Centromere diversity: How different repeat‐based holocentromeres may have evolved

• Published in: BioEssays 2024-06, Vol.46 (6), p.e2400013-n/a
• Main Authors: Kuo, Yi‐Tzu, Schubert, Veit, Marques, André, Schubert, Ingo, Houben, Andreas
• Format: Article
• Language: English
• Subjects: centromere; Centromere - genetics; Centromeres; Chromosomes; Chromosomes, Plant - genetics; Deoxyribonucleic acid; Dispersal; DNA; DNA Breaks, Double-Stranded; DNA damage; DNA Transposable Elements - genetics; DNA, Satellite - genetics; Eukaryotes; evolution; Evolution, Molecular; Histone H3; Histones; holocentromere; Repetitive Sequences, Nucleic Acid - genetics; Satellite DNA
• ISSN: 0265-9247; 1521-1878
• DOI: 10.1002/bies.202400013

In addition to monocentric eukaryotes, which have a single localized centromere on each chromosome, there are holocentric species, with extended repeat‐based or repeat‐less centromeres distributed over the entire chromosome length. At least two types of repeat‐based holocentromeres exist, one composed of many small repeat‐based centromere units (small unit‐type), and another one characterized by a few large centromere units (large unit‐type). We hypothesize that the transposable element‐mediated dispersal of hundreds of short satellite arrays formed the small centromere unit‐type holocentromere in Rhynchospora pubera. The large centromere unit‐type of the plant Chionographis japonica is likely a product of simultaneous DNA double‐strand breaks (DSBs), which initiated the de novo formation of repeat‐based holocentromeres via insertion of satellite DNA, derived from extra‐chromosomal circular DNAs (eccDNAs). The number of initial DSBs along the chromosomes must be higher than the number of centromere units since only a portion of the breaks will have incorporated eccDNA at an appropriate position to serve as future centromere unit sites. Subsequently, preferential incorporation of the centromeric histone H3 variant at these positions is assumed. The identification of repeat‐based holocentromeres across lineages will unveil the centromere plasticity and elucidate the mechanisms underlying the diverse formation of holocentromeres. The conserved function of the centromere does not limit its structural diversity. Various mechanisms drive the evolution of structurally diverse holocentromeres across different lineages. The incorporation of centromeric DNA‐carrying extra‐chromosomal circular DNAs (eccDNAs) and transposable elements (TEs) might be involved in mono‐to‐holocentric transition in the species with large or small centromere unit‐type of holocentromeres.