An evolutionary perspective on the relationship between kinetochore size and CENP-E dependence for chromosome alignment

J Cell Sci. 2024 Dec 15;137(24):jcs263466. doi: 10.1242/jcs.263466. Epub 2024 Dec 19.

Abstract

Chromosome alignment during mitosis can occur as a consequence of bi-orientation or is assisted by the CENP-E (kinesin-7) motor at kinetochores. We previously found that Indian muntjac chromosomes with larger kinetochores bi-orient more efficiently and are biased to align in a CENP-E-independent manner, suggesting that CENP-E dependence for chromosome alignment negatively correlates with kinetochore size. Here, we used targeted phylogenetic profiling of CENP-E in monocentric (localized centromeres) and holocentric (centromeres spanning the entire chromosome length) clades to test this hypothesis at an evolutionary scale. We found that, despite being present in common ancestors, CENP-E was lost more frequently in taxa with holocentric chromosomes, such as Hemiptera and Nematoda. Functional experiments in two nematodes with holocentric chromosomes in which a CENP-E ortholog is absent (Caenorhabditis elegans) or present (Pristionchus pacificus) revealed that targeted expression of human CENP-E to C. elegans kinetochores partially rescued chromosome alignment defects associated with attenuated polar-ejection forces, whereas CENP-E inactivation in P. pacificus had no detrimental effects on mitosis and viability. These data showcase the dispensability of CENP-E for mitotic chromosome alignment in species with larger kinetochores.

Keywords: CENP-E; Chromosome; Holocentric; Kinesin; Kinetochore; Mitosis.

MeSH terms

  • Animals
  • Biological Evolution
  • Caenorhabditis elegans* / genetics
  • Caenorhabditis elegans* / metabolism
  • Centromere / genetics
  • Centromere / metabolism
  • Chromosomal Proteins, Non-Histone* / genetics
  • Chromosomal Proteins, Non-Histone* / metabolism
  • Chromosome Segregation
  • Chromosomes / genetics
  • Chromosomes / metabolism
  • Evolution, Molecular
  • Humans
  • Kinetochores* / metabolism
  • Mitosis
  • Phylogeny

Substances

  • Chromosomal Proteins, Non-Histone
  • centromere protein E