Mixing and matching nuclear envelope remodeling and spindle assembly strategies in the evolution of mitosis

Abstract

In eukaryotes, cellular genome is enclosed inside a membrane-bound organelle called the nucleus. The nucleus compartmentalizes genome replication, repair and expression, keeping these activities separated from protein synthesis and other metabolic processes. Each proliferative division, the duplicated chromosomes must be equipartitioned between the daughter cells and this requires precise coordination between assembly of the microtubule-based mitotic spindle and nuclear remodeling. Here we review a surprising variety of strategies used by modern eukaryotes to manage these processes and discuss possible mechanisms that might have led to the emergence of this diversity in evolution.

Figure 1

Diagrams summarizing representative modes of mitosis across eukaryotes. The mitotic apparatuses are shown in anaphase. Left column: (A) the excavate Trypanosoma brucei, (B) the fission yeast Schizosaccharomyces pombe, (C) the fission yeast Schizosaccharomyces japonicus, (D) the filamentous Ascomycete Aspergillus nidulans. Right column: (E) the dinoflagellate Crypthecodinium cohnii, (F) the green algae Chlamydomonas reinhardtii, (G) an yeast form of the Basidiomycete Ustilago maydis, (H) an embryo of the nematode Caenorhabditis elegans, (I) a cultured human cell. Yellow background indicates “closed” modes of mitosis and green background denotes mitotic NE breakdown. Pictorial legend is shown below.

Figure 2

A schematic diagram describing NE “vulnerabilities” (e.g. NPC selectivity, membrane integrity and lamina function, outlined in red) that can be attacked by mitotic regulators (e.g. CDK1, Aurora, Polo and NIMA kinases) to induce NE disassembly or remodeling. Pictorial legend is included.