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The Aspergillus nidulans pkcA gene is involved in polarized growth, morphogenesis and maintenance of cell wall integrity

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Abstract

The protein kinase C (PKC) family participates in maintaining integrity and growth of fungal cell walls. However, the precise molecular role of these proteins in the filamentous fungi remains unknown. In this work, pkcA, the gene encoding the PKC homolog in the filamentous fungus Aspergillus nidulans, was cloned and its function analyzed using a conditional alcA-PKC mutant strain. Repression of pkcA expression resulted in increased conidial swelling, decreased rates of hyphal growth, changes in the ultrastructure of the cell wall and increased sensitivity to antifungal agents. These results suggest that the protein encoded by pkcA is involved in key aspects of cell morphogenesis and cell wall integrity.

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References

  • Antonsson B, Montessuit S, Friedli L, Payton MA, Paravicini G (1994) Protein kinase C in yeast. Characteristics of the Saccharomyces cerevisiae PKC1 gene product. J Biol Chem 269:16821–16828

    PubMed  CAS  Google Scholar 

  • Arpaia G, Cerri F, Baima S, Macino G (1999) Involvement of protein kinase C in the response of Neurospora crassa to blue light. Mol Gen Genet 262:314–322

    Article  PubMed  CAS  Google Scholar 

  • Bussink HJ, Osmani SA (1999) A mitogen-activated protein kinase (MPKA) is involved in polarized growth in the filamentous fungus, Aspergillus nidulans. FEMS Microbiol Lett 173:117–125

    PubMed  CAS  Google Scholar 

  • Buurman ET, Andrews B, Blodgett AE, Chavda JS, Schnell NF (2005) Utilization of target-specific, hypersensitive strains of Saccharomyces cerevisiae to determine the mode of action of antifungal compounds. Antimicrob Agents Chemother 49:2558–2560

    Article  PubMed  CAS  Google Scholar 

  • Davenport K R, Sohaskey M, Kamada Y, Levin D E, Gustin MC (1995) A second osmosensing signal transduction pathway in yeast. Hypotonic shock activates the PKC1 protein kinase-regulated cell integrity pathway. J Biol Chem 270:30157–30161

    Article  PubMed  CAS  Google Scholar 

  • Franchi L, Fulci V, Macino G (2005) Protein kinase C modulates light responses in Neurospora by regulating the blue light photoreceptor WC-1. Mol Microbiol 56:334–345

    Article  PubMed  CAS  Google Scholar 

  • Gatherar IM, Pollerman S, Dunn-Coleman N, Turner G (2004) Identification of a novel gene hbrB required for polarised growth in Aspergillus nidulans. Fungal Genet Biol 41:463–471

    Article  PubMed  CAS  Google Scholar 

  • Geissenhoner A, Sievers N, Brock M, Fischer R (2001) Aspergillus nidulans DigA, a potential homolog of Saccharomyces cerevisiae Pep3(Vps18), is required for nuclear migration, mitochondrial morphology andpolarized growth. Mol Genet Genomics 266:672–685

    Article  PubMed  CAS  Google Scholar 

  • Guest GM, Lin X, Momany M (2004) Aspergillus nidulans RhoA is involved in polar growth, branching, and cell wall synthesis. Fungal Genet Biol 41:13–22

    Article  PubMed  CAS  Google Scholar 

  • Gwynne DI, Buxton FP, Sibley S, Davies RW, Lockington RA, Scazzocchio C, Sealy-Lewis HM (1987) Comparison of the cis-acting control regions of two coordinately controlled genes involved in ethanol utilization in Aspergillus nidulans. Gene 51:205–216

    Article  PubMed  CAS  Google Scholar 

  • Heinisch JJ, Lorberg A, Schmitz HP, Jacoby JJ (1999) The protein kinase C-mediated MAP kinase pathway involved in the maintenance of cellular integrity in Saccharomyces cerevisiae. Mol Microbiol 32:671–680

    Article  PubMed  CAS  Google Scholar 

  • Herrmann M, Sprote P, Brakhage AA (2006) Protein kinase C (PkcA) of Aspergillus nidulans is involved in penicillin production. Appl Environ Microbiol 72:2957–2970

    Article  PubMed  CAS  Google Scholar 

  • Horiuchi H, Fujiwara M, Yamashita S, Ohta A, Takagi M (1999) Proliferation of intrahyphal hyphae caused by disruption of csmA, which encodes a class V chitin synthase with a myosin motor-like domain in Aspergillus nidulans. J Bacteriol 181:3721–3729

    PubMed  CAS  Google Scholar 

  • Ichinomiya M, Motoyama T, Fujiwara M, Takagi M, Horiuchi H, Ohta A (2002) Repression of chsB expression reveals the functional importance of class IV chitin synthase gene chsD in hyphal growth and conidiation of Aspergillus nidulans. Microbiology 148:1335–1347

    PubMed  CAS  Google Scholar 

  • Jadoun J, Shadkchan Y, Osherov N (2004) Disruption of the Aspergillus fumigatus argB gene using a novel in vitro transposon-based mutagenesis approach. Curr Genet 45:235–241

    Article  PubMed  CAS  Google Scholar 

  • Jung US, Levin DE (1999) Genome-wide analysis of gene expression regulated by the yeast cell wall integrity signalling pathway. Mol Microbiol 34:1049–1057

    Article  PubMed  CAS  Google Scholar 

  • Kamada Y, Jung US, Piotrowski J, Levin DE (1995a) The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev 9:1559–1571

    CAS  Google Scholar 

  • Kamada Y, Jung US, Piotrowski J, Levin DE (1995b) The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev 9:1559–1571

    CAS  Google Scholar 

  • Ketela T, Green R, Bussey H (1999) Saccharomyces cerevisiae Mid2p is a potential cell wall stress sensor and upstream activator of the PKC1-MPK1 cell integrity pathway. J Bacteriol 181:3330–3340

    PubMed  CAS  Google Scholar 

  • Kiso T, Fujita K, Ping X, Tanaka T, Taniguchi M (2004) Screening for microtubule-disrupting antifungal agents by using a mitotic-arrest mutant of Aspergillus nidulans and novel action of phenylalanine derivatives accompanying tubulin loss. Antimicrob Agents Chemother 48:1739–1748

    Article  PubMed  CAS  Google Scholar 

  • Klionsky DJ, Herman PK, Emr SD (1990) The fungal vacuole: composition, function, and biogenesis. Microbiol Rev 54:266–292

    PubMed  CAS  Google Scholar 

  • Kobori H, Toda T, Yaguchi H, Toya M, Yanagida M, Osumi M (1994) Fission yeast protein kinase C gene homologues are required for protoplast regeneration: a functional link between cell wall formation and cell shape control. J Cell Sci 107:1131–1136

    PubMed  CAS  Google Scholar 

  • Levin DE, Fields FO, Kunisawa R, Bishop JM, Thorner J (1990) A candidate protein kinase C gene, PKC1, is required for the S. cerevisiae cell cycle. Cell 62:213–224

    Article  PubMed  CAS  Google Scholar 

  • May GS, Morris NR (1988) Developmental regulation of a conidiation-specific β-tubulin in Aspergillus nidulans. Dev Biol 128:406–414

    Article  PubMed  CAS  Google Scholar 

  • McGoldrick CA, Gruver C, May GS (1995) myoA of Aspergillus nidulans encodes an essential myosin I required for secretion and polarized growth. J Cell Biol 128:577–587

    Article  PubMed  CAS  Google Scholar 

  • Mellor H, Parker PJ (1998) The extended protein kinase C superfamily. Biochem J 332:281–292

    PubMed  CAS  Google Scholar 

  • Nonaka H, Tanaka K, Hirano H, Fujiwara T, Kohno H, Umikawa M, Mino A, Takai Y (1995) A downstream target of RHO1 small GTP-binding protein is PKC1, a homolog of protein kinase C, which leads to activation of the MAP kinase cascade in Saccharomyces cerevisiae. EMBO J 14:5931–5938

    PubMed  CAS  Google Scholar 

  • Oeser B (1998) PKC1, encoding a protein kinase C, and FAT1, encoding a fatty acid transporter protein, are neighbours in Cochliobolus heterostrophus. FEMS Microbiol Lett 165:273–280

    Article  PubMed  CAS  Google Scholar 

  • Osherov N, Yamashita RA, Chung YS, May GS (1998) Structural requirements for in vivo myosin I function in Aspergillus nidulans. J Biol Chem 273:27017–27025

    Article  PubMed  CAS  Google Scholar 

  • Paravicini G, Cooper M, Friedli L, Smith DJ, Carpentier JL, Klig LS, Payton MA (1992) The osmotic integrity of the yeast cell requires a functional PKC1 gene product. Mol Cell Biol 12:4896–4905

    PubMed  CAS  Google Scholar 

  • Paravicini G, Mendoza A, Antonsson B, Cooper M, Losberger C, Payton MA (1996) The C. albicans PKC1 gene encodes a protein kinase C homolog necessary for cellular integrity but not dimorphism. Yeast 12:741–756

    Article  PubMed  CAS  Google Scholar 

  • Sambrook J, Russel DW (2001) Molecular cloning: a laboratory manual, 3rd edn. CSHL Press, Cold Spring Harbor

    Google Scholar 

  • Schmitz HP, Jockel J, Block C, Heinisch JJ (2001) Domain shuffling as a tool for investigation of protein function: substitution of the cysteine-rich region of Raf kinase and PKC eta for that of yeast Pkc1p. J Mol Biol 311:1–7

    Article  PubMed  CAS  Google Scholar 

  • Schmitz HP, Heinisch JJ (2003) Evolution, biochemistry and genetics of protein kinase C in fungi. Curr Genet 43:245–254

    Article  PubMed  CAS  Google Scholar 

  • Steidl S, Hynes MJ, Brakhage AA (2001) The Aspergillus nidulans multimeric CCAAT binding complex AnCF is negatively autoregulated via its hapB subunit gene. J Mol Biol 306:643–653

    Article  PubMed  CAS  Google Scholar 

  • Sussman A, Huss K, Chio LC, Heidler S, Shaw M, Ma D, Zhu G, Campbell RM, Park TS, Kulanthaivel P, Scott JE, Carpenter JW, Strege MA, Belvo MD, Swartling JR, Fischl A, Yeh WK, Shih C, Ye XS (2004) Discovery of cercosporamide, a known antifungal natural product, as a selective Pkc1 kinase inhibitor through high-throughput screening. Eukaryot Cell 3:932–943

    Article  PubMed  CAS  Google Scholar 

  • Waring RB, May GS, Morris NR (1989) Characterization of an inducible expression system in Aspergillus nidulans using alcA and tubulin-coding genes. Gene 79:119–130

    Article  PubMed  CAS  Google Scholar 

  • Watanabe M, Chen CY, Levin DE (1994) Saccharomyces cerevisiae PKC1 encodes a protein kinase C (PKC) homolog with a substrate specificity similar to that of mammalian PKC. J Biol Chem 269:16829–16836

    PubMed  CAS  Google Scholar 

  • Xiang X, Zuo W, Efimov VP, Morris NR (1999) Isolation of a new set of Aspergillus nidulans mutants defective in nuclear migration. Curr Genet 35:626–630

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by the Stoltz Foundation and the Israel Academy of Sciences, grant 741/01 to NO.

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Correspondence to Nir Osherov.

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Communicated by A. Brakhage.

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Ronen, R., Sharon, H., Levdansky, E. et al. The Aspergillus nidulans pkcA gene is involved in polarized growth, morphogenesis and maintenance of cell wall integrity. Curr Genet 51, 321–329 (2007). https://doi.org/10.1007/s00294-007-0129-y

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  • DOI: https://doi.org/10.1007/s00294-007-0129-y

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