A mutation in the Rho1-GAP-encoding gene BEM2 of Saccharomyces cerevisiae affects morphogenesis and cell wall functionality
Abstract
Summary: Saccharomyces cerevisiae strain V918 was previously isolated in a search for thermosensitive autolytic mutants and found to bear a recessive mutation that caused the development of multinucleate swollen cells undergoing cell lysis. The BEM2 gene has been isolated by complementation of the phenotype of a V918 segregant. BEM2 encodes a Rho-GTPase-activating protein (GAP) which is thought to act as a modulator of the Rho1 small GTPase. It is shown that the mutation causing the morphogenetic and autolytic phenotype in strain V918 and its segregants lies in the BEM2 gene, defining a new mutant allele, bem2-21. Mutants in the BEM2 gene have been reported to display loss of cell polarity and depolarization of the actin cytoskeleton, causing a bud-emergence defect. Low resistance to sonication and to hydrolytic enzymes proved that the cell wall is less protective in bem2-21 mutants than in wild-type strains. Moreover, bem2-21 mutants are more sensitive than the wild-type to several antifungal drugs. Transmission electron microscopy revealed the development of abnormally thick and wide septa and the existence of thin areas in the cell wall which probably account for cell lysis. The depolarization of actin in bem2-21 mutants did not preclude morphogenetic events such as cell elongation in homozygous diploid strains during nitrogen starvation in solid media, hyperpolarization of growth in a background bearing a mutated septin, or sporulation. Multinucleate cells from bem2-21 homozygous diploids underwent sporulation giving rise to multispored asci (‘polyads’), containing up to 36 spores. This phenomenon occurred only under osmotically stabilized conditions, suggesting that the integrity of the ascus wall is impaired in cells expressing the bem2-21 mutation. It is concluded that the function of the BEM2 gene product is essential for the maintenance of a functional cell wall.
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Bem2 in S. cerevisiae acts as a GAP for Rho1 and is implicated in antifungal sensitivity, actin cytoskeleton organization, and bud emergence.
“Bem2 in S. cerevisiae acts as a GAP for Rho1 and is implicated in antifungal sensitivity (assumed to be due to increased permeability of the cell surface), actin cytoskeleton organization, and bud emergence (35,36).”
From The Rho1 GTPase-activating protein CgBem2 is required for survival of azole stress in Candida glabrata (2011) · cites this paper as [35]
Cites
Molecular cloning: A laboratory manual
Deininger, P. L. (1990) · Analytical Biochemistry · doi:10.1016/0003-2697(90)90595-z · Cited by 84,684 · see citing works
Sikorski, R. S., & Hieter, P. (1989) · Genetics · doi:10.1093/genetics/122.1.19 · Cited by 8,685 · see citing works
Current Protocols in Molecular Biology
(2018) · Current Protocols in Molecular Biology · doi:10.1002/(issn)1934-3647 · Cited by 1,395 · see citing works
Gimeno, C. J., Ljungdahl, P. O., Styles, C. A., & Fink, G. R. (1992) · Cell · doi:10.1016/0092-8674(92)90079-r · Cited by 1,184 · see citing works
Adams, A. E., & Pringle, J. R. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.98.3.934 · Cited by 834 · see citing works
HARTWELL, L. (1971) · Experimental Cell Research · doi:10.1016/0014-4827(71)90223-0 · Cited by 650 · see citing works
Adams, A. E., Johnson, D. I., Longnecker, R., Sloat, B. F., & Pringle, J. R. (1990) · The Journal of Cell Biology · doi:10.1083/jcb.111.1.131 · Cited by 603 · see citing works
Review: Cell wall assembly in yeast
Klis, F. M. (1994) · Yeast · doi:10.1002/yea.320100702 · Cited by 552 · see citing works
The septins: roles in cytokinesis and other processes
Longtine, M. S., DeMarini, D. J., Valencik, M. L., et al. (1996) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(96)80054-8 · Cited by 509 · see citing works
Johnston, G. C., Prendergast, J. A., & Singer, R. A. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.113.3.539 · Cited by 477 · see citing works
Molecular basis of cell integrity and morphogenesis in Saccharomyces cerevisiae
Cid, V. J., Durán, A., del Rey, F., Snyder, M. P., Nombela, C., & Sánchez, M. (1995) · Microbiological Reviews · doi:10.1128/mr.59.3.345-386.1995 · Cited by 464 · see citing works
Self-citationIdentification of Yeast Rho1p GTPase as a Regulatory Subunit of 1,3-β-Glucan Synthase
Qadota, H., Python, C. P., Inoue, S., Arisawa, M., Anraku, Y., Zheng, Y., Watanabe, T., Levin, D. E., & Ohya, Y. (1996) · Science · doi:10.1126/science.272.5259.279 · Cited by 445 · see citing works
Bender, A., & Pringle, J. R. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.3.1295 · Cited by 433 · see citing works
A Yeast Mitogen-Activated Protein Kinase Homolog (Mpk1p) Mediates Signalling by Protein Kinase C
Lee, K. S., Irie, K., Gotoh, Y., Watanabe, Y., Araki, H., Nishida, E., Matsumoto, K., & Levin, D. E. (1993) · Molecular and Cellular Biology · doi:10.1128/mcb.13.5.3067 · Cited by 377 · see citing works
Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane.
Mulholland, J., Preuss, D., Moon, A., Wong, A. M., Drubin, D. G., & Botstein, D. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.125.2.381 · Cited by 358 · see citing works
Nonaka, H., Tanaka, K., Hirano, H., Fujiwara, T., Kohno, H., Umikawa, M., Mino, A., & Takai, Y. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb00281.x · Cited by 341 · see citing works
Rho1p, a Yeast Protein at the Interface Between Cell Polarization and Morphogenesis
Drgonová, J., Drgon, T., Tanaka, K., KOLLÁR, R., Chen, G.-C., Ford, R. A., Chan, C. S. M., Takai, Y., & Cabib, E. (1996) · Science · doi:10.1126/science.272.5259.277 · Cited by 336 · see citing works
Isolation and characterization of chromosome-gain and increase-in-ploidy mutants in yeast.
Chan, C. S. M., & Botstein, D. (1993) · Genetics · doi:10.1093/genetics/135.3.677 · Cited by 310 · see citing works
Schmidt, A., Bickle, M., Beck, T. W., & Hall, M. N. (1997) · Cell · doi:10.1016/s0092-8674(00)81893-0 · Cited by 300 · see citing works
Tunicamycin — An inhibitor of yeast glycoprotein synthesis
Kuo, S. ‐., & Lampen, J. O. (1974) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(74)90925-5 · Cited by 292 · see citing works
Healy, A. M., Zołnierowicz, S., Stapleton, A. E., Goebl, M. G., DePaoli-Roach, A. A., & Pringle, J. R. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.11.5767-5780.1991 · Cited by 284 · see citing works
Kohno, H., Tanaka, K., Mino, A., et al. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00994.x · Cited by 282 · see citing works
Zheng, Y., Cerione, R. A., & Bender, A. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)41953-3 · Cited by 280 · see citing works
Bénédetti, H., Raths, S., Crausaz, F., & Riezman, H. (1994) · Molecular Biology of the Cell · doi:10.1091/mbc.5.9.1023 · Cited by 262 · see citing works
Characterization of two members of the rho gene family from the yeast Saccharomyces cerevisiae.
Madaule, P., Axel, R., & Myers, A. M. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.3.779 · Cited by 258 · see citing works
Sloat, B. F., Adams, A., & Pringle, J. R. (1981) · The Journal of Cell Biology · doi:10.1083/jcb.89.3.395 · Cited by 253 · see citing works
Yamochi, W., Tanaka, K., Nonaka, H., Maeda, A., Musha, T., & Takai, Y. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.125.5.1077 · Cited by 242 · see citing works
The SLT2(MPK1) MAP kinase is activated during periods of polarized cell growth in yeast.
Zarzov, P., Mazzoni, C., & Mann, C. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00336.x · Cited by 238 · see citing works
The osmotic integrity of the yeast cell requires a functional PKC1 gene product.
Paravicini, G., Cooper, M., Friedli, L., Smith, D. J., Carpentier, J. L., Klig, L. S., & Payton, M. A. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.11.4896 · Cited by 222 · see citing works
Elledge, S. J., & Davis, R. W. (1988) · Gene · doi:10.1016/0378-1119(88)90202-8 · Cited by 222 · see citing works
Ozaki, K., Tanaka, K., Imamura, H., Hihara, T., Kameyama, T., Nonaka, H., Hirano, H., Matsuura, Y., & Takai, Y. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00573.x · Cited by 209 · see citing works
Interactions between the bud emergence proteins Bem1p and Bem2p and Rho-type GTPases in yeast.
Peterson, J., Zheng, Y., Bender, L., Myers, A., Cerione, R., & Bender, A. (1994) · The Journal of cell biology · doi:10.1083/jcb.127.5.1395 · Cited by 197 · see citing works
A protein kinase gene complements the lytic phenotype of Saccharomyces cerevisiae lyt2 mutants
Torres, L., Martı́n, H., García-Sáez, M. I., Arroyo, J., Molina, M., Sánchez, M., & Nombela, C. (1991) · Molecular Microbiology · doi:10.1111/j.1365-2958.1991.tb01993.x · Cited by 191 · see citing works
Self-citationRho-related proteins: actin cytoskeleton and cell cycle
Ridley, A. J. (1995) · Current Opinion in Genetics & Development · doi:10.1016/s0959-437x(95)90049-7 · Cited by 174 · see citing works
Liu, H., & Bretscher, A. P. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.118.2.285 · Cited by 157 · see citing works
Activity of the yeast MAP kinase homologue Slt2 is critically required for cell integrity at 37° C
Martı́n, H., Arroyo, J., Sánchez, M., Molina, M., & Nombela, C. (1993) · Molecular and General Genetics MGG · doi:10.1007/bf00280215 · Cited by 148 · see citing works
Self-citationStevenson, B. J., Ferguson, B., Virgilio, C. D., Bi, E., Pringle, J. R., Ammerer, G., & Sprague, G. F. (1995) · Genes & Development · doi:10.1101/gad.9.23.2949 · Cited by 130 · see citing works
A Saccharomyces cerevisiae mutant with echinocandin-resistant 1,3-beta-D-glucan synthase
Douglas, C. M., Marrinan, J. A., Li, W., & Kurtz, M. (1994) · Journal of Bacteriology · doi:10.1128/jb.176.18.5686-5696.1994 · Cited by 129 · see citing works
Vanadate-resistant yeast mutants are defective in protein glycosylation.
Ballou, L., Hitzeman, R. A., Lewis, M. S., & Ballou, C. E. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.8.3209 · Cited by 125 · see citing works
Donnelly, S. F. H., Pocklington, M. J., Pallotta, D. J., et al. (1993) · Molecular Microbiology · doi:10.1111/j.1365-2958.1993.tb00930.x · Cited by 93 · see citing works
Molecular cloning and characterization of yeast rho GDP dissociation inhibitor.
Masuda, T., Tanaka, K., Nonaka, H., et al. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)32079-3 · Cited by 85 · see citing works
Kim, Y., Francisco, L., Chen, G. C., Marcotte, E. M., & Chan, C. S. M. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.127.5.1381 · Cited by 84 · see citing works
Castro, C., Ribas, J. C., Valdivieso, M. ‐., Varona, R., del Rey, F., & Duran, A. (1995) · Journal of Bacteriology · doi:10.1128/jb.177.20.5732-5739.1995 · Cited by 67 · see citing works
The rho-GAP encoded by BEM2 regulates cytoskeletal structure in budding yeast.
Wang, T., & Bretscher, A. (1995) · Molecular Biology of the Cell · doi:10.1091/mbc.6.8.1011 · Cited by 64 · see citing works
Simple and sensitive procedure for screening yeast mutants that lyse at nonpermissive temperatures
Cabib, E., & Duran, A. (1975) · Journal of Bacteriology · doi:10.1128/jb.124.3.1604-1606.1975 · Cited by 57 · see citing works
Disruption of the actin cytoskeleton in budding yeast results in formation of an aberrant cell wall
Gabriel, M., & Kopecká, M. (1995) · Microbiology · doi:10.1099/13500872-141-4-891 · Cited by 51 · see citing works
Chen, G.-C., Li, Z., & Chan, C. S. M. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.4.1376 · Cited by 37 · see citing works
Liu, H., & Bretscher, A. P. (1992) · Trends in Cell Biology · doi:10.1016/0962-8924(92)90112-z · Cited by 27 · see citing works
Polyamines and cell wall organization in Saccharomyces cerevisiae
Miret, J. J., Solari, A. J., Barderi, P. A., & Goldemberg, S. H. (1992) · Yeast · doi:10.1002/yea.320081206 · Cited by 21 · see citing works
Characterization of thermosensitive autolytic mutants from diploid Saccharomyces cerevisiae
Cid, V. J., Sanchez, M., & Nombela, C. (1994) · Microbiology · doi:10.1099/00221287-140-3-559 · Cited by 11 · see citing works
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Levin, D. E. (2005) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.69.2.262-291.2005 · Cited by 1,136 · see citing works
Transcription Profiling of <i>Candida albicans</i> Cells Undergoing the Yeast-to-Hyphal Transition
Nantel, A., Dignard, D., Bachewich, C., Harcus, D., Marcil, A., Bouin, A.-P., Sensen, C. W., Hogues, H., van het Hoog, M., Gordon, P., et al. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-05-0272 · Cited by 378 · see citing works
Rho GTPases: regulation of cell polarity and growth in yeasts
Perez, P., & Rincón, S. A. (2010) · Biochemical Journal · doi:10.1042/bj20091823 · Cited by 162 · see citing works
Borah, S., Shivarathri, R., & Kaur, R. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.264671 · Cited by 44 · see citing works
- Authors
- Cid, V. J., Cenamor, R., Sánchez, M., & Nombela, C.
- Affiliations
- Departamento de Microbiología II, Facultad de Farmacia, Universidad Complutense de Madrid, 28040 Madrid, Spain
- Universidad Complutense de Madrid (ES)
- Corresponding author
- Sánchez, Miguel
- ORCID
- Nombela, César
- Venue
- Microbiology
- Publisher
- Microbiology Society
- Published
- 1998-01-01
- Volume
- 144
- Issue
- 1
- Pages
- 25-36
- ISSN
- 1350-0872 (ISSN-L)
- 1465-2080
- OpenAlex
- W2152106868
- Cited by
- 39
- References
- 50
- Citations by year
- 2025: 1 · 2022: 2 · 2021: 1 · 2017: 1 · 2016: 1 · 2014: 1 · 2013: 1 · 2012: 1
- FWCI
- 1.40
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Microbiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministerio de Economía y Competitividad
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Keywords
- RhoGAP, Saccharomyces cerevisiae, cell morphogenesis, cell wall integrity, cell lysis, multinucleated cells, cell polarity, bud emergence, septa, antifungal susceptibility, polyads, sporulation, nitrogen starvation, osmotic stress
- MeSH terms
- Alleles, Antifungal Agents, Cell Wall, Fungal Proteins, Genetic Complementation Test, Microbial Sensitivity Tests, Microscopy, Electron, Morphogenesis, Mutation, Proteins, Saccharomyces cerevisiae, Protein Biosynthesis, GTPase-Activating Proteins, Saccharomyces cerevisiae Proteins
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