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PMID: 16757736 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Functional characterization of Aspergillus nidulans homologues of Saccharomyces cerevisiae Spa2 and Bud6.

Eukaryotic cell ·Vol. 5 ·No. 6 ·2006-06-00 ·Pages 881-95

Virag A, Harris SD

Abstract

The importance of polarized growth for fungi has elicited significant effort directed at better understanding underlying mechanisms of polarization, with a focus on yeast systems. At sites of tip growth, multiple protein complexes assemble and coordinate to ensure that incoming building material reaches the appropriate destination sites, and polarized growth is maintained. One of these complexes is the polarisome that consists of Spa2, Bud6, Pea2, and Bni1 in Saccharomyces cerevisiae. Filamentous hyphae differ in their development and life style from yeasts and likely regulate polarized growth in a different way. This is expected to reflect on the composition and presence of protein complexes that assemble at the hyphal tip. In this study we searched for polarisome homologues in the model filamentous fungus Aspergillus nidulans and characterized the S. cerevisiae Spa2 and Bud6 homologues, SpaA and BudA. Compared to the S. cerevisiae Spa2, SpaA lacks domain II but has three additional domains that are conserved within filamentous fungi. Gene replacement strains and localization studies show that SpaA functions exclusively at the hyphal tip, while BudA functions at sites of septum formation and possibly at hyphal tips. We show that SpaA is not required for the assembly or maintenance of the Spitzenkörper. We propose that the core function of the polarisome in polarized growth is maintained but with different contributions of polarisome components to the process.

MeSH Terms
Amino Acid Sequence Aspergillus nidulans/chemistry,genetics,growth & development Conserved Sequence Cytoskeletal Proteins Fungal Proteins/chemistry,physiology Genes, Fungal Hyphae/chemistry,growth & development Microfilament Proteins/chemistry Molecular Sequence Data Monomeric GTP-Binding Proteins/chemistry Saccharomyces cerevisiae Proteins/chemistry
Chemicals
BUD6 protein, S cerevisiae Cytoskeletal Proteins Fungal Proteins Microfilament Proteins SPA2 protein, S cerevisiae Saccharomyces cerevisiae Proteins Monomeric GTP-Binding Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Virag Aleksandra
Plant Science Initiative, and Department of Plant Pathology, University of Nebraska, Lincoln, NE 68588-0660, USA.
Harris Steven D
References (60)
60 references, click to expand
  1. Dominant active Rac and dominant negative Rac revert the dominant active Ras phenotype in Colletotrichum trifolii by distinct signalling pathways.
    Mol Microbiol. 2004 Mar;51(5):1493-507 PMID: 14982641
  2. Aspergillus nidulans septin AspB plays pre- and postmitotic roles in septum, branch, and conidiophore development.
    Mol Biol Cell. 2002 Jan;13(1):110-8 PMID: 11809826
  3. Establishment of mRFP1 as a fluorescent marker in Aspergillus nidulans and construction of expression vectors for high-throughput protein tagging using recombination in vitro (GATEWAY).
    Curr Genet. 2004 Jun;45(6):383-9 PMID: 15071756
  4. CD-Search: protein domain annotations on the fly.
    Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W327-31 PMID: 15215404
  5. The distinct morphogenic states of Candida albicans.
    Trends Microbiol. 2004 Jul;12(7):317-24 PMID: 15223059
  6. MesA, a novel fungal protein required for the stabilization of polarity axes in Aspergillus nidulans.
    Mol Biol Cell. 2004 Aug;15(8):3658-72 PMID: 15155805
  7. Rapid production of gene replacement constructs and generation of a green fluorescent protein-tagged centromeric marker in Aspergillus nidulans.
    Eukaryot Cell. 2004 Oct;3(5):1359-62 PMID: 15470263
  8. Mitotic mutants of Aspergillus nidulans.
    Genet Res. 1975 Dec;26(3):237-54 PMID: 773766
  9. Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations.
    Adv Genet. 1977;19:33-131 PMID: 327767
  10. The SPA2 protein of yeast localizes to sites of cell growth.
    J Cell Biol. 1989 Apr;108(4):1419-29 PMID: 2647769
  11. Characterization of an inducible expression system in Aspergillus nidulans using alcA and tubulin-coding genes.
    Gene. 1989 Jun 30;79(1):119-30 PMID: 2673931
  12. The SPA2 gene of Saccharomyces cerevisiae is important for pheromone-induced morphogenesis and efficient mating.
    J Cell Biol. 1990 Oct;111(4):1451-64 PMID: 2211820
  13. Identification and characterization of Aspergillus nidulans mutants defective in cytokinesis.
    Genetics. 1994 Feb;136(2):517-32 PMID: 8150280
  14. Genetic analysis of the bipolar pattern of bud site selection in the yeast Saccharomyces cerevisiae.
    Mol Cell Biol. 1996 Apr;16(4):1857-70 PMID: 8657162
  15. Pea2 protein of yeast is localized to sites of polarized growth and is required for efficient mating and bipolar budding.
    J Cell Biol. 1996 Nov;135(3):725-39 PMID: 8909546
  16. Bni1p implicated in cytoskeletal control is a putative target of Rho1p small GTP binding protein in Saccharomyces cerevisiae.
    EMBO J. 1996 Nov 15;15(22):6060-8 PMID: 8947028
  17. Bni1p, a yeast formin linking cdc42p and the actin cytoskeleton during polarized morphogenesis.
    Science. 1997 Apr 4;276(5309):118-22 PMID: 9082982
  18. Bni1p and Bnr1p: downstream targets of the Rho family small G-proteins which interact with profilin and regulate actin cytoskeleton in Saccharomyces cerevisiae.
    EMBO J. 1997 May 15;16(10):2745-55 PMID: 9184220
  19. The Aspergillus nidulans sepA gene encodes an FH1/2 protein involved in cytokinesis and the maintenance of cellular polarity.
    EMBO J. 1997 Jun 16;16(12):3474-83 PMID: 9218790
  20. Aip3p/Bud6p, a yeast actin-interacting protein that is involved in morphogenesis and the selection of bipolar budding sites.
    Mol Biol Cell. 1997 Apr;8(4):729-53 PMID: 9247651
  21. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  22. The duplication cycle in Aspergillus nidulans.
    Fungal Genet Biol. 1997 Aug;22(1):1-12 PMID: 9344627
  23. The Spa2-related protein, Sph1p, is important for polarized growth in yeast.
    J Cell Sci. 1998 Feb;111 ( Pt 4):479-94 PMID: 9443897
  24. Plant-adapted green fluorescent protein is a versatile vital reporter for gene expression, protein localization and mitosis in the filamentous fungus, Aspergillus nidulans.
    Mol Microbiol. 1998 Jan;27(1):121-30 PMID: 9466261
  25. FH3, a domain found in formins, targets the fission yeast formin Fus1 to the projection tip during conjugation.
    J Cell Biol. 1998 Jun 1;141(5):1217-28 PMID: 9606213
  26. Spa2p interacts with cell polarity proteins and signaling components involved in yeast cell morphogenesis.
    Mol Cell Biol. 1998 Jul;18(7):4053-69 PMID: 9632790
  27. CDD: a Conserved Domain Database for protein classification.
    Nucleic Acids Res. 2005 Jan 1;33(Database issue):D192-6 PMID: 15608175
  28. Functional characterization and localization of the Aspergillus nidulans formin SEPA.
    Mol Biol Cell. 2002 Feb;13(2):469-79 PMID: 11854405
  29. An actin nucleation mechanism mediated by Bni1 and profilin.
    Nat Cell Biol. 2002 Aug;4(8):626-31 PMID: 12134165
  30. Subcellular localization of Axl1, the cell type-specific regulator of polarity.
    Curr Biol. 2002 Aug 6;12(15):1347-52 PMID: 12176366
  31. Spa2p functions as a scaffold-like protein to recruit the Mpk1p MAP kinase module to sites of polarized growth.
    Curr Biol. 2002 Oct 1;12(19):1698-703 PMID: 12361575
  32. Control of morphogenesis and actin localization by the Penicillium marneffei RAC homolog.
    J Cell Sci. 2003 Apr 1;116(Pt 7):1249-60 PMID: 12615967
  33. Roles of NUDE and NUDF proteins of Aspergillus nidulans: insights from intracellular localization and overexpression effects.
    Mol Biol Cell. 2003 Mar;14(3):871-88 PMID: 12631710
  34. Formins: signaling effectors for assembly and polarization of actin filaments.
    J Cell Sci. 2003 Jul 1;116(Pt 13):2603-11 PMID: 12775772
  35. Different roles of the Mre11 complex in the DNA damage response in Aspergillus nidulans.
    Mol Microbiol. 2003 Jun;48(6):1693-709 PMID: 12791148
  36. Formin-dependent actin assembly is regulated by distinct modes of Rho signaling in yeast.
    J Cell Biol. 2003 Jun 23;161(6):1081-92 PMID: 12810699
  37. TINA interacts with the NIMA kinase in Aspergillus nidulans and negatively regulates astral microtubules during metaphase arrest.
    Mol Biol Cell. 2003 Aug;14(8):3169-79 PMID: 12925754
  38. CaSPA2 is important for polarity establishment and maintenance in Candida albicans.
    Mol Microbiol. 2003 Sep;49(5):1391-405 PMID: 12940995
  39. Maximal polar growth potential depends on the polarisome component AgSpa2 in the filamentous fungus Ashbya gossypii.
    Mol Biol Cell. 2003 Oct;14(10):4140-54 PMID: 12937275
  40. Aspergillus nidulans RhoA is involved in polar growth, branching, and cell wall synthesis.
    Fungal Genet Biol. 2004 Jan;41(1):13-22 PMID: 14643255
  41. A conserved mechanism for Bni1- and mDia1-induced actin assembly and dual regulation of Bni1 by Bud6 and profilin.
    Mol Biol Cell. 2004 Feb;15(2):896-907 PMID: 14657240
  42. Rax1, a protein required for the establishment of the bipolar budding pattern in yeast.
    Gene. 2004 Mar 3;327(2):161-9 PMID: 14980713
  43. Candida albicans hyphae have a Spitzenkörper that is distinct from the polarisome found in yeast and pseudohyphae.
    J Cell Sci. 2005 Jul 1;118(Pt 13):2935-47 PMID: 15976451
  44. Differential activities and regulation of Saccharomyces cerevisiae formin proteins Bni1 and Bnr1 by Bud6.
    J Biol Chem. 2005 Jul 29;280(30):28023-33 PMID: 15923184
  45. Cell polarity protein Spa2P associates with proteins involved in actin function in Saccharomyces cerevisiae.
    Mol Biol Cell. 2005 Oct;16(10):4595-608 PMID: 16030260
  46. Tracing the endocytic pathway of Aspergillus nidulans with FM4-64.
    Fungal Genet Biol. 2005 Dec;42(12):963-75 PMID: 16291501
  47. The Spitzenkörper: a molecular perspective.
    Mycol Res. 2006 Jan;110(Pt 1):4-13 PMID: 16378719
  48. A versatile and efficient gene-targeting system for Aspergillus nidulans.
    Genetics. 2006 Mar;172(3):1557-66 PMID: 16387870
  49. The multifunctional GIT family of proteins.
    J Cell Sci. 2006 Apr 15;119(Pt 8):1469-75 PMID: 16598076
  50. Polarization of cell growth in yeast. I. Establishment and maintenance of polarity states.
    J Cell Sci. 2000 Feb;113 ( Pt 3):365-75 PMID: 10639324
  51. Polarisome meets spitzenkörper: microscopy, genetics, and genomics converge.
    Eukaryot Cell. 2005 Feb;4(2):225-9 PMID: 15701784
  52. Septin-dependent compartmentalization of the endoplasmic reticulum during yeast polarized growth.
    J Cell Biol. 2005 Jun 20;169(6):897-908 PMID: 15967812
  53. The secretory pathway mediates localization of the cell polarity regulator Aip3p/Bud6p.
    Mol Biol Cell. 2000 Feb;11(2):647-61 PMID: 10679021
  54. Polarized growth controls cell shape and bipolar bud site selection in Saccharomyces cerevisiae.
    Mol Cell Biol. 2000 Jul;20(14):5235-47 PMID: 10866679
  55. Dynamic localization and function of Bni1p at the sites of directed growth in Saccharomyces cerevisiae.
    Mol Cell Biol. 2001 Feb;21(3):827-39 PMID: 11154270
  56. The CDC42 homolog of the dimorphic fungus Penicillium marneffei is required for correct cell polarization during growth but not development.
    J Bacteriol. 2001 Jun;183(11):3447-57 PMID: 11344153
  57. Role of bud6p and tea1p in the interaction between actin and microtubules for the establishment of cell polarity in fission yeast.
    Curr Biol. 2001 Jun 5;11(11):836-45 PMID: 11516644
  58. Septum formation in Aspergillus nidulans.
    Curr Opin Microbiol. 2001 Dec;4(6):736-9 PMID: 11731327
  59. Yeast formins regulate cell polarity by controlling the assembly of actin cables.
    Nat Cell Biol. 2002 Jan;4(1):42-50 PMID: 11740491
  60. Polarity in filamentous fungi: moving beyond the yeast paradigm.
    Fungal Genet Biol. 2004 Apr;41(4):391-400 PMID: 14998522
Article Info
Journal
Eukaryotic cell
Abbr.
Eukaryot Cell
ISSN
1535-9778
Published
2006-06-00
Pages
881-95
Language
English
Region
United States
NLM ID
101130731
PMCID
PMC1489272
Subset
IM
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