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. 2001 Feb;157(2):601–610. doi: 10.1093/genetics/157.2.601

Cell polarity and hyphal morphogenesis are controlled by multiple rho-protein modules in the filamentous ascomycete Ashbya gossypii.

J Wendland 1, P Philippsen 1
PMCID: PMC1461536  PMID: 11156982

Abstract

Polarized cell growth requires a polarized organization of the actin cytoskeleton. Small GTP-binding proteins of the Rho-family have been shown to be involved in the regulation of actin polarization as well as other processes. Hyphal growth in filamentous fungi represents an ideal model to investigate mechanisms involved in generating cell polarity and establishing polarized cell growth. Since a potential role of Rho-proteins has not been studied so far in filamentous fungi we isolated and characterized the Ashbya gossypii homologs of the Saccharomyces cerevisiae CDC42, CDC24, RHO1, and RHO3 genes. The AgCDC42 and AgCDC24 genes can both complement conditional mutations in the S. cerevisiae CDC42 and CDC24 genes and both proteins are required for the establishment of actin polarization in A. gossypii germ cells. Agrho1 mutants show a cell lysis phenotype. Null mutant strains of Agrho3 show periodic swelling of hyphal tips that is overcome by repolarization and polar hyphal growth in a manner resembling the germination pattern of spores. Thus different Rho-protein modules are required for distinct steps during polarized hyphal growth of A. gossypii.

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Selected References

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  1. Adamo J. E., Rossi G., Brennwald P. The Rho GTPase Rho3 has a direct role in exocytosis that is distinct from its role in actin polarity. Mol Biol Cell. 1999 Dec;10(12):4121–4133. doi: 10.1091/mbc.10.12.4121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Adams A. E., Johnson D. I., Longnecker R. M., Sloat B. F., Pringle J. R. CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J Cell Biol. 1990 Jul;111(1):131–142. doi: 10.1083/jcb.111.1.131. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  4. Becker D. M., Guarente L. High-efficiency transformation of yeast by electroporation. Methods Enzymol. 1991;194:182–187. doi: 10.1016/0076-6879(91)94015-5. [DOI] [PubMed] [Google Scholar]
  5. Boguski M. S., McCormick F. Proteins regulating Ras and its relatives. Nature. 1993 Dec 16;366(6456):643–654. doi: 10.1038/366643a0. [DOI] [PubMed] [Google Scholar]
  6. Cabib E., Drgonová J., Drgon T. Role of small G proteins in yeast cell polarization and wall biosynthesis. Annu Rev Biochem. 1998;67:307–333. doi: 10.1146/annurev.biochem.67.1.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eby J. J., Holly S. P., van Drogen F., Grishin A. V., Peter M., Drubin D. G., Blumer K. J. Actin cytoskeleton organization regulated by the PAK family of protein kinases. Curr Biol. 1998 Aug 27;8(17):967–970. doi: 10.1016/s0960-9822(98)00398-4. [DOI] [PubMed] [Google Scholar]
  8. Hall A. Rho GTPases and the actin cytoskeleton. Science. 1998 Jan 23;279(5350):509–514. doi: 10.1126/science.279.5350.509. [DOI] [PubMed] [Google Scholar]
  9. Harris S. D., Hofmann A. F., Tedford H. W., Lee M. P. Identification and characterization of genes required for hyphal morphogenesis in the filamentous fungus Aspergillus nidulans. Genetics. 1999 Mar;151(3):1015–1025. doi: 10.1093/genetics/151.3.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Harris S. D. The duplication cycle in Aspergillus nidulans. Fungal Genet Biol. 1997 Aug;22(1):1–12. doi: 10.1006/fgbi.1997.0990. [DOI] [PubMed] [Google Scholar]
  11. Imai J., Toh-e A., Matsui Y. Genetic analysis of the Saccharomyces cerevisiae RHO3 gene, encoding a rho-type small GTPase, provides evidence for a role in bud formation. Genetics. 1996 Feb;142(2):359–369. doi: 10.1093/genetics/142.2.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kaminskyj S. G., Hamer J. E. hyp loci control cell pattern formation in the vegetative mycelium of Aspergillus nidulans. Genetics. 1998 Feb;148(2):669–680. doi: 10.1093/genetics/148.2.669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kron S. J., Gow N. A. Budding yeast morphogenesis: signalling, cytoskeleton and cell cycle. Curr Opin Cell Biol. 1995 Dec;7(6):845–855. doi: 10.1016/0955-0674(95)80069-7. [DOI] [PubMed] [Google Scholar]
  14. Lew D. J., Reed S. I. Morphogenesis in the yeast cell cycle: regulation by Cdc28 and cyclins. J Cell Biol. 1993 Mar;120(6):1305–1320. doi: 10.1083/jcb.120.6.1305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Maeting I., Schmidt G., Sahm H., Revuelta J. L., Stierhof Y. D., Stahmann K. P. Isocitrate lyase of Ashbya gossypii--transcriptional regulation and peroxisomal localization. FEBS Lett. 1999 Feb 5;444(1):15–21. doi: 10.1016/s0014-5793(99)00017-4. [DOI] [PubMed] [Google Scholar]
  16. Matsui Y., Toh-E A. Yeast RHO3 and RHO4 ras superfamily genes are necessary for bud growth, and their defect is suppressed by a high dose of bud formation genes CDC42 and BEM1. Mol Cell Biol. 1992 Dec;12(12):5690–5699. doi: 10.1128/mcb.12.12.5690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Momany M., Westfall P. J., Abramowsky G. Aspergillus nidulans swo mutants show defects in polarity establishment, polarity maintenance and hyphal morphogenesis. Genetics. 1999 Feb;151(2):557–567. doi: 10.1093/genetics/151.2.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Nern A., Arkowitz R. A. Nucleocytoplasmic shuttling of the Cdc42p exchange factor Cdc24p. J Cell Biol. 2000 Mar 20;148(6):1115–1122. doi: 10.1083/jcb.148.6.1115. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pruyne D., Bretscher A. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states. J Cell Sci. 2000 Feb;113(Pt 3):365–375. doi: 10.1242/jcs.113.3.365. [DOI] [PubMed] [Google Scholar]
  20. Ramírez-Ramírez N., García-Soto J., González-Hernández A., Martínez-Cadena G. The small GTP-binding protein Rho is expressed differentially during spore germination of Phycomyces blakesleeanus. Microbiology. 1999 May;145(Pt 5):1097–1104. doi: 10.1099/13500872-145-5-1097. [DOI] [PubMed] [Google Scholar]
  21. Shimada Y., Gulli M. P., Peter M. Nuclear sequestration of the exchange factor Cdc24 by Far1 regulates cell polarity during yeast mating. Nat Cell Biol. 2000 Feb;2(2):117–124. doi: 10.1038/35000073. [DOI] [PubMed] [Google Scholar]
  22. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sloat B. F., Adams A., Pringle J. R. Roles of the CDC24 gene product in cellular morphogenesis during the Saccharomyces cerevisiae cell cycle. J Cell Biol. 1981 Jun;89(3):395–405. doi: 10.1083/jcb.89.3.395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Som T., Kolaparthi V. S. Developmental decisions in Aspergillus nidulans are modulated by Ras activity. Mol Cell Biol. 1994 Aug;14(8):5333–5348. doi: 10.1128/mcb.14.8.5333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Steiner S., Wendland J., Wright M. C., Philippsen P. Homologous recombination as the main mechanism for DNA integration and cause of rearrangements in the filamentous ascomycete Ashbya gossypii. Genetics. 1995 Jul;140(3):973–987. doi: 10.1093/genetics/140.3.973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Symons M. Rho family GTPases: the cytoskeleton and beyond. Trends Biochem Sci. 1996 May;21(5):178–181. [PubMed] [Google Scholar]
  27. Tanaka K., Takai Y. Control of reorganization of the actin cytoskeleton by Rho family small GTP-binding proteins in yeast. Curr Opin Cell Biol. 1998 Feb;10(1):112–116. doi: 10.1016/s0955-0674(98)80093-8. [DOI] [PubMed] [Google Scholar]
  28. Tatsumoto T., Xie X., Blumenthal R., Okamoto I., Miki T. Human ECT2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis. J Cell Biol. 1999 Nov 29;147(5):921–928. doi: 10.1083/jcb.147.5.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Toenjes K. A., Sawyer M. M., Johnson D. I. The guanine-nucleotide-exchange factor Cdc24p is targeted to the nucleus and polarized growth sites. Curr Biol. 1999 Oct 21;9(20):1183–1186. doi: 10.1016/S0960-9822(00)80022-6. [DOI] [PubMed] [Google Scholar]
  30. Torralba S., Raudaskoski M., Pedregosa A. M., Laborda F. Effect of cytochalasin A on apical growth, actin cytoskeleton organization and enzyme secretion in Aspergillus nidulans. Microbiology. 1998 Jan;144(Pt 1):45–53. doi: 10.1099/00221287-144-1-45. [DOI] [PubMed] [Google Scholar]
  31. Wendland J., Ayad-Durieux Y., Knechtle P., Rebischung C., Philippsen P. PCR-based gene targeting in the filamentous fungus Ashbya gossypii. Gene. 2000 Jan 25;242(1-2):381–391. doi: 10.1016/s0378-1119(99)00509-0. [DOI] [PubMed] [Google Scholar]
  32. Wendland J., Philippsen P. Determination of cell polarity in germinated spores and hyphal tips of the filamentous ascomycete Ashbya gossypii requires a rhoGAP homolog. J Cell Sci. 2000 May;113(Pt 9):1611–1621. doi: 10.1242/jcs.113.9.1611. [DOI] [PubMed] [Google Scholar]
  33. Wendland J., Pöhlmann R., Dietrich F., Steiner S., Mohr C., Philippsen P. Compact organization of rRNA genes in the filamentous fungus Ashbya gossypii. Curr Genet. 1999 Jul;35(6):618–625. doi: 10.1007/s002940050460. [DOI] [PubMed] [Google Scholar]

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