasts related to Saccharomyces cerevisiae have a unique type of centromere, known as point centromeres [8,9] These are generally less than 200 bases long and are defined by specific sequences, the CDEI, CDEII and CDEIII regions which are bound by CEN DNAbinding proteins [10,11]. Telomeres of S. cerevisiae chromosomes consist of a heterogeneous repeating sequence (basic unit TGGGTG(TG)0–3) that is maintained by the enzyme
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