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

Summary Microtubule‐organizing centers (MTOCs) are large, multi‐subunit protein complexes. Schizosaccharomyces pombe harbors MTOCs at spindle pole bodies, transient MTOCs in the division plane (eMTOCs) and nuclear‐envelope associated MTOCs in interphase cells (iMTOCs). In the filamentous fungus Aspe...

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Veröffentlicht in:Molecular microbiology 2017-10, Vol.106 (2), p.285-303
Hauptverfasser: Zhang, Ying, Gao, Xiaolei, Manck, Raphael, Schmid, Marjorie, Osmani, Aysha H., Osmani, Stephen A., Takeshita, Norio, Fischer, Reinhard
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container_end_page 303
container_issue 2
container_start_page 285
container_title Molecular microbiology
container_volume 106
creator Zhang, Ying
Gao, Xiaolei
Manck, Raphael
Schmid, Marjorie
Osmani, Aysha H.
Osmani, Stephen A.
Takeshita, Norio
Fischer, Reinhard
description Summary Microtubule‐organizing centers (MTOCs) are large, multi‐subunit protein complexes. Schizosaccharomyces pombe harbors MTOCs at spindle pole bodies, transient MTOCs in the division plane (eMTOCs) and nuclear‐envelope associated MTOCs in interphase cells (iMTOCs). In the filamentous fungus Aspergillus nidulans SPBs and septum‐associated MTOCs were described. Although comparable to S. pombe eMTOCs, A. nidulans sMTOCS are permanent septum‐associated structures. The composition of sMTOCs is poorly understood and how they are targeted to septa was unknown. Here, we show that in A. nidulans several SPB outer plaque proteins also locate to sMTOCs while other SPB proteins do not, including SfiA, a protein required for SPB duplication in Saccharomyces cerevisiae and S. pombe and PcpA, the anchor for γ‐TuSCs at the SPB inner plaque. The A. nidulans disordered protein Spa18Mto2 and the centrosomin‐domain containing protein ApsBMto1 were required for recruiting the γ‐TuRC component GcpC to sMTOCs and for seeding MT formation from septa. Testing different septum‐associated proteins for a role in sMTOC function, Spa10 was identified. It forms a septal pore disc structure, recruits Spa18 and ApsB to septa and is required for sMTOC activity. This is the first evidence for a septum‐specific protein, Spa10, as anchor for a specific class of MTOCs. Microtubules are polymerized from large protein complexes with gamma tubulin as a central component. In fungi spindle pole bodies polymerize mitotic as well as cytoplasmic microtubules. There is good evidence that other microtubule‐organizing centers exist at septa of filamentous fungi. We studied the composition of septal MTOCs in Aspergillus nidulans and identified a disordered protein required for their anchorage.
doi_str_mv 10.1111/mmi.13763
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Schizosaccharomyces pombe harbors MTOCs at spindle pole bodies, transient MTOCs in the division plane (eMTOCs) and nuclear‐envelope associated MTOCs in interphase cells (iMTOCs). In the filamentous fungus Aspergillus nidulans SPBs and septum‐associated MTOCs were described. Although comparable to S. pombe eMTOCs, A. nidulans sMTOCS are permanent septum‐associated structures. The composition of sMTOCs is poorly understood and how they are targeted to septa was unknown. Here, we show that in A. nidulans several SPB outer plaque proteins also locate to sMTOCs while other SPB proteins do not, including SfiA, a protein required for SPB duplication in Saccharomyces cerevisiae and S. pombe and PcpA, the anchor for γ‐TuSCs at the SPB inner plaque. The A. nidulans disordered protein Spa18Mto2 and the centrosomin‐domain containing protein ApsBMto1 were required for recruiting the γ‐TuRC component GcpC to sMTOCs and for seeding MT formation from septa. Testing different septum‐associated proteins for a role in sMTOC function, Spa10 was identified. It forms a septal pore disc structure, recruits Spa18 and ApsB to septa and is required for sMTOC activity. This is the first evidence for a septum‐specific protein, Spa10, as anchor for a specific class of MTOCs. Microtubules are polymerized from large protein complexes with gamma tubulin as a central component. In fungi spindle pole bodies polymerize mitotic as well as cytoplasmic microtubules. There is good evidence that other microtubule‐organizing centers exist at septa of filamentous fungi. 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Schizosaccharomyces pombe harbors MTOCs at spindle pole bodies, transient MTOCs in the division plane (eMTOCs) and nuclear‐envelope associated MTOCs in interphase cells (iMTOCs). In the filamentous fungus Aspergillus nidulans SPBs and septum‐associated MTOCs were described. Although comparable to S. pombe eMTOCs, A. nidulans sMTOCS are permanent septum‐associated structures. The composition of sMTOCs is poorly understood and how they are targeted to septa was unknown. Here, we show that in A. nidulans several SPB outer plaque proteins also locate to sMTOCs while other SPB proteins do not, including SfiA, a protein required for SPB duplication in Saccharomyces cerevisiae and S. pombe and PcpA, the anchor for γ‐TuSCs at the SPB inner plaque. The A. nidulans disordered protein Spa18Mto2 and the centrosomin‐domain containing protein ApsBMto1 were required for recruiting the γ‐TuRC component GcpC to sMTOCs and for seeding MT formation from septa. 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Schizosaccharomyces pombe harbors MTOCs at spindle pole bodies, transient MTOCs in the division plane (eMTOCs) and nuclear‐envelope associated MTOCs in interphase cells (iMTOCs). In the filamentous fungus Aspergillus nidulans SPBs and septum‐associated MTOCs were described. Although comparable to S. pombe eMTOCs, A. nidulans sMTOCS are permanent septum‐associated structures. The composition of sMTOCs is poorly understood and how they are targeted to septa was unknown. Here, we show that in A. nidulans several SPB outer plaque proteins also locate to sMTOCs while other SPB proteins do not, including SfiA, a protein required for SPB duplication in Saccharomyces cerevisiae and S. pombe and PcpA, the anchor for γ‐TuSCs at the SPB inner plaque. The A. nidulans disordered protein Spa18Mto2 and the centrosomin‐domain containing protein ApsBMto1 were required for recruiting the γ‐TuRC component GcpC to sMTOCs and for seeding MT formation from septa. Testing different septum‐associated proteins for a role in sMTOC function, Spa10 was identified. It forms a septal pore disc structure, recruits Spa18 and ApsB to septa and is required for sMTOC activity. This is the first evidence for a septum‐specific protein, Spa10, as anchor for a specific class of MTOCs. Microtubules are polymerized from large protein complexes with gamma tubulin as a central component. In fungi spindle pole bodies polymerize mitotic as well as cytoplasmic microtubules. There is good evidence that other microtubule‐organizing centers exist at septa of filamentous fungi. We studied the composition of septal MTOCs in Aspergillus nidulans and identified a disordered protein required for their anchorage.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>28787538</pmid><doi>10.1111/mmi.13763</doi><tpages>19</tpages><orcidid>https://orcid.org/0000-0002-6704-2569</orcidid><oa>free_for_read</oa></addata></record>
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subjects Amino Acid Sequence - genetics
Aspergillus nidulans
Aspergillus nidulans - metabolism
Eukaryotes
Fungal Proteins - metabolism
Fungi
Microtubule-Associated Proteins - metabolism
Microtubule-Organizing Center - metabolism
Microtubules - metabolism
Protein Binding - physiology
Protein Transport - genetics
Proteins
Saccharomyces cerevisiae
Saccharomyces cerevisiae Proteins - metabolism
Schizosaccharomyces - metabolism
Schizosaccharomyces pombe Proteins - metabolism
Septum
Spindle Apparatus - metabolism
Spindle pole bodies
Tubulin - metabolism
Yeast
title Microtubule‐organizing centers of Aspergillus nidulans are anchored at septa by a disordered protein
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