Divergent Strategies for Controlling the Nuclear Membrane Satisfy Geometric Constraints during Nuclear Division

Abstract

Eukaryotes segregate chromosomes in "open" or "closed" mitosis, depending on whether their nuclear envelopes (NEs) break down or remain intact. Here we show that the control of the nuclear surface area may determine the choice between these two modes. The dividing nucleus does not expand its surface in the fission yeast Schizosaccharomyces japonicus, confining the mitotic spindle and causing it to buckle. The NE ruptures in anaphase, releasing the compressive stress and allowing chromosome segregation. Blocking the NE expansion in the related species Schizosaccharomyces pombe that undergoes closed mitosis induces spindle buckling and collapse in the absence of an intrinsic NE rupture mechanism. We propose that scaling considerations could have shaped the evolution of eukaryotic mitosis by necessitating either nuclear surface expansion or the NE breakdown.

The NIMA Kinase Is Required To Execute Stage-Specific Mitotic Functions after Initiation of Mitosis

“…In support of this idea, the dispersal of proteasomal components, which are expected to be in large complexes, has been observed to occur later than NPC disassembly in WT A. nidulans cells but can be made to occur earlier when the mitotic nuclear pores are more dramatically disassembled and further opened in the absence of nup37 and elys (Yi Xiong and Berl Oakley, personal communication). Furthermore, NE breakdown in anaphase has been demonstrated in the fission yeast Schizosaccharomyces japonicas in a manner independent of the mitotic spindle, similar to the case for our nimA7 cells (56). This suggests the existence of a second mechanism, in addition to partial NPC disassembly, in A. nidulans regulating the permeability properties of the NE late in mitosis that is potentially important for normal mitotic progression.…”

A nuclear contortionist: the mitotic migration ofMagnaporthe oryzaenuclei during plant infection

“…The persistence of Nup84 at the NE throughout mitosis confirms that portions of the NE do remain intact during nuclear division. Additionally, the polar localisation of Nup84 in M. oryzae is similar to other fungi known to use intermediate mitosis, including S. japonicus (Aoki et al 2011; Yam et al 2011) and A. nidulans (Osmani et al 2006). While these results confirm distinct components of the NE remain intact during mitosis, the details of the mechanism responsible for intermediate mitosis remain to be discovered in M. oryzae .…”

“…Generally, mechanisms of intermediate mitosis in fungi can be grouped into two broad categories: tearing of the NE or altering the composition of a largely intact NE to enhance permeability. Fungi such as U. maydis and Schizosaccharomyces japonicus experience NE tearing during mitosis (Straube et al 2005; Aoki et al 2011; Yam et al 2011). In A. nidulans , a subset of proteins found within nuclear pore complexes (NPCs) disperse into the cytoplasm during mitosis (De Souza et al 2004; Osmani et al 2006).…”

Shape Transformation of the Nuclear Envelope during Closed Mitosis

“…However, given that the main objective of this study is to explain the shape transformation of the NE without introducing prior assumptions, this scenario is not further pursued here. Another reason is that the nuclear volume could start to deviate from its original value slightly when the pole-to-pole distance becomes relatively large (4). As such, proper modifications in the formulation may be needed to describe such phenomena in an accurate manner.…”

“…In general, the NE maintains a spherical shape during interphase but then starts to break down when mitosis begins in higher eukaryotic cells (3). In contrast, in many lower eukaryotes, such as the fission yeast Schizosaccharomyces pombe, the NE remains intact during mitosis despite undergoing remarkable morphological transformations, usually from a sphere to a spherical cylinder, and then to a dumbbell before eventually separating into two identical daughter nuclei (a process often referred to as ''closed mitosis'') (3,4). It is widely known that such shape evolution is driven by the poleward force generated by kinesins along with other microtubule-associated proteins that reside at the overlapping region of antiparallel spindle microtubules (MTs) nucleated from the two spindle pole bodies (SPBs) at both ends of a dividing nucleus (5)(6)(7)(8).…”