Role of septins in the orientation of forespore membrane extension during sporulation in fission yeast

Masayuki Onishi, Takako Koga, Aiko Hirata, Taro Nakamura, Haruhiko Asakawa, Chikashi Shimoda, Jürg Bähler, Jian Qiu Wu, Kaoru Takegawa, Hiroyuki Tachikawa, John R. Pringle, Yasuhisa Fukui

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Abstract

During yeast sporulation, a forespore membrane (FSM) initiates at each spindle-pole body and extends to form the spore envelope. We used Schizosaccharomyces pombe to investigate the role of septins during this process. During the prior conjugation of haploid cells, the four vegetatively expressed septins (Spn1, Spn2, Spn3, and Spn4) coassemble at the fusion site and are necessary for its normal morphogenesis. Sporulation involves a different set of four septins (Spn2, Spn5, Spn6, and the atypical Spn7) that does not include the core subunits of the vegetative septin complex. The four sporulation septins form a complex in vitro and colocalize interdependently to a ring-shaped structure along each FSM, and septin mutations result in disoriented FSM extension. The septins and the leading-edge proteins appear to function in parallel to orient FSM extension. Spn2 and Spn7 bind to phosphatidylinositol 4-phosphate [PtdIns(4)P] in vitro, and PtdIns(4)P is enriched in the FSMs, suggesting that septins bind to the FSMs via this lipid. Cells expressing a mutant Spn2 protein unable to bind PtdIns(4)P still form extended septin structures, but these structures fail to associate with the FSMs, which are frequently disoriented. Thus, septins appear to form a scaffold that helps to guide the oriented extension of the FSM.

Original languageEnglish
Pages (from-to)2057-2074
Number of pages18
JournalMolecular and cellular biology
Volume30
Issue number8
DOIs
Publication statusPublished - Apr 1 2010

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Septins
Schizosaccharomyces
Membranes
Spindle Pole Bodies
Haploidy
Mutant Proteins
Spores
Morphogenesis
Yeasts

All Science Journal Classification (ASJC) codes

  • Molecular Biology
  • Cell Biology

Cite this

Onishi, M., Koga, T., Hirata, A., Nakamura, T., Asakawa, H., Shimoda, C., ... Fukui, Y. (2010). Role of septins in the orientation of forespore membrane extension during sporulation in fission yeast. Molecular and cellular biology, 30(8), 2057-2074. https://doi.org/10.1128/MCB.01529-09

Role of septins in the orientation of forespore membrane extension during sporulation in fission yeast. / Onishi, Masayuki; Koga, Takako; Hirata, Aiko; Nakamura, Taro; Asakawa, Haruhiko; Shimoda, Chikashi; Bähler, Jürg; Wu, Jian Qiu; Takegawa, Kaoru; Tachikawa, Hiroyuki; Pringle, John R.; Fukui, Yasuhisa.

In: Molecular and cellular biology, Vol. 30, No. 8, 01.04.2010, p. 2057-2074.

Research output: Contribution to journalArticle

Onishi, M, Koga, T, Hirata, A, Nakamura, T, Asakawa, H, Shimoda, C, Bähler, J, Wu, JQ, Takegawa, K, Tachikawa, H, Pringle, JR & Fukui, Y 2010, 'Role of septins in the orientation of forespore membrane extension during sporulation in fission yeast', Molecular and cellular biology, vol. 30, no. 8, pp. 2057-2074. https://doi.org/10.1128/MCB.01529-09
Onishi, Masayuki ; Koga, Takako ; Hirata, Aiko ; Nakamura, Taro ; Asakawa, Haruhiko ; Shimoda, Chikashi ; Bähler, Jürg ; Wu, Jian Qiu ; Takegawa, Kaoru ; Tachikawa, Hiroyuki ; Pringle, John R. ; Fukui, Yasuhisa. / Role of septins in the orientation of forespore membrane extension during sporulation in fission yeast. In: Molecular and cellular biology. 2010 ; Vol. 30, No. 8. pp. 2057-2074.
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