Mechanism of Nuclear Movements in a Multinucleated Cell

Abstract

Multinucleated cells are important in many organisms, but the mechanisms governing the movements of nuclei sharing a common cytoplasm are not understood. In the hyphae of the plant pathogenic fungus Ashbya gossypii, nuclei move back and forth, occasionally bypassing each other, preventing the formation of nuclear clusters. This is essential for genetic stability. These movements depend on cytoplasmic microtubules emanating from the nuclei that are pulled by dynein motors anchored at the cortex. Using three-dimensional stochastic simulations with parameters constrained by the literature, we predict the cortical anchor density from the characteristics of nuclear movements. The model accounts for the complex nuclear movements seen in vivo, using a minimal set of experimentally determined ingredients. Of interest, these ingredients power the oscillations of the anaphase spindle in budding yeast, but in A. gossypii, this system is not restricted to a specific nuclear cycle stage, possibly as a result of adaptation to hyphal growth and multinuclearity. INTRODUCTIONPositioning of the nucleus and mitotic spindle appropriately within the cell is critical in eukaryotes during many processes, ranging from simple growth to tissue development (Morris, 2002;Dupin and Etienne-Manneville, 2011;Gundersen and Worman, 2013;Kiyomitsu, 2015). Accordingly, cells have evolved various strategies to place their nucleus or spindle in suitable locations. In most systems, this process is driven by dynein pulling on nuclei-associated cytoplasmic microtubules (cMTs). Dynein is a minus end-directed motor that can act primarily in two ways. End-on pulling occurs when cortex-anchored dynein captures a growing cMT plus end, thereby initiating its shrinkage while maintaining the attachment. Lateral or side-on pulling occurs when cortex-anchored dynein walks on cMTs toward the minus end using its motor activity. This mode of action is independent of cMT shrinkage and may result in cMT sliding parallel to the cortex (Kotak and Gönczy, 2013;McNally, 2013;Akhmanova and van den Heuvel, 2016).A detailed mechanistic view for directing nuclei during the cell cycle is known in the budding yeast Saccharomyces cerevisiae, as outlined in Figure 1 and references therein. In contrast to most eukaryotic cells, the site of the cleavage plane in S. cerevisiae is selected early in the cell cycle by generating a ring structure (future bud neck) at the mother cell cortex at which the daughter cell (bud) will emerge. In addition, in budding yeast the nuclear envelope does not disassemble during mitosis, and nuclei are always attached to the minus end of cMTs via spindle pole bodies (SPBs) embedded in the nuclear envelope. The two pathways elucidated in S. cerevisiae involve cortical pulling, but only the second pathway relies on dynein. During the Kar9-Bim1-Myo2 pathway, the nucleus is directed toward the bud neck by transporting cMT plus ends first along bud neck-emerging actin cables, followed by depolymerization of the transported cMT. In metaphase, cMTs ...

Fungal evolution: cellular, genomic and metabolic complexity

“…Cytoplasmic currents prevent stochastic extinction by actively mixing the cytoplasm of the whole colony (Roper et al ., , ; Johannesson & Samils, ). In Eremothecium , however, nuclear migration is mediated by the cytoskeleton (Gladfelter, ; Anderson et al ., ; Dundon et al ., ; Gibeaux et al ., ). The ability to transport nuclei from distant regions in the network would provide a steady supply of nuclei, maintaining directed growth even if comparatively less‐fit nuclei are present, as is likely to be the case to some degree in any nuclear population (Nobre et al ., ; Anderson et al ., ).…”

Effects of a proteasome inhibitor on the riboflavin production in Ashbya gossypii

“…Growth rates of WT strain and AgSDH1 −/+ were almost the same because the sizes of both colonies are the same. A. gossypii is a multinucleate fungus and a cell has multiple nuclei (Gibeaux et al, 2017;Gladfelter et al, 2006). A cell of the heterozygous strain has genomes of both WT strain and AgSDH1∆.…”

“…A . gossypii is a multinucleate fungus and a cell has multiple nuclei (Gibeaux et al, 2017; Gladfelter et al, 2006). A cell of the heterozygous strain has genomes of both WT strain and AgSDH1∆ .…”

Aster Swarming by Collective Mechanics of Dyneins and Kinesins

“…Asters contacting these membrane anchored motors result in radial pulling forces acting on asters driving them to the cell center in cells with sizes comparable to the asters [36]. In multi-nucleate cells such as the filamentous fungus Ashbya gossypii, these astral-MT interactions with cortical dynein are essential for maintaining a regular spacing between nuclei [18]. Cortical dynein localization forms the mechanical basis of the asymmetric cell division of one-celled embryos of C. elegans [20] and the cortical density of dynein has been shown to determine spindle oscillations [53].…”