1887

Abstract

The genome encodes two 1,3-α-glucan synthases. One of these 1,3-α-glucan synthase genes, , was shown to be required for the synthesis of 1,3-α-glucan in the aerial hyphae and macroconidia cell walls. 1,3-α-Glucan was found in the conidia cell wall, but was absent from the vegetative hyphae cell wall. Deletion of affected conidial development. Δ produced only 5 % as many conidia as the WT and most of the conidia produced by Δ were not viable. The upstream regulatory elements were shown to direct cell-type-specific expression of red fluorescent protein in conidia and aerial hyphae. A haemagglutinin-tagged AGS-1 was found to be expressed in aerial hyphae and conidia. The research showed that 1,3-α-glucan is an aerial hyphae and conidia cell wall component, and is required for normal conidial differentiation.

Funding
This study was supported by the:
  • National Institutes of Health (Award R01 GM078589)
  • National Science Foundation (Award DBI0923133)
  • University at Buffalo Foundation
  • National Institutes of Health (Award P01 GM068087)
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.080002-0
2014-08-01
2021-10-27
Loading full text...

Full text loading...

/deliver/fulltext/micro/160/8/1618.html?itemId=/content/journal/micro/10.1099/mic.0.080002-0&mimeType=html&fmt=ahah

References

  1. Bates S., Hughes H. B., Munro C. A., Thomas W. P., MacCallum D. M., Bertram G., Atrih A., Ferguson M. A., Brown A. J. & other authors ( 2006). Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J Biol Chem 281:90–98 [View Article][PubMed]
    [Google Scholar]
  2. Beauvais A., Bozza S., Kniemeyer O., Formosa C., Balloy V., Henry C., Roberson R. W., Dague E., Chignard M. & other authors ( 2013). Deletion of the α-(1,3)-glucan synthase genes induces a restructuring of the conidial cell wall responsible for the avirulence of Aspergillus fumigatus. PLoS Pathog 9:e1003716 [View Article][PubMed]
    [Google Scholar]
  3. Borkovich K. A., Alex L. A., Yarden O., Freitag M., Turner G. E., Read N. D., Seiler S., Bell-Pedersen D., Paietta J. & other authors ( 2004). Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 68:1–108 [View Article][PubMed]
    [Google Scholar]
  4. Bowman S. M., Free S. J. ( 2006). The structure and synthesis of the fungal cell wall. Bioessays 28:799–808 [View Article][PubMed]
    [Google Scholar]
  5. Bowman B. J., Draskovic M., Freitag M., Bowman E. J. ( 2009). Structure and distribution of organelles and cellular location of calcium transporters in Neurospora crassa. Eukaryot Cell 8:1845–1855 [View Article][PubMed]
    [Google Scholar]
  6. Colot H. V., Park G., Turner G. E., Ringelberg C., Crew C. M., Litvinkova L., Weiss R. L., Borkovich K. A., Dunlap J. C. ( 2006). A high-throughput gene knockout procedure for Neurospora reveals functions for multiple transcription factors. Proc Natl Acad Sci U S A 103:10352–10357 [View Article][PubMed]
    [Google Scholar]
  7. Cortés J. C., Sato M., Muñoz J., Moreno M. B., Clemente-Ramos J. A., Ramos M., Okada H., Osumi M., Durán A., Ribas J. C. ( 2012). Fission yeast Ags1 confers the essential septum strength needed for safe gradual cell abscission. J Cell Biol 198:637–656 [View Article][PubMed]
    [Google Scholar]
  8. Davis R. H., DeSerres F. J. ( 1970). Genetic and microbiological research techniques for Neurospora crassa. Methods Enzymol 17:79–143 [View Article]
    [Google Scholar]
  9. Fontaine T., Simenel C., Dubreucq G., Adam O., Delepierre M., Lemoine J., Vorgias C. E., Diaquin M., Latgé J. P. ( 2000). Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J Biol Chem 275:27594–27607[PubMed]
    [Google Scholar]
  10. Fontaine T., Beauvais A., Loussert C., Thevenard B., Fulgsang C. C., Ohno N., Clavaud C., Prevost M. C., Latgé J. P. ( 2010). Cell wall alpha1–3glucans induce the aggregation of germinating conidia of Aspergillus fumigatus. Fungal Genet Biol 47:707–712 [View Article][PubMed]
    [Google Scholar]
  11. Free S. J. ( 2013). Fungal cell wall organization and biosynthesis. Adv Genet 81:33–82 [View Article][PubMed]
    [Google Scholar]
  12. Freitag M., Selker E. U. ( 2005). Expression and visualization of red fluorescent protein (RFP) in Neurospora crassa.. Fungal Genet Newslett 52:14–17
    [Google Scholar]
  13. Fu C., Iyer P., Herkal A., Abdullah J., Stout A., Free S. J. ( 2011). Identification and characterization of genes required for cell-to-cell fusion in Neurospora crassa. Eukaryot Cell 10:1100–1109 [View Article][PubMed]
    [Google Scholar]
  14. Fujikawa T., Sakaguchi A., Nishizawa Y., Kouzai Y., Minami E., Yano S., Koga H., Meshi T., Nishimura M. ( 2012). Surface α-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants. PLoS Pathog 8:e1002882 [View Article][PubMed]
    [Google Scholar]
  15. Futagami T., Goto M. ( 2012). Putative cell wall integrity sensor proteins in Aspergillus nidulans. Commun Integr Biol 5:206–208 [View Article][PubMed]
    [Google Scholar]
  16. Futagami T., Nakao S., Kido Y., Oka T., Kajiwara Y., Takashita H., Omori T., Furukawa K., Goto M. ( 2011). Putative stress sensors WscA and WscB are involved in hypo-osmotic and acidic pH stress tolerance in Aspergillus nidulans. Eukaryot Cell 10:1504–1515 [View Article][PubMed]
    [Google Scholar]
  17. Galagan J. E., Calvo S. E., Borkovich K. A., Selker E. U., Read N. D., Jaffe D., FitzHugh W., Ma L. J., Smirnov S. & other authors ( 2003). The genome sequence of the filamentous fungus Neurospora crassa. Nature 422:859–868 [View Article][PubMed]
    [Google Scholar]
  18. Gastebois A., Clavaud C., Aimanianda V., Latgé J. P. ( 2009). Aspergillus fumigatus: cell wall polysaccharides, their biosynthesis and organization. Future Microbiol 4:583–595 [View Article][PubMed]
    [Google Scholar]
  19. Hochstenbach F., Klis F. M., van den Ende H., van Donselaar E., Peters P. J., Klausner R. D. ( 1998). Identification of a putative alpha-glucan synthase essential for cell wall construction and morphogenesis in fission yeast. Proc Natl Acad Sci U S A 95:9161–9166 [View Article][PubMed]
    [Google Scholar]
  20. Kapteyn J. C., Montijin R. C., Vink E., de la Cruz J., Llobell A., Douwes J. E., Shimoi H., Lipke P. N., Klis F. M. ( 1996). Retention of Saccharomyces cerevisiae cell wall proteins through a phosphodiester-linked beta-1,3-/beta-1,6-glucan heteropolymer. Glycobiology 6:337–345 [View Article][PubMed]
    [Google Scholar]
  21. Kikuchi N., Narimatsu H. ( 2006). Bioinformatics for comprehensive finding and analysis of glycosyltransferases. Biochim Biophys Acta 1760:578–583 [View Article][PubMed]
    [Google Scholar]
  22. Klis F. M., Boorsma A., De Groot P. W. ( 2006). Cell wall construction in Saccharomyces cerevisiae. Yeast 23:185–202 [View Article][PubMed]
    [Google Scholar]
  23. Kollár R., Reinhold B. B., Petráková E., Yeh H. J., Ashwell G., Drgonová J., Kapteyn J. C., Klis F. M., Cabib E. ( 1997). Architecture of the yeast cell wall. beta(1→6)-glucan interconnects mannoprotein, beta(1→)3-glucan, and chitin. J Biol Chem 272:17762–17775 [View Article][PubMed]
    [Google Scholar]
  24. Kumar V. ( 2011). Identification of the sequence motif of glycoside hydrolase 13 family members. Bioinformation 6:61–63 [View Article][PubMed]
    [Google Scholar]
  25. Latgé J. P. ( 2007). The cell wall: a carbohydrate armour for the fungal cell. Mol Microbiol 66:279–290 [View Article][PubMed]
    [Google Scholar]
  26. Latgé J. P., Mouyna I., Tekaia F., Beauvais A., Debeaupuis J. P., Nierman W. ( 2005). Specific molecular features in the organization and biosynthesis of the cell wall of Aspergillus fumigatus. Med Mycol 43:Suppl 1S15–S22 [View Article][PubMed]
    [Google Scholar]
  27. Lesage G., Bussey H. ( 2006). Cell wall assembly in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70:317–343 [View Article][PubMed]
    [Google Scholar]
  28. Linding R., Russell R. B., Neduva V., Gibson T. J. ( 2003). GlobPlot: exploring protein sequences for globularity and disorder. Nucleic Acids Res 31:3701–3708 [View Article][PubMed]
    [Google Scholar]
  29. Lu C. F., Montijn R. C., Brown J. L., Klis F., Kurjan J., Bussey H., Lipke P. N. ( 1995). Glycosyl phosphatidylinositol-dependent cross-linking of alpha-agglutinin and beta 1,6-glucan in the Saccharomyces cerevisiae cell wall. J Cell Biol 128:333–340 [View Article][PubMed]
    [Google Scholar]
  30. Maddi A., Free S. J. ( 2010). α-1,6-Mannosylation of N-linked oligosaccharide present on cell wall proteins is required for their incorporation into the cell wall in the filamentous fungus Neurospora crassa. Eukaryot Cell 9:1766–1775 [View Article][PubMed]
    [Google Scholar]
  31. Margolin B. S., Frietag M., Selker E. U. ( 1997). Improved plasmids for gene targeting at the his-3 locus of Neurospora crassa.. Fungal Genet Newslett 44:34–36
    [Google Scholar]
  32. Maubon D., Park S., Tanguy M., Huerre M., Schmitt C., Prévost M. C., Perlin D. S., Latgé J. P., Beauvais A. ( 2006). AGS3, an alpha(1–3)glucan synthase gene family member of Aspergillus fumigatus, modulates mycelium growth in the lung of experimentally infected mice. Fungal Genet Biol 43:366–375 [View Article][PubMed]
    [Google Scholar]
  33. Pardini G., De Groot P. W., Coste A. T., Karababa M., Klis F. M., de Koster C. G., Sanglard D. ( 2006). The CRH family coding for cell wall glycosylphosphatidylinositol proteins with a predicted transglycosidase domain affects cell wall organization and virulence of Candida albicans. J Biol Chem 281:40399–40411 [View Article][PubMed]
    [Google Scholar]
  34. Rappleye C. A., Engle J. T., Goldman W. E. ( 2004). RNA interference in Histoplasma capsulatum demonstrates a role for alpha-(1,3)-glucan in virulence. Mol Microbiol 53:153–165 [View Article][PubMed]
    [Google Scholar]
  35. Rappleye C. A., Eissenberg L. G., Goldman W. E. ( 2007). Histoplasma capsulatum alpha-(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor. Proc Natl Acad Sci U S A 104:1366–1370 [View Article][PubMed]
    [Google Scholar]
  36. Reese A. J., Yoneda A., Breger J. A., Beauvais A., Liu H., Griffith C. L., Bose I., Kim M. J., Skau C. & other authors ( 2007). Loss of cell wall alpha(1-3) glucan affects Cryptococcus neoformans from ultrastructure to virulence. Mol Microbiol 63:1385–1398 [View Article][PubMed]
    [Google Scholar]
  37. Ruiz-Herrera J., Elorza M. V., Valentín E., Sentandreu R. ( 2006). Molecular organization of the cell wall of Candida albicans and its relation to pathogenicity. FEMS Yeast Res 6:14–29 [View Article][PubMed]
    [Google Scholar]
  38. Selker E. U. ( 1999). Gene silencing: repeats that count. Cell 97:157–160 [View Article][PubMed]
    [Google Scholar]
  39. Sestero C. M., Scalarone G. M. ( 2007). Detection of the surface antigens BAD1 and alpha-(1,3)-glucan in six different strains of Blastomyces dermatitidus using monoclonal antibodies. J Med Biol Sci 1:1–7
    [Google Scholar]
  40. Springer M. L., Yanofsky C. ( 1989). A morphological and genetic analysis of conidiophore development in Neurospora crassa. Genes Dev 3:559–571 [View Article][PubMed]
    [Google Scholar]
  41. Vos A., Dekker N., Distel B., Leunissen J. A., Hochstenbach F. ( 2007). Role of the synthase domain of Ags1p in cell wall alpha-glucan biosynthesis in fission yeast. J Biol Chem 282:18969–18979 [View Article][PubMed]
    [Google Scholar]
  42. Yoshimi A., Sano M., Inaba A., Kokubun Y., Fujioka T., Mizutani O., Hagiwara D., Fujikawa T., Nishimura M. & other authors ( 2013). Functional analysis of the α-1,3-glucan synthase genes agsA and agsB in Aspergillus nidulans: agsB is the major α-1,3-glucan synthase in this fungus. PLoS ONE 8:e54893 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.080002-0
Loading
/content/journal/micro/10.1099/mic.0.080002-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error