Microtubule‐organizing centers of <i>Aspergillus nidulans</i> are anchored at septa by a disordered protein

Zhang, Ying; Gao, Xiaolei; Manck, Raphael; Schmid, Marjorie; Osmani, Aysha H.; Osmani, Stephen A.; Takeshita, Norio; Fischer, Reinhard

doi:10.1111/mmi.13763

Cited by 35 publications

(38 citation statements)

References 80 publications

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“…␥-Tubulin itself was detectable only at septa in interaction assays with ApsB (orthologue of S. pombe Mto1) (129). In a recent study, it was suggested that SPB outer plaque proteins are conserved at septal MTOCs (sMTOCs), in contrast to proteins specific for the central or the inner plaque (130). It was shown that the protein complex is recruited during septation to the constricting ring with the help of two intrinsically disordered proteins, Spa18 (Mto2 in S. pombe) and Spa10.…”

Section: The Fungal Cytoskeleton the Microtubule Cytoskeletonmentioning

confidence: 99%

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

Riquelme

Aguirre

Bartnicki-García

et al. 2018

Microbiol Mol Biol Rev

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288

246

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SUMMARYFilamentous fungi constitute a large group of eukaryotic microorganisms that grow by forming simple tube-like hyphae that are capable of differentiating into more-complex morphological structures and distinct cell types. Hyphae form filamentous networks by extending at their tips while branching in subapical regions. Rapid tip elongation requires massive membrane insertion and extension of the rigid chitin-containing cell wall. This process is sustained by a continuous flow of secretory vesicles that depends on the coordinated action of the microtubule and actin cytoskeletons and the corresponding motors and associated proteins. Vesicles transport cell wall-synthesizing enzymes and accumulate in a special structure, the Spitzenkörper, before traveling further and fusing with the tip membrane. The place of vesicle fusion and growth direction are enabled and defined by the position of the Spitzenkörper, the so-called cell end markers, and other proteins involved in the exocytic process. Also important for tip extension is membrane recycling by endocytosis via early endosomes, which function as multipurpose transport vehicles for mRNA, septins, ribosomes, and peroxisomes. Cell integrity, hyphal branching, and morphogenesis are all processes that are largely dependent on vesicle and cytoskeleton dynamics. When hyphae differentiate structures for asexual or sexual reproduction or to mediate interspecies interactions, the hyphal basic cellular machinery may be reprogrammed through the synthesis of new proteins and/or the modification of protein activity. Although some transcriptional networks involved in such reprogramming of hyphae are well studied in several model filamentous fungi, clear connections between these networks and known determinants of hyphal morphogenesis are yet to be established.

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Section: The Fungal Cytoskeleton the Microtubule Cytoskeletonmentioning

confidence: 99%

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

Riquelme

Aguirre

Bartnicki-García

et al. 2018

Microbiol Mol Biol Rev

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288

246

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“…In A . nidulans , there are MTOCs anchored at the septum (Zhang et al ., ). Many animal cells, especially differentiated ones like epithelial cells and neurons, often establish centrosome‐independent MT nucleation sites as well (Sanchez & Feldman, ).…”

Section: Mt Nucleation Sites or Flexible Mtocs In Plant Cellsmentioning

confidence: 99%

“…Furthermore, MTs can be nucleated without nucleus-associated MTOCs and assembled into interphase arrays along the cell axis (Carazo-Salas & Nurse, 2006). In A. nidulans, there are MTOCs anchored at the septum (Zhang et al, 2017). Many animal cells, especially differentiated ones like epithelial cells and neurons, often establish centrosomeindependent MT nucleation sites as well (Sanchez & Feldman, 2017).…”

Section: Mt Nucleation Sites or Flexible Mtocs In Plant Cellsmentioning

confidence: 99%

Microtubule nucleation for the assembly of acentrosomal microtubule arrays in plant cells

Lee

Liu

2019

New Phytologist

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Contents SummaryI.IntroductionII.MT arrays in plant cellsIII.γ‐Tubulin and MT nucleationIV.MT nucleation sites or flexible MTOCs in plant cellsV.MT‐dependent MT nucleationVI.Generating new MTs for spindle assemblyVII.Generation of MTs for phragmoplast expansion during cytokinesisVIII.MT generation for the cortical MT arrayIX.MT nucleation: looking forward AcknowledgementsReferences Summary Cytoskeletal microtubules (MTs) have a multitude of functions including intracellular distribution of molecules and organelles, cell morphogenesis, as well as segregation of the genetic material and separation of the cytoplasm during cell division among eukaryotic organisms. In response to internal and external cues, eukaryotic cells remodel their MT network in a regulated manner in order to assemble physiologically important arrays for cell growth, cell proliferation, or for cells to cope with biotic or abiotic stresses. Nucleation of new MTs is a critical step for MT remodeling. Although many key factors contributing to MT nucleation and organization are well conserved in different kingdoms, the centrosome, representing the most prominent microtubule organizing centers (MTOCs), disappeared during plant evolution as angiosperms lack the structure. Instead, flexible MTOCs may emerge on the plasma membrane, the nuclear envelope, and even organelles depending on types of cells and organisms and/or physiological conditions. MT‐dependent MT nucleation is particularly noticeable in plant cells because it accounts for the primary source of MT generation for assembling spindle, phragmoplast, and cortical arrays when the γ‐tubulin ring complex is anchored and activated by the augmin complex. It is intriguing what proteins are associated with plant‐specific MTOCs and how plant cells activate or inactivate MT nucleation activities in spatiotemporally regulated manners.

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“…Several SPA proteins have been identified in A . nidulans including SPA10 which locates to forming septa, remains stably associated at mature septa [ 13 ] and plays roles in nucleating microtubules from septa [ 20 ]. We therefore chose SPA10-GBP as a stable septal pore anchor for GFP-tagged proteins that do not normally associate with septa.…”

Section: Resultsmentioning

confidence: 99%

Tools for retargeting proteins within Aspergillus nidulans

et al. 2017

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Endogenously tagging proteins with green fluorescent protein (GFP) enables the visualization of the tagged protein using live cell microscopy. GFP-tagging is widely utilized to study biological processes in model experimental organisms including filamentous fungi such as Aspergillus nidulans. Many strains of A. nidulans have therefore been generated with different proteins endogenously tagged with GFP. To further enhance experimental approaches based upon GFP-tagging, we have adapted the GFP Binding Protein (GBP) system for A. nidulans. GBP is a genetically encoded Llama single chain antibody against GFP which binds GFP with high affinity. Using gene replacement approaches, it is therefore possible to link GBP to anchor proteins, which will then retarget GFP-tagged proteins away from their normal location to the location of the anchor-GBP protein. To facilitate this approach in A. nidulans, we made four base plasmid cassettes that can be used to generate gene replacement GBP-tagging constructs by utilizing fusion PCR. Using these base cassettes, fusion PCR, and gene targeting approaches, we generated strains with SPA10-GBP and Tom20-GBP gene replacements. These strains enabled test targeting of GFP-tagged proteins to septa or to the surface of mitochondria respectively. SPA10-GBP is shown to effectively target GFP-tagged proteins to both forming and mature septa. Tom20-GBP has a higher capacity to retarget GFP-tagged proteins being able to relocate all Nup49-GFP from its location within nuclear pore complexes (NPCs) to the cytoplasm in association with mitochondria. Notably, removal of Nup49-GFP from NPCs causes cold sensitivity as does deletion of the nup49 gene. The cassette constructs described facilitate experimental approaches to generate precise protein-protein linkages in fungi. The A. nidulans SPA10-GBP and Tom20-GBP strains can be utilized to modulate other GFP-tagged proteins of interest.

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Microtubule‐organizing centers of Aspergillus nidulans are anchored at septa by a disordered protein

Cited by 35 publications

References 80 publications

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

Microtubule nucleation for the assembly of acentrosomal microtubule arrays in plant cells

Tools for retargeting proteins within Aspergillus nidulans

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