3D genomics across the tree of life reveals condensin II as a determinant of architecture type

Abstract

We investigated genome folding across the eukaryotic tree of life. We find two types of three-dimensional (3D) genome architectures at the chromosome scale. Each type appears and disappears repeatedly during eukaryotic evolution. The type of genome architecture that an organism exhibits correlates with the absence of condensin II subunits. Moreover, condensin II depletion converts the architecture of the human genome to a state resembling that seen in organisms such as fungi or mosquitoes. In this state, centromeres cluster together at nucleoli, and heterochromatin domains merge. We propose a physical model in which lengthwise compaction of chromosomes by condensin II during mitosis determines chromosome-scale genome architecture, with effects that are retained during the subsequent interphase. This mechanism likely has been conserved since the last common ancestor of all eukaryotes.

A chromosome-scale genome assembly and karyotype of the ctenophore Hormiphora californensis

“…The P. bachei genome assembly was recently scaffolded using Hi-C data ( Hoencamp et al 2021 ). The new, scaffolded assembly did not include a genome annotation.…”

A simple model explains the cell cycle-dependent assembly of centromeric nucleosomes in holocentric species

“…This short comparison, supported by our models, indicates that the spatial chromosome length might be a valuable parameter to describe chromosome organization. Recently, lengthwise compaction of mitotic chromosome was also proposed to determine the subsequent architecture in interphase ( 27 ). More data are required to confirm our observations, but we expect that future studies could relate chromosome organization to its length observed by chromosome imaging.…”

“…In mitotic chromosomes, cohesins are related to sister chromatid cohesion, while the condensation of chromosomes relies on the function of condensin I and II ( 26 , 27 ). In vertebrates, the two condensins have been associated with different phases of the cell cycle.…”

Understanding three-dimensional chromatin organization in diploid genomes

“…Most recently, Hoencamp and colleagues [67] have determined that homologs tend to be separated or paired across species depending on whether they carry functional condensin II subunits. Species lacking all or partial condensin II subunits (e.g., fruit flies and mosquitoes), exhibit Rabl-like architectural features (centromere clustering, telomere clustering, and a telomere-to-centromere axis), and tend to be homolog pairing.…”