During cell division, eukaryotic cells must faithfully pass on their genetic material to the next generation during mitosis. It has long been known that lower eukaryotes and higher eukaryotes achieve this in strikingly different ways. Higher eukaryotes undergo an open mitosis in which the nuclear envelope is completely disassembled at the G2/M transition and is not reassembled until after DNA segregation in telophase/G1. In contrast, many lower eukaryotes undergo a closed mitosis in which the nuclear envelope remains intact and mitosis occurs within the nucleus. However, classifying mitosis as being either open or closed has its limitations. Many early studies using phase and electron microscopy indicated that fungi have evolved variations in how the mitotic segregation of the DNA and the nuclear envelope is achieved (1, 2, 16, 38). For example, even in organisms which break down their nuclear envelope during mitosis, the phase during mitosis when the nuclear envelope breaks down can vary between organisms (16). Many of these early studies are described in an extensive and excellent review by Heath (16), which summarized the different morphological characteristics of many fungi and other lower eukaryotes during mitosis. More recently, the availability of fungal genome sequences combined with molecular genetics and live cell imaging has shed light on the mechanisms regulating such variant mitoses. Here we review recent advances in our understanding of fungal mitosis and discuss how the biology of different organisms and cell types may have necessitated variant mitoses.
The physical process of segregating duplicated chromosomes occurs on one of the most striking and dynamic of all subcellular structures, the mitotic spindle. Simplistically, the mitotic spindle is composed of microtubules which extend from each spindle pole and connect to the kinetochore region of chromosomes. Microtubules are composed of α and β tubulin subunits, and microtubule lengthening and shortening are important to segregate chromosomal DNA. One problem facing cells undergoing a closed mitosis is the need to relocalize tubulin and mitotic regulators from the cytoplasm to the nucleus in order to form a spindle within the nucleus. If the nuclear envelope is intact, the only way in and out of the nucleus is through nuclear pore complexes (NPCs) (17, 51). Therefore, in organisms undergoing a closed mitosis, tubulin must gain access to the nucleus through the NPC in order to form a spindle. NPCs are embedded in the nuclear envelope and act as molecular sieves, selectively facilitating the transport of proteins and nucleic acids in and out of the nucleus. Each nucleus contains many NPCs, which are composed of ~30 different proteins called nucleoporins, or Nups (17). The basic overall structure of the NPC is conserved between lower and higher eukaryotes, and many of the individual Nups can be identified in highly divergent species based on sequence homology (17). Not surprisingly, some Nups contain transmembrane domains and likely anchor the NPC in the nuclear envelope. Other Nups are part of a core ring structure which transits the nuclear envelope. The center of this ring structure is termed the central channel and acts as the gateway between the nucleus and cytoplasm (52, 53). The central channel of the NPC is occupied by a class of Nups which contain phenylalanine-glycine (FG) repeats and are termed FG-repeat Nups (39, 51, 52). In addition, other Nups form cytoplasmic fibrils and a nuclear basket (51). The FG-repeat Nups restrict the diffusion of macromolecules through the NPC central channel and also have the ability to bind transport factors carrying their cargo (11, 23, 39, 52). The binding of FG-repeat Nups to cargo-ladened transport factors helps facilitate active transport through the NPC in a Ran-dependent manner (5, 39, 45, 52).