Identification of a developmentally regulated septin and involvement of the septins in spore formation in Saccharomyces cerevisiae

doi:10.1083/jcb.132.3.399

This Article

	Full Text (PDF, 2853K)
	Alert me when this article is cited
	Citation Map

Services

	Email this article
	Similar articles in this journal
	Similar articles in PubMed
	Alert me to new content in the JCB
	Download to citation manager

Citing Articles

	Citing Articles via HighWire
	Citing Articles via CrossRef
	Citing Articles via Google Scholar

Google Scholar

	Articles by Fares, H.
	Articles by Pringle, J. R.
	Search for Related Content

PubMed

	PubMed Citation
	Articles by Fares, H.
	Articles by Pringle, J. R.


Social Bookmarking

	What's this?

ARTICLES

Identification of a developmentally regulated septin and involvement of the septins in spore formation in Saccharomyces cerevisiae

H Fares, L Goetsch and JR Pringle
Department of Biology, University of North Carolina, Chapel Hill 27599, USA.

The Saccharomyces cerevisiae CDC3, CDC10, CDC11, and CDC12 genes encode a family of related proteins, the septins, which are involved in cell division and the organization of the cell surface during vegetative growth. A search for additional S. cerevisiae septin genes using the polymerase chain reaction identified SPR3, a gene that had been identified previously on the basis of its sporulation-specific expression. The predicted SPR3 product shows 25-40% identity in amino acid sequence to the previously known septins from S. cerevisiae and other organisms. Immunoblots confirmed the sporulation-specific expression of Spr3p and showed that other septins are also present at substantial levels in sporulating cells. Consistent with the expression data, deletion of SPR3 in either of two genetic backgrounds had no detectable effect on exponentially growing cells. In one genetic background, deletion of SPR3 produced a threefold reduction in sporulation efficiency, although meiosis appeared to be completed normally. In this background, deletion of CDC10 had no detectable effect on sporulation. In the other genetic background tested, the consequences of the two deletions were reversed. Immunofluorescence observations suggest that Spr3p, Cdc3p, and Cdc11p are localized to the leading edges of the membrane sacs that form near the spindle-pole bodies and gradually extend to engulf the nuclear lobes that contain the haploid chromosome sets, thus forming the spores. Deletion of SPR3 does not prevent the localization of Cdc3p and Cdc11p, but these proteins appear to be less well organized, and the intensity of their staining is reduced. Taken together, the results suggest that the septins play important but partially redundant roles during the process of spore formation.
Add to CiteULike CiteULike Add to Complore Complore Add to Connotea Connotea Add to Del.icio.us Del.icio.us Add to Digg Digg Facebook Add to Reddit Reddit Add to Technorati Technorati Twitter What's this?

This article has been cited by other articles:

Ishihara, M., Suda, Y., Inoue, I., Tanaka, T., Takahashi, T., Gao, X.-D., Fukui, Y., Ihara, S., Neiman, A. M., Tachikawa, H. (2009). Protein Phosphatase Type 1-Interacting Protein Ysw1 Is Involved in Proper Septin Organization and Prospore Membrane Formation during Sporulation. Eukaryot Cell 8: 1027-1037 [Abstract] [Full Text]
Nagaraj, S., Rajendran, A., Jackson, C. E., Longtine, M. S. (2008). Role of Nucleotide Binding in Septin-Septin Interactions and Septin Localization in Saccharomyces cerevisiae. Mol. Cell. Biol. 28: 5120-5137 [Abstract] [Full Text]
Schlecht, U., Erb, I., Demougin, P., Robine, N., Borde, V., Nimwegen, E. v., Nicolas, A., Primig, M. (2008). Genome-wide Expression Profiling, In Vivo DNA Binding Analysis, and Probabilistic Motif Prediction Reveal Novel Abf1 Target Genes during Fermentation, Respiration, and Sporulation in Yeast. Mol. Biol. Cell 19: 2193-2207 [Abstract] [Full Text]
Huang, Y.-W., Yan, M., Collins, R. F., DiCiccio, J. E., Grinstein, S., Trimble, W. S. (2008). Mammalian Septins Are Required for Phagosome Formation. Mol. Biol. Cell 19: 1717-1726 [Abstract] [Full Text]
Suda, Y., Nakanishi, H., Mathieson, E. M., Neiman, A. M. (2007). Alternative Modes of Organellar Segregation during Sporulation in Saccharomyces cerevisiae. Eukaryot Cell 6: 2009-2017 [Abstract] [Full Text]
Pablo-Hernando, M. E., Arnaiz-Pita, Y., Nakanishi, H., Dawson, D., del Rey, F., Neiman, A. M., de Aldana, C. R. V. (2007). Cdc15 Is Required for Spore Morphogenesis Independently of Cdc14 in Saccharomyces cerevisiae. Genetics 177: 281-293 [Abstract] [Full Text]
Krajaejun, T., Gauthier, G. M., Rappleye, C. A., Sullivan, T. D., Klein, B. S. (2007). Development and Application of a Green Fluorescent Protein Sentinel System for Identification of RNA Interference in Blastomyces dermatitidis Illuminates the Role of Septin in Morphogenesis and Sporulation. Eukaryot Cell 6: 1299-1309 [Abstract] [Full Text]
Lesage, G., Bussey, H. (2006). Cell Wall Assembly in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 70: 317-343 [Abstract] [Full Text]
Neiman, A. M. (2005). Ascospore Formation in the Yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69: 565-584 [Abstract] [Full Text]
Douglas, L. M., Alvarez, F. J., McCreary, C., Konopka, J. B. (2005). Septin Function in Yeast Model Systems and Pathogenic Fungi. Eukaryot Cell 4: 1503-1512 [Full Text]
Morishita, M., Engebrecht, J. (2005). End3p-Mediated Endocytosis Is Required for Spore Wall Formation in Saccharomyces cerevisiae. Genetics 170: 1561-1574 [Abstract] [Full Text]
Kozubowski, L., Larson, J. R., Tatchell, K. (2005). Role of the Septin Ring in the Asymmetric Localization of Proteins at the Mother-Bud Neck in Saccharomyces cerevisiae. Mol. Biol. Cell 16: 3455-3466 [Abstract] [Full Text]
Martin, S. W., Douglas, L. M., Konopka, J. B. (2005). Cell Cycle Dynamics and Quorum Sensing in Candida albicans Chlamydospores Are Distinct from Budding and Hyphal Growth. Eukaryot Cell 4: 1191-1202 [Abstract] [Full Text]
Iwamoto, M. A., Fairclough, S. R., Rudge, S. A., Engebrecht, J. (2005). Saccharomyces cerevisiae Sps1p Regulates Trafficking of Enzymes Required for Spore Wall Synthesis. Eukaryot Cell 4: 536-544 [Abstract] [Full Text]
Gomez-Esquer, F., Rodriguez-Pena, J. M., Diaz, G., Rodriguez, E., Briza, P., Nombela, C., Arroyo, J. (2004). CRR1, a gene encoding a putative transglycosidase, is required for proper spore wall assembly in Saccharomyces cerevisiae. Microbiology 150: 3269-3280 [Abstract] [Full Text]
Martin, S. W., Konopka, J. B. (2004). SUMO Modification of Septin-interacting Proteins in Candida albicans. J. Biol. Chem. 279: 40861-40867 [Abstract] [Full Text]
Shimoda, C. (2004). Forespore membrane assembly in yeast: coordinating SPBs and membrane trafficking. J. Cell Sci. 117: 389-396 [Abstract] [Full Text]
Caviston, J. P., Longtine, M., Pringle, J. R., Bi, E. (2003). The Role of Cdc42p GTPase-activating Proteins in Assembly of the Septin Ring in Yeast. Mol. Biol. Cell 14: 4051-4066 [Abstract] [Full Text]
Warenda, A. J., Kauffman, S., Sherrill, T. P., Becker, J. M., Konopka, J. B. (2003). Candida albicans Septin Mutants Are Defective for Invasive Growth and Virulence. Infect. Immun. 71: 4045-4051 [Abstract] [Full Text]
Casamayor, A., Snyder, M. (2003). Molecular Dissection of a Yeast Septin: Distinct Domains Are Required for Septin Interaction, Localization, and Function. Mol. Cell. Biol. 23: 2762-2777 [Abstract] [Full Text]
Lee, P. R., Song, S., Ro, H.-S., Park, C. J., Lippincott, J., Li, R., Pringle, J. R., De Virgilio, C., Longtine, M. S., Lee, K. S. (2002). Bni5p, a Septin-Interacting Protein, Is Required for Normal Septin Function and Cytokinesis in Saccharomyces cerevisiae. Mol. Cell. Biol. 22: 6906-6920 [Abstract] [Full Text]
Felder, T., Bogengruber, E., Tenreiro, S., Ellinger, A., Sa-Correia, I., Briza, P. (2002). Dtr1p, a Multidrug Resistance Transporter of the Major Facilitator Superfamily, Plays an Essential Role in Spore Wall Maturation in Saccharomyces cerevisiae. Eukaryot Cell 1: 799-810 [Abstract] [Full Text]
Warenda, A. J., Konopka, J. B. (2002). Septin Function in Candida albicans Morphogenesis. Mol. Biol. Cell 13: 2732-2746 [Abstract] [Full Text]
Hohmann, S. (2002). Osmotic Stress Signaling and Osmoadaptation in Yeasts. Microbiol. Mol. Biol. Rev. 66: 300-372 [Abstract] [Full Text]
Peng, X.-R., Jia, Z., Zhang, Y., Ware, J., Trimble, W. S. (2002). The Septin CDCrel-1 Is Dispensable for Normal Development and Neurotransmitter Release. Mol. Cell. Biol. 22: 378-387 [Abstract] [Full Text]
Deng, C., Saunders, W. S. (2001). ADY1, A Novel Gene Required for Prospore Membrane Formation at Selected Spindle Poles in Saccharomyces cerevisiae. Mol. Biol. Cell 12: 2646-2659 [Abstract] [Full Text]
Drees, B. L., Sundin, B., Brazeau, E., Caviston, J. P., Chen, G.-C., Guo, W., Kozminski, K. G., Lau, M. W., Moskow, J. J., Tong, A., Schenkman, L. R., McKenzie, A. III, Brennwald, P., Longtine, M., Bi, E., Chan, C., Novick, P., Boone, C., Pringle, J. R., Davis, T. N., Fields, S., Drubin, D. G. (2001). A protein interaction map for cell polarity development. JCB 154: 549-576 [Abstract] [Full Text]
Cid, V. J., Adamikova, L., Sanchez, M., Molina, M., Nombela, C. (2001). Cell cycle control of septin ring dynamics in the budding yeast. Microbiology 147: 1437-1450 [Abstract] [Full Text]
Watanabe, T., Miyashita, K., Saito, T. T., Yoneki, T., Kakihara, Y., Nabeshima, K., Kishi, Y. A., Shimoda, C., Nojima, H. (2001). Comprehensive isolation of meiosis-specific genes identifies novel proteins and unusual non-coding transcripts in Schizosaccharomyces pombe. Nucleic Acids Res 29: 2327-2337 [Abstract] [Full Text]
Bajgier, B. K., Malzone, M., Nickas, M., Neiman, A. M. (2001). SPO21 Is Required for Meiosis-specific Modification of the Spindle Pole Body in Yeast. Mol. Biol. Cell 12: 1611-1621 [Abstract] [Full Text]
Momany, M., Zhao, J., Lindsey, R., Westfall, P. J. (2001). Characterization of the Aspergillus nidulans Septin (asp) Gene Family. Genetics 157: 969-977 [Abstract] [Full Text]
Song, S., Lee, K. S. (2001). A Novel Function of Saccharomyces cerevisiae CDC5 in Cytokinesis. JCB 152: 451-470 [Abstract] [Full Text]
Kartmann, B, Roth, D (2001). Novel roles for mammalian septins: from vesicle trafficking to oncogenesis. J. Cell Sci. 114: 839-844 [Abstract]
Newman, J. R. S., Wolf, E., Kim, P. S. (2000). From the Cover: A computationally directed screen identifying interacting coiled coils from Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 97: 13203-13208 [Abstract] [Full Text]
Adam, J. C., Pringle, J. R., Peifer, M. (2000). Evidence for Functional Differentiation among Drosophila Septins in Cytokinesis and Cellularization. Mol. Biol. Cell 11: 3123-3135 [Abstract] [Full Text]
Neiman, A. M., Katz, L., Brennwald, P. J. (2000). Identification of Domains Required for Developmentally Regulated SNARE Function in Saccharomyces cerevisiae. Genetics 155: 1643-1655 [Abstract] [Full Text]
Abe, H., Shimoda, C. (2000). Autoregulated Expression of Schizosaccharomyces pombe Meiosis-Specific Transcription Factor Mei4 and a Genome-Wide Search for Its Target Genes. Genetics 154: 1497-1508 [Abstract] [Full Text]
Xue, J., Wang, X., Malladi, C. S., Kinoshita, M., Milburn, P. J., Lengyel, I., Rostas, J. A. P., Robinson, P. J. (2000). Phosphorylation of a New Brain-specific Septin, G-septin, by cGMP-dependent Protein Kinase. J. Biol. Chem. 275: 10047-10056 [Abstract] [Full Text]
Carroll, C. W., Altman, R., Schieltz, D., Yates, J. R. III, Kellogg, D. (1998). The Septins Are Required for the Mitosis-specific Activation of the Gin4 Kinase. JCB 143: 709-717 [Abstract] [Full Text]
Longtine, M. S., Fares, H., Pringle, J. R. (1998). Role of the Yeast Gin4p Protein Kinase in Septin Assembly and the Relationship between Septin Assembly and Septin Function. JCB 143: 719-736 [Abstract] [Full Text]
Frazier, J. A., Wong, M. L., Longtine, M. S., Pringle, J. R., Mann, M., Mitchison, T. J., Field, C. (1998). Polymerization of Purified Yeast Septins: Evidence That Organized Filament Arrays May Not Be Required for Septin Function. JCB 143: 737-749 [Abstract] [Full Text]
Neiman, A. M. (1998). Prospore Membrane Formation Defines a Developmentally Regulated Branch of the Secretory Pathway in Yeast. JCB 140: 29-37 [Abstract] [Full Text]
Rudge, S. A., Morris, A. J., Engebrecht, J. (1998). Relocalization of Phospholipase D Activity Mediates Membrane Formation During Meiosis. JCB 140: 81-90 [Abstract] [Full Text]
Inoue, S, Turgeon, B., Yoder, O., Aist, J. (1998). Role of fungal dynein in hyphal growth, microtubule organization, spindle pole body motility and nuclear migration. J. Cell Sci. 111: 1555-1566 [Abstract]
DeMarini, D. J., Adams, A. E.M., Fares, H., Virgilio, C. D., Valle, G., Chuang, J. S., Pringle, J. R. (1997). A Septin-based Hierarchy of Proteins Required for Localized Deposition of Chitin in the Saccharomyces cerevisiae Cell Wall. JCB 139: 75-93 [Abstract] [Full Text]
Kinoshita, M, Kumar, S, Mizoguchi, A, Ide, C, Kinoshita, A, Haraguchi, T, Hiraoka, Y, Noda, M (1997). Nedd5, a mammalian septin, is a novel cytoskeletal component interacting with actin-based structures.. Genes Dev. 11: 1535-1547 [Abstract]
Tachikawa, H., Bloecher, A., Tatchell, K., Neiman, A. M. (2001). A Gip1p-Glc7p phosphatase complex regulates septin organization and spore wall formation. JCB 155: 797-808 [Abstract] [Full Text]
Westfall, P. J., Momany, M. (2002). Aspergillus nidulans Septin AspB Plays Pre- and Postmitotic Roles in Septum, Branch, and Conidiophore Development. Mol. Biol. Cell 13: 110-118 [Abstract] [Full Text]