Microtubule dynamics and organization during hyphal growth and branching in Neurospora crassa

Mouriño-Pérez, Rosa R.; Roberson, Robert W.; Bartnicki-García, S.

doi:10.1016/j.fgb.2005.10.007

Cited by 83 publications

(86 citation statements)

References 63 publications

(100 reference statements)

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“…The migration and positioning of nuclei within fungal hyphae have been reported to be regulated by the microtubuleassociated motor protein dynein and its activator, dynactin (9,38,41,49). Our analysis of three ropy mutants that were defective in different components of the cytoplasmic dynein/ dynactin complex confirmed its role in nuclear positioning because the nuclei of these mutants had a strong tendency to remain in the conidium after germination.…”

Section: Discussionsupporting

confidence: 65%

“…However, these roles are not well understood and may differ in different types of hyphae and in different species. The available evidence suggests that microtubules are required for maintaining the fast growth rate, the shape of the tip, and the directionality of mature vegetative hyphae (30,41,53). Horio and Oakley (30) reported previously that cytoplasmic microtubules in A. nidulans disappear altogether during the synchronized mitoses that occur within germ tubes but that germ tubes continued to grow during this period.…”

Section: Discussionmentioning

confidence: 99%

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Nuclear Dynamics, Mitosis, and the Cytoskeleton during the Early Stages of Colony Initiation in Neurospora crassa

et al. 2010

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Neurospora crassa macroconidia form germ tubes that are involved in colony establishment and conidial anastomosis tubes (CATs) that fuse to form interconnected networks of conidial germlings. Nuclear and cytoskeletal behaviors were analyzed in macroconidia, germ tubes, and CATs in strains that expressed fluorescently labeled proteins. Heterokaryons formed by CAT fusion provided a rapid method for the imaging of multiple labeled fusion proteins and minimized the potential risk of overexpression artifacts. Mitosis occurred more slowly in nongerminated macroconidia (1.0 to 1.5 h) than in germ tubes (16 to 20 min). The nucleoporin SON-1 was not released from the nuclear envelope during mitosis, which suggests that N. crassa exhibits a form of "closed mitosis." During CAT homing, nuclei did not enter CATs, and mitosis was arrested. Benomyl treatment showed that CAT induction, homing, fusion, as well as nuclear migration through fused CATs do not require microtubules or mitosis. Three ropy mutants (ro-1, ro-3, and ro-11) defective in the dynein/dynactin microtubule motor were impaired in nuclear positioning, but nuclei still migrated through fused CATs. Latrunculin B treatment, imaging of F-actin in living cells using Lifeact-red fluorescent protein (RFP), and analysis of mutants defective in the Arp2/3 complex demonstrated that actin plays important roles in CAT fusion.

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Section: Discussionsupporting

confidence: 65%

Section: Discussionmentioning

confidence: 99%

Nuclear Dynamics, Mitosis, and the Cytoskeleton during the Early Stages of Colony Initiation in Neurospora crassa

et al. 2010

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“…Cytoplasmic microtubules first become associated with the branch site at the same time the Spitzenkorper appears (Mourino-Perez et al 2006). Further microtubule organization at the branch site appears to reflect both the pulling of existing microtubules into the branch and the nucleation of microtubules within the new tip.…”

Section: How Are Branches Formed?mentioning

confidence: 97%

Branching of fungal hyphae: regulation, mechanisms and comparison with other branching systems

2008

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"Branching of fungal hyphae: regulation, mechanisms and comparison with other branching systems" (2008 Abstract: The ability of rapidly growing hyphae to generate new polarity axes that result in the formation of a branch represents one of the most important yet least understood aspects of fungal cell biology. Branching is central to the development of mycelial colonies and also appears to play a key role in fungal interactions with other organisms. This review presents a description of the two major patterns of hyphal branching, apical and lateral, and highlights the roles of internal and external factors in the induction of branch formation. In addition, potential mechanisms underlying branch site selection are outlined, and the possible roles of multiple signaling pathways (i.e., G protein alpha, Cdc42, NDR kinases) and subcellular structures (i.e., the Spitzenkorper, septins) are discussed. Finally, other forms of branching in the plant and animal kingdoms are briefly summarized and compared to hyphal branching.

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“…However, it is not exactly known how nuclei move apart and which cortical forces dictate their dispersion and final positioning at the cortex. An essential role of dynein and cMTs in controlling movements and distribution of multiple nuclei in a common cytoplasm has also been documented for several filamentous fungi (Morris, 2002;Xiang and Fischer, 2004;Fink et al, 2006;Mouriño-Pérez et al, 2006). Attempts to analyze molecular mechanisms for controlling movements of multiple nuclei in these fungi were hampered by the fact that dynein and cMTs are also involved in essential transports of organelles.…”

Section: Introductionmentioning

confidence: 99%

Mechanism of Nuclear Movements in a Multinucleated Cell

Gibeaux

Politi

Philippsen

et al. 2016

Preprint

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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 ...

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Microtubule dynamics and organization during hyphal growth and branching in Neurospora crassa

Cited by 83 publications

References 63 publications

Nuclear Dynamics, Mitosis, and the Cytoskeleton during the Early Stages of Colony Initiation in Neurospora crassa

Nuclear Dynamics, Mitosis, and the Cytoskeleton during the Early Stages of Colony Initiation in Neurospora crassa

Branching of fungal hyphae: regulation, mechanisms and comparison with other branching systems

Mechanism of Nuclear Movements in a Multinucleated Cell

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