Architecture and evolution of subtelomeres in the unicellular green alga Chlamydomonas reinhardtii

In most eukaryotes, subtelomeres are dynamic genomic regions populated by multi-copy sequences of different origins, which can promote segmental duplications and chromosomal rearrangements. However, their repetitive nature has complicated the efforts to sequence them, analyze their structure and infer how they evolved. Here, we use recent and forthcoming genome assemblies of Chlamydomonas reinhardtii based on long-read sequencing to comprehensively describe the subtelomere architecture of the 17 chromosomes of this model unicellular green alga.

We identify three main repeated elements present at subtelomeres, which we call Sultan, Subtile and Suber, alongside three chromosome extremities with ribosomal DNA as the only identified component of their subtelomeres. The most common architecture, present in 27 out of 34 subtelomeres, is an array of 1 to 46 tandem copies of Sultan elements adjacent to the telomere and followed by a transcribed centromere-proximal Spacer sequence, a G-rich microsatellite and a region rich in transposable elements.

Sequence similarity analyses suggest that Sultan elements underwent segmental duplications within each subtelomere and rearranged between subtelomeres at a much lower frequency. Comparison of genomic sequences of three laboratory strains and a wild isolate of C. reinhardtii shows that the overall subtelomeric architecture was already present in their last common ancestor, although subtelomeric rearrangements are on-going at the species level.

Analysis of other green algae reveals the presence of species-specific repeated elements, highly conserved across subtelomeres and unrelated to the Sultan element, but with a subtelomere structure similar to C. reinhardtii. Overall, our work uncovers the complexity and evolution of subtelomere architecture in green algae.