1887

Abstract

Asexual development in the filamentous fungus is governed by the timely expression and cellular localization of multiple transcription factors. Hence, factors mediating import and export across the nuclear pore complexes (karyopherins) are expected to play a key role in coordinating the developmental programme. Here we characterize KapI, a putative homologue of the Kap121/Pse1p karyopherin. KapI is a non-essential importin--like protein located in the nucleus during vegetative growth and conidiophore development. The Δ phenotype is aconidial with many aerial hyphae. This phenotype can be suppressed under abiotic stress. In this regard, it resembles that of the null allele of the bZIP transcription factor FlbB. However a Δ Δ double mutant exhibited an additive phenotype with totally impaired conidiation, unresponsive to abiotic stress. In contrast to Δ, the null mutant is not a fluffy-low-bristle expression mutant. Taken together the findings indicate that KapI is required during asexual development, mediating the nuclear transport of factors acting in a different pathway(s) from those involving the upstream developmental activators.

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2009-12-01
2019-11-12
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References

  1. Adams, T. H., Wieser, J. K. & Yu, J. H. ( 1998; ). Asexual sporulation in Aspergillus nidulans. Microbiol Mol Biol Rev 62, 35–54.
    [Google Scholar]
  2. Baake, M., Bauerle, M., Doenecke, D. & Albig, W. ( 2001; ). Core histones and linker histones are imported into the nucleus by different pathways. Eur J Cell Biol 80, 669–677.[CrossRef]
    [Google Scholar]
  3. Chook, Y. M. & Blobel, G. ( 1999; ). Structure of the nuclear transport complex karyopherin-beta2-Ran x GppNHp. Nature 399, 230–237.[CrossRef]
    [Google Scholar]
  4. Delahodde, A., Pandjaitan, R., Corral-Debrinski, M. & Jacq, C. ( 2001; ). Pse1/Kap121-dependent nuclear localization of the major yeast multidrug resistance (MDR) transcription factor Pdr1. Mol Microbiol 39, 304–312.[CrossRef]
    [Google Scholar]
  5. Dutton, J. R., Johns, S. & Miller, B. L. ( 1997; ). StuAp is a sequence-specific transcription factor that regulates developmental complexity in Aspergillus nidulans. EMBO J 16, 5710–5721.[CrossRef]
    [Google Scholar]
  6. Espeso, E. A. & Osmani, S. A. ( 2008; ). Nuclear pore complex and transport in Aspergillus nidulans. In The Aspergilli: Genomics, Medical Aspects, Biotechnology, and Research Methods, pp. 261–277. Edited by G. H. Goldman & S. A. Osmani. Boca Raton: Taylor & Francis.
  7. Etxebeste, O., Ni, M., Garzia, A., Kwon, N. J., Fischer, R., Yu, J. H., Espeso, E. A. & Ugalde, U. ( 2008; ). Basic-zipper-type transcription factor FlbB controls asexual development in Aspergillus nidulans. Eukaryot Cell 7, 38–48.[CrossRef]
    [Google Scholar]
  8. Etxebeste, O., Herrero-Garcia, E., Araujo-Bazan, L., Rodriguez, A., Garzia, A., Ugalde, U. & Espeso, E. A. ( 2009; ). The bZIP-type transcription factor FlbB regulates distinct morphogenetic stages of colony formation in Aspergillus nidulans. Mol Microbiol 73, 775–789.
    [Google Scholar]
  9. Fried, H. & Kutay, U. ( 2003; ). Nucleocytoplasmic transport: taking an inventory. Cell Mol Life Sci 60, 1659–1688.[CrossRef]
    [Google Scholar]
  10. Fu, X., Choi, Y. K., Qu, D., Yu, Y., Cheung, N. S. & Qi, R. Z. ( 2006; ). Identification of nuclear import mechanisms for the neuronal Cdk5 activator. J Biol Chem 281, 39014–39021.[CrossRef]
    [Google Scholar]
  11. Garzia, A., Etxebeste, O., Herrero-Garcia, E., Fischer, R., Espeso, E. A. & Ugalde, U. ( 2009; ). Aspergillus nidulans FlbE is an upstream developmental activator of conidiation functionally associated with the putative transcription factor FlbB. Mol Microbiol 71, 172–184.[CrossRef]
    [Google Scholar]
  12. Glover, J. N. M. & Harrison, S. C. ( 1995; ). Crystal structure of the heterodimeric bZIP transcription factor c-Fos-c-Jun bound to DNA. Nature 373, 257–261.[CrossRef]
    [Google Scholar]
  13. Groves, M. R., Hanlon, N., Turowski, P., Hemmings, B. A. & Barford, D. ( 1999; ). The structure of the protein phosphatase 2A PR65/A subunit reveals the conformation of its 15 tandemly repeated HEAT motifs. Cell 96, 99–110.[CrossRef]
    [Google Scholar]
  14. Isoyama, T., Murayama, A., Nomoto, A. & Kuge, S. ( 2001; ). Nuclear import of the yeast AP-1-like transcription factor Yap1p is mediated by transport receptor Pse1p, and this import step is not affected by oxidative stress. J Biol Chem 276, 21863–21869.[CrossRef]
    [Google Scholar]
  15. Kaffman, A., Rank, N. M. & O'Shea, E. K. ( 1998; ). Phosphorylation regulates association of the transcription factor Pho4 with its import receptor Pse1/Kap121. Genes Dev 12, 2673–2683.[CrossRef]
    [Google Scholar]
  16. Kües, U. & Fischer, R. ( 2006; ). Asexual sporulation in mycelial fungi. In The Mycota, vol. I, Growth, Differentiation and Sexuality, pp. 263–292. Edited by U. Kües & R. Fischer. Berlin: Springer.
  17. Leslie, D. M., Grill, B., Rout, M. P., Wozniak, R. W. & Aitchison, J. D. ( 2002; ). Kap121p-mediated nuclear import is required for mating and cellular differentiation in yeast. Mol Cell Biol 22, 2544–2555.[CrossRef]
    [Google Scholar]
  18. Mims, C. W., Richardson, W. D. & Timberlake, W. E. ( 1988; ). Ultrastructural analysis of conidiophore development in the fungus Aspergillus nidulans using freeze-substitution. Protoplasma 144, 132–141.[CrossRef]
    [Google Scholar]
  19. Mosammaparast, N. & Pemberton, L. F. ( 2004; ). Karyopherins: from nuclear-transport mediators to nuclear-function regulators. Trends Cell Biol 14, 547–556.[CrossRef]
    [Google Scholar]
  20. Nayak, T., Szewczyk, E., Oakley, C. E., Osmani, A., Ukil, L., Murray, S. L., Hynes, M. J., Osmani, S. A. & Oakley, B. R. ( 2006; ). A versatile and efficient gene-targeting system for Aspergillus nidulans. Genetics 172, 1557–1566.
    [Google Scholar]
  21. Petosa, C., Schoehn, G., Askjaer, P., Bauer, U., Moulin, M., Steuerwald, U., Soler-Lopez, M., Baudin, F., Mattaj, I. W. & Muller, C. W. ( 2004; ). Architecture of CRM1/Exportin1 suggests how cooperativity is achieved during formation of a nuclear export complex. Mol Cell 16, 761–775.[CrossRef]
    [Google Scholar]
  22. Prade, R. A. & Timberlake, W. E. ( 1993; ). The Aspergillus nidulans brlA regulatory locus consists of overlapping transcription units that are individually required for conidiophore development. EMBO J 12, 2439–2447.
    [Google Scholar]
  23. Ramon, A., Muro-Pastor, M. I., Scazzocchio, C. & Gonzalez, R. ( 2000; ). Deletion of the unique gene encoding a typical histone H1 has no apparent phenotype in Aspergillus nidulans. Mol Microbiol 35, 223–233.[CrossRef]
    [Google Scholar]
  24. Reeslev, M. & Kjoller, A. ( 1995; ). Comparison of biomass dry weights and radial growth rates of fungal colonies on media solidified with different gelling compounds. Appl Environ Microbiol 61, 4236–4239.
    [Google Scholar]
  25. Ross, A. E., Vuica, M. & Desiderio, S. ( 2003; ). Overlapping signals for protein degradation and nuclear localization define a role for intrinsic RAG-2 nuclear uptake in dividing cells. Mol Cell Biol 23, 5308–5319.[CrossRef]
    [Google Scholar]
  26. Rout, M. P., Blobel, G. & Aitchison, J. D. ( 1997; ). A distinct nuclear import pathway used by ribosomal proteins. Cell 89, 715–725.[CrossRef]
    [Google Scholar]
  27. Schaper, S., Franke, J., Meijsing, S. H. & Ehrenhofer-Murray, A. E. ( 2005; ). Nuclear import of the histone acetyltransferase complex SAS-I in Saccharomyces cerevisiae. J Cell Sci 118, 1473–1484.[CrossRef]
    [Google Scholar]
  28. Seedorf, M. & Silver, P. A. ( 1997; ). Importin/karyopherin protein family members required for mRNA export from the nucleus. Proc Natl Acad Sci U S A 94, 8590–8595.[CrossRef]
    [Google Scholar]
  29. Seo, J. A., Guan, Y. & Yu, J. H. ( 2006; ). FluG-dependent asexual development in Aspergillus nidulans occurs via derepression. Genetics 172, 1535–1544.
    [Google Scholar]
  30. Sewall, T. C., Mims, C. W. & Timberlake, W. E. ( 1990; ). abaA controls phialide differentiation in Aspergillus nidulans. Plant Cell 2, 731–739.[CrossRef]
    [Google Scholar]
  31. Stewart, M. ( 2007; ). Molecular mechanism of the nuclear protein import cycle. Nat Rev Mol Cell Biol 8, 195–208.[CrossRef]
    [Google Scholar]
  32. Strom, A. C. & Weis, K. ( 2001; ). Importin-beta-like nuclear transport receptors. Genome Biology 2, reviews3008
    [Google Scholar]
  33. Timney, B. L., Tetenbaum-Novatt, J., Agate, D. S., Williams, R., Zhang, W., Chait, B. T. & Rout, M. P. ( 2006; ). Simple kinetic relationships and nonspecific competition govern nuclear import rates in vivo. J Cell Biol 175, 579–593.[CrossRef]
    [Google Scholar]
  34. Toda, T., Shimanuki, M., Saka, Y., Yamano, H., Adachi, Y., Shirakawa, M., Kyogoku, Y. & Yanagida, M. ( 1992; ). Fission yeast pap1-dependent transcription is negatively regulated by an essential nuclear protein, crm1. Mol Cell Biol 12, 5474–5484.
    [Google Scholar]
  35. Trinci, A. P. ( 1974; ). A study of the kinetics of hyphal extension and branch initiation of fungal mycelia. J Gen Microbiol 81, 225–236.[CrossRef]
    [Google Scholar]
  36. Trinci, A. P. J., Wiebe, M. G. & Robson, G. D. ( 1994; ). The mycelium as an integrated entity. In The Mycota, vol. I, Growth, Differentiation and Sexuality, pp. 175–193. Edited by J. G. H. Wessels & F. Meinhardt. Berlin & Heidelberg: Springer.
  37. Vesentini, D., Dickinson, D. J. & Murphy, R. J. ( 2006; ). Fungicides affect the production of extracellular mucilaginous material (ECMM) and the peripheral growth unit (PGU) in two wood-rotting basidiomycetes. Mycol Res 110, 1207–1213.[CrossRef]
    [Google Scholar]
  38. Wieser, J. & Adams, T. H. ( 1995; ). flbD encodes a Myb-like DNA-binding protein that coordinates initiation of Aspergillus nidulans conidiophore development. Genes Dev 9, 491–502.[CrossRef]
    [Google Scholar]
  39. Wieser, J., Lee, B., Fondon, J., III & Adams, T. H. ( 1994; ). Genetic requirements for initiating asexual development in Aspergillus nidulans. Curr Genet 27, 62–69.[CrossRef]
    [Google Scholar]
  40. Yang, L., Ukil, L., Osmani, A., Nahm, F., Davies, J., De Souza, C. P. C., Dou, X., Perez-Balaguer, A. & Osmani, S. A. ( 2004; ). Rapid production of gene replacement constructs and generation of a green fluorescent protein-tagged centromeric marker in Aspergillus nidulans. Eukaryot Cell 3, 1359–1362.[CrossRef]
    [Google Scholar]
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vol. , part 12, pp. 3934 - 3945

Multiple alignments of KapI-like karyopherins: amino acid sequence alignment of putative KapI homologues [ PDF] (1.5 MB)



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