Architecture and evolution of subtelomeres in the unicellular green algaChlamydomonas reinhardtii

Abstract

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, analyse their structure and infer how they evolved. Here, we use recent 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 a heterochromatic array of Sultan elements adjacent to the telomere, followed by a transcribed Spacer sequence, a G-rich microsatellite and transposable elements. Sequence similarity analyses suggest that Sultan elements underwent segmental duplications within each subtelomere and rearranged between subtelomeres at a much lower frequency. Analysis of other green algae reveals species-specific repeated elements that are shared across subtelomeres, with an overall organization similar to C. reinhardtii. This work uncovers the complexity and evolution of subtelomere architecture in green algae.

Rates and spectra of de novo structural mutation in Chlamydomonas reinhardtii

“…unequal exchange) rather than active transposition. Subtelomeres feature a unique satellite called Sultan , and we observed expansions and contractions of the Sultan monomer within the same subtelomere, as hypothesised by Chaux-Jukic et al (2021). Interestingly, we observed one example in each of CC-1952 (∼94 kb) and CC-2931 (∼163 kb) of the truncation of a chromosome terminus, followed by de novo telomere addition (i.e.…”

“…A final set of tandem repeats for each assembly was produced by combining simple repeats and satellites from RepeatMasker, satellites and microsatellites from Tandem Repeats Finder, and manually curated centromeric, subtelomeric and ribosomal DNA array coordinates. Centromeres were identified based on the span of the constituent LINE ZeppL-1_cRei (Craig et al 2021a) and subtelomeres as any sequence telomere-proximal to the characteristic spacer sequence (see Chaux-Jukic et al 2021). A microsatellite was considered as a tandem repeat sequence with a monomer length <10 bp, with tandem repeats consisting of any longer monomer length considered satellite DNA.…”

The Chlamydomonas Genome Project, version 6: reference assemblies for mating type plus and minus strains reveal extensive structural mutation in the laboratory

“…Despite the complexity of the Sultan satellites present at subtelomeres, 26 of the 34 chromosome termini are capped with telomeric repeats. Among the incomplete termini are the two ribosomal DNA (rDNA) arrays on the right arms of chromosome 8 and 14 (Figure 1A; note that the chromosome 1 rDNA array is truncated and likely non-functional in laboratory strains, but potentially not so in field isolates (Chaux-Jukic et al 2021)). One gap corresponds to the 5S rDNA array on chromosome 1, while the second 5S rDNA array on chromosome 8 is putatively complete (Figure 1A).…”

“…Several short contigs that mostly contained satellite DNA were manually removed since they appeared to duplicate a region already assembled on a larger contig. Other short contigs entirely consisting of subtelomeric repeats, which generally did not map uniquely, were assigned to chromosome termini by specific alignment and phylogenetic analysis (see Chaux-Jukic et al (2021)).…”

“…Unplaced sequence was assembled as scaffolds in v4 and v5, and contigs in all other assemblies. The single unplaced contig in the released version of the CC-1690 assembly was later assembled to the right arm of chromosome 15 (Chaux-Jukic et al 2021).…”