Crossref journal-article
Rockefeller University Press
The Journal of Cell Biology (291)
Abstract

Spore formation in yeast is an unusual form of cell division in which the daughter cells are formed within the mother cell cytoplasm. This division requires the de novo synthesis of a membrane compartment, termed the prospore membrane, which engulfs the daughter nuclei. The effect of mutations in late-acting genes on sporulation was investigated. Mutation of SEC1, SEC4, or SEC8 blocked spore formation, and electron microscopic analysis of the sec4-8 mutant indicated that this inability to produce spores was caused by a failure to form the prospore membrane. The soluble NSF attachment protein 25 (SNAP-25) homologue SEC9, by contrast, was not required for sporulation. The absence of a requirement for SEC9 was shown to be due to the sporulation-specific induction of a second, previously undescribed, SNAP-25 homologue, termed SPO20. These results define a developmentally regulated branch of the secretory pathway and suggest that spore morphogenesis in yeast proceeds by the targeting and fusion of secretory vesicles to form new plasma membranes in the interior of the mother cell. Consistent with this model, the extracellular proteins Gas1p and Cts1p were localized to an internal compartment in sporulating cells. Spore formation in yeast may be a useful model for understanding secretion-driven cell division events in a variety of plant and animal systems.

Bibliography

Neiman, A. M. (1998). Prospore Membrane Formation Defines a Developmentally Regulated Branch of the Secretory Pathway in Yeast. The Journal of Cell Biology, 140(1), 29–37.

Authors 1
  1. Aaron M. Neiman (first)
References 41 Referenced 178
  1. 10.1002/j.1460-2075.1993.tb06093.x / EMBO (Eur Mol Biol Organ) J / Yeast syntaxins Sso1p and Sso2p belong to a family of related membrane proteins that function in vesicular transport by Aalto (1993)
  2. 10.1242/jcs.3.4.573 / J Cell Sci / The formation of the generative cell in the pollen grain of Emdmyion non-scriptus(L) by Angold (1968)
  3. 10.1016/0092-8674(94)90194-5 / Cell / Sec9 is a SNAP-25-like component of a yeast SNARE complex that may be the effector of Sec4 function in exocytosis by Brennwald (1994)
  4. 10.1101/gad.4.10.1775 / Genes Dev / Isolation of two developmentally regulated genes involved in spore wall maturation in Saccharomyces cerevisiae. by Briza (1990)
  5. {'key': '2023072207204795800_B5'}
  6. {'key': '2023072207204795800_B6'}
  7. 10.1083/jcb.132.3.399 / J Cell Biol / Identification of a developmentally regulated septin and involvement of the septins in spore formation in Saccharomyces cerevisiae. by Fares (1996)
  8. 10.1101/gad.8.18.2162 / Genes Dev / Mutation of the SPS1- encoded protein kinase of Saccharomyces cerevisiaeleads to defects in transcription and morphology during spore formation by Friesen (1994)
  9. 10.1007/BF01248742 / Protoplasma / Generative cell envelope in pollen grains as a secretion system, a postulate by Gimenez-Martin (1969)
  10. 10.1083/jcb.131.2.297 / J Cell Biol / Parallel secretory pathways to the cell surface in yeast by Harsay (1995)
  11. 10.1242/jcs.3.3.457 / J Cell Sci / Synchronous pollen mitosis and the formation of generative cell in massulate orchids by Heslop-Harrison (1968)
  12. 10.1101/gad.8.18.2151 / Genes Dev / SMK1, a developmentally regulated MAP kinase, is required for spore wall assembly in Saccharomyces cerevisiae. by Krisak (1994)
  13. {'key': '2023072207204795800_B13'}
  14. 10.1073/pnas.84.9.2585 / Proc Natl Acad Sci USA / Cloning and heterologous expression of glycosidase genes from Saccharomyces cerevisiae. by Kuranda (1987)
  15. {'key': '2023072207204795800_B15'}
  16. 10.1073/pnas.92.6.2199 / Proc Natl Acad Sci USA / Cell membrane formation during the cellularization of the syncytial blastoderm of Drosophila. by Loncar (1995)
  17. 10.1083/jcb.44.3.688 / J Cell Biol / Development of the spore wall during ascospore formation in Saccharomyces cerevisiae. by Lynn (1970)
  18. 10.2307/3869779 / Plant Cell / Male gametophyte development by McCormick (1993)
  19. 10.1139/m71-084 / Can J Microbiol / Fine structure of ascospore development in the yeast Saccharomyces cerevisiae. by Moens (1971)
  20. 10.1083/jcb.50.2.344 / J Cell Biol / Spindles, spindle plaques, and meiosis in the yeast Saccharomyces cerevisiae(Hansen) by Moens (1971)
  21. 10.1016/0014-4827(74)90700-9 / Exp Cell Res / Aberrant nuclear behavior at meiosis and anucleate spore formation by sporulation-deficient (SPO) mutants of Saccharomyces cerevisiae. by Moens (1974)
  22. 10.1093/genetics/145.3.637 / Genetics / Saccharomyces cerevisiae HOC1, a suppressor of pkc1, encodes a putative glycosyltransferase by Neiman (1997)
  23. 10.1016/0092-8674(81)90064-7 / Cell / Order of events in the yeast secretory pathway by Novick (1981)
  24. {'key': '2023072207204795800_B24', 'first-page': '27', 'article-title': 'Determinants for glycophospholipid anchoring of the Saccharomyces cerevisiaeGAS1 protein to the plasma membrane', 'volume': '11', 'author': 'Nuoffer', 'year': '1991', 'journal-title': 'Mol Cell Biol'} / Mol Cell Biol / Determinants for glycophospholipid anchoring of the Saccharomyces cerevisiaeGAS1 protein to the plasma membrane by Nuoffer (1991)
  25. 10.1002/j.1460-2075.1988.tb03005.x / EMBO (Eur Mol Biol Organ) J / Sorting of soluble ER proteins in yeast by Pelham (1988)
  26. 10.1016/0092-8674(93)90465-3 / Cell / Homologues of the synaptobrevin/VAMP family of synaptic vesicle proteins function in the late secretory pathway in S. cerevisiae. by Protopopov (1993)
  27. 10.1073/pnas.92.26.12151 / Proc Natl Acad Sci USA / Phospholipase D signaling is essential for meiosis by Rose (1995)
  28. {'key': '2023072207204795800_B28'}
  29. 10.1038/372055a0 / Nature / Mechanisms of intracellular protein transport by Rothman (1994)
  30. 10.1073/pnas.83.10.3248 / Proc Natl Acad Sci USA / Overproduction-induced mislocalization of a yeast vacuolar protein allows isolation of its structural gene by Rothman (1986)
  31. 10.1016/0076-6879(83)01015-0 / Methods Enzymol / One-step gene disruption in yeast by Rothstein (1983)
  32. 10.1016/0092-8674(87)90455-7 / Cell / A ras-like protein is required for a post-Golgi event in yeast secretion by Salminen (1987)
  33. 10.1093/genetics/122.1.19 / Genetics / A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. by Sikorski (1989)
  34. 10.1038/362318a0 / Nature / SNAP receptors implicated in vesicle targeting and fusion by Söllner (1993)
  35. 10.1016/0092-8674(94)90270-4 / Cell / A Rab protein is required for the assembly of SNARE complexes in the docking of transport vesicles by Søgaard (1994)
  36. 10.1016/S0092-8674(00)81060-0 / Cell / Cytokinesis in higher plants by Staehelin (1996)
  37. 10.1083/jcb.130.2.299 / J Cell Biol / Sec6, Sec8, and Sec15 are components of a multisubunit complex which localizes to small bud tips in Saccharomyces cerevisiae. by TerBush (1995)
  38. 10.1007/BF00335253 / Z Zellforsch / Dynamics of spermiogenesis in Drosophila melanogaster. I. Individualization process by Tokuyasu (1972)
  39. 10.1128/MCB.16.8.4199 / Mol Cell Biol / Protein phosphatase type 1 interacts with proteins required for meiosis and other cellular processes in Saccharomyces cerevisiae. by Tu (1996)
  40. 10.1016/0955-0674(91)90149-S / Curr Opin Cell Biol / Spatial aspects of cytokinesis in plant cells by Wick (1991)
  41. 10.1002/(SICI)1097-0061(199704)13:5<399::AID-YEA126>3.0.CO;2-9 / Yeast / An overview of the Saccharomyces cerevisiaemicrotubule and microfilament cytoskeleton by Winsor (1997)
Dates
Type When
Created 23 years, 1 month ago (July 26, 2002, 12:47 p.m.)
Deposited 2 years, 1 month ago (July 22, 2023, 3:21 a.m.)
Indexed 1 month, 1 week ago (July 20, 2025, 12:12 a.m.)
Issued 27 years, 7 months ago (Jan. 12, 1998)
Published 27 years, 7 months ago (Jan. 12, 1998)
Published Online 27 years, 7 months ago (Jan. 12, 1998)
Published Print 27 years, 7 months ago (Jan. 12, 1998)
Funders 0

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@article{Neiman_1998, title={Prospore Membrane Formation Defines a Developmentally Regulated Branch of the Secretory Pathway in Yeast}, volume={140}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.140.1.29}, DOI={10.1083/jcb.140.1.29}, number={1}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Neiman, Aaron M.}, year={1998}, month=jan, pages={29–37} }