1887

Abstract

Sporulation is an essential part of the life cycle of the industrially important filamentous fungus . The formation of conidiophores, spore-bearing structures, requires remodelling of the fungal cell wall, as demonstrated by the differences in carbohydrate composition of cell walls of vegetative mycelium and spores. Glycoside hydrolases that are involved in this process have so far remained unidentified. Using transcriptome analysis, we have identified genes encoding putative cell-wall-modifying proteins with enhanced expression in sporulating aerial mycelium compared to vegetative mycelium. Among the most strongly induced genes were those encoding a protein consisting of a putative chitin binding module (CBM14) and the chitinolytic enzymes NagA, CfcI and CtcB. Reporter studies showed that the -acetyl-β-hexosaminidase gene was expressed both in vegetative hyphae and in aerial structures (aerial hyphae, conidiophores and conidia) upon starvation. In contrast, promoter activities of the chitinase genes and were specifically localized in the conidiophores and conidia. CtcB is an endo-chitinase and CfcI releases monomers from chitin oligosaccharides: together these enzymes have the potential to degrade chitin of the fungal cell wall. Inactivation of both the and genes affected neither radial growth rate, nor formation and germination of spores. The amount of chitin in the spore walls of a ΔΔ double deletion strain, however, was significantly increased compared with the wild-type, thus indicating that CfcI and CtcB indeed modify the cell walls during sporulation. These novel insights in the sporulation process in aspergilli are of strong scientific relevance, and also may aid industrial strain engineering.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.067967-0
2013-09-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/9/1853.html?itemId=/content/journal/micro/10.1099/mic.0.067967-0&mimeType=html&fmt=ahah

References

  1. Adams T. H., Wieser J. K., Yu J. H. ( 1998). Asexual sporulation in Aspergillus nidulans . Microbiol Mol Biol Rev 62:35–54[PubMed]
    [Google Scholar]
  2. Aguilar-Osorio G., Vankuyk P. A., Seiboth B., Blom D., Solomon P. S., Vinck A., Kindt F., Wösten H. A., de Vries R. P. ( 2010). Spatial and developmental differentiation of mannitol dehydrogenase and mannitol-1-phosphate dehydrogenase in Aspergillus niger . Eukaryot Cell 9:1398–1402 [View Article][PubMed]
    [Google Scholar]
  3. Alcazar-Fuoli L., Clavaud C., Lamarre C., Aimanianda V., Seidl-Seiboth V., Mellado E., Latgé J. P. ( 2011). Functional analysis of the fungal/plant class chitinase family in Aspergillus fumigatus . Fungal Genet Biol 48:418–429 [View Article][PubMed]
    [Google Scholar]
  4. Alic M., Bennett J. W., Lasure L. L. ( 1991). More Gene Manipulations in Fungi San Diego, CA: Academic Press;
    [Google Scholar]
  5. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. ( 1990). Basic local alignment search tool. J Mol Biol 215:403–410[PubMed] [CrossRef]
    [Google Scholar]
  6. Arentshorst M., Ram A. F., Meyer V. ( 2012). Using non-homologous end-joining-deficient strains for functional gene analyses in filamentous fungi. Methods Mol Biol 835:133–150 [View Article][PubMed]
    [Google Scholar]
  7. Arnaud M. B., Chibucos M. C., Costanzo M. C., Crabtree J., Inglis D. O., Lotia A., Orvis J., Shah P., Skrzypek M. S. & other authors ( 2010). The Aspergillus Genome Database, a curated comparative genomics resource for gene, protein and sequence information for the Aspergillus research community. Nucleic Acids Res 38:Database issueD420–D427 [View Article][PubMed]
    [Google Scholar]
  8. Barrett T., Troup D. B., Wilhite S. E., Ledoux P., Evangelista C., Kim I. F., Tomashevsky M., Marshall K. A., Phillippy K. H. & other authors ( 2011). NCBI GEO: archive for functional genomics data sets–10 years on. Nucleic Acids Res 39:Database issueD1005–D1010 [View Article][PubMed]
    [Google Scholar]
  9. Bauer S., Vasu P., Persson S., Mort A. J., Somerville C. R. ( 2006). Development and application of a suite of polysaccharide-degrading enzymes for analyzing plant cell walls. Proc Natl Acad Sci U S A 103:11417–11422 [View Article][PubMed]
    [Google Scholar]
  10. Bleichrodt R., Vinck A., Krijgsheld P., van Leeuwen M. R., Dijksterhuis J., Wösten H. A. B. ( 2013). Cytosolic streaming in vegetative mycelium and aerial structures of Aspergillus niger . Stud Mycol 74:31–46 [View Article][PubMed]
    [Google Scholar]
  11. Bolwerk A., Lagopodi A. L., Lugtenberg B. J., Bloemberg G. V. ( 2005). Visualization of interactions between a pathogenic and a beneficial Fusarium strain during biocontrol of tomato foot and root rot. Mol Plant Microbe Interact 18:710–721 [View Article][PubMed]
    [Google Scholar]
  12. Bos C. J., Debets A. J., Swart K., Huybers A., Kobus G., Slakhorst S. M. ( 1988). Genetic analysis and the construction of master strains for assignment of genes to six linkage groups in Aspergillus niger . Curr Genet 14:437–443 [View Article][PubMed]
    [Google Scholar]
  13. Braaksma M., Martens-Uzunova E. S., Punt P. J., Schaap P. J. ( 2010). An inventory of the Aspergillus niger secretome by combining in silico predictions with shotgun proteomics data. BMC Genomics 11:584 [View Article][PubMed]
    [Google Scholar]
  14. Cabib E. ( 2009). Two novel techniques for determination of polysaccharide cross-links show that Crh1p and Crh2p attach chitin to both β(1-6)- and β(1-3)glucan in the Saccharomyces cerevisiae cell wall. Eukaryot Cell 8:1626–1636 [View Article][PubMed]
    [Google Scholar]
  15. Cabib E., Farkas V., Kosík O., Blanco N., Arroyo J., McPhie P. ( 2008). Assembly of the yeast cell wall. Crh1p and Crh2p act as transglycosylases in vivo and in vitro . J Biol Chem 283:29859–29872 [View Article][PubMed]
    [Google Scholar]
  16. Cantarel B. L., Coutinho P. M., Rancurel C., Bernard T., Lombard V., Henrissat B. ( 2009). The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:Database issueD233–D238 [View Article][PubMed]
    [Google Scholar]
  17. de Groot P. W., Hellingwerf K. J., Klis F. M. ( 2003). Genome-wide identification of fungal GPI proteins. Yeast 20:781–796 [View Article][PubMed]
    [Google Scholar]
  18. Delmas S., Pullan S. T., Gaddipati S., Kokolski M., Malla S., Blythe M. J., Ibbett R., Campbell M., Liddell S. & other authors ( 2012). Uncovering the genome-wide transcriptional responses of the filamentous fungus Aspergillus niger to lignocellulose using RNA sequencing. PLoS Genet 8:e1002875 [View Article][PubMed]
    [Google Scholar]
  19. Eisenhaber B., Schneider G., Wildpaner M., Eisenhaber F. ( 2004). A sensitive predictor for potential GPI lipid modification sites in fungal protein sequences and its application to genome-wide studies for Aspergillus nidulans, Candida albicans, Neurospora crassa, Saccharomyces cerevisiae and Schizosaccharomyces pombe . J Mol Biol 337:243–253 [View Article][PubMed]
    [Google Scholar]
  20. Erdei E., Pusztahelyi T., Miskei M., Barna T., Pócsi I. ( 2008). Characterization and heterologous expression of an age-dependent fungal/bacterial type chitinase of Aspergillus nidulans . Acta Microbiol Immunol Hung 55:351–361 [View Article][PubMed]
    [Google Scholar]
  21. Etxebeste O., Garzia A., Espeso E. A., Ugalde U. ( 2010). Aspergillus nidulans asexual development: making the most of cellular modules. Trends Microbiol 18:569–576 [View Article][PubMed]
    [Google Scholar]
  22. Foreman P. K., Brown D., Dankmeyer L., Dean R., Diener S., Dunn-Coleman N. S., Goedegebuur F., Houfek T. D., England G. J. & other authors ( 2003). Transcriptional regulation of biomass-degrading enzymes in the filamentous fungus Trichoderma reesei . J Biol Chem 278:31988–31997 [View Article][PubMed]
    [Google Scholar]
  23. François J. M. ( 2007). A simple method for quantitative determination of polysaccharides in fungal cell walls. Nat Protoc 1:2995–3000 [View Article][PubMed]
    [Google Scholar]
  24. Fujiwara M., Ichinomiya M., Motoyama T., Horiuchi H., Ohta A., Takagi M. ( 2000). Evidence that the Aspergillus nidulans class I and class II chitin synthase genes, chsC and chsA, share critical roles in hyphal wall integrity and conidiophore development. J Biochem 127:359–366 [View Article][PubMed]
    [Google Scholar]
  25. 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]
  26. Gastebois A., Fontaine T., Latgé J. P., Mouyna I. ( 2010a). β(1-3)Glucanosyltransferase Gel4p is essential for Aspergillus fumigatus . Eukaryot Cell 9:1294–1298 [View Article][PubMed]
    [Google Scholar]
  27. Gastebois A., Mouyna I., Simenel C., Clavaud C., Coddeville B., Delepierre M., Latgé J. P., Fontaine T. ( 2010b). Characterization of a new β(1-3)-glucan branching activity of Aspergillus fumigatus . J Biol Chem 285:2386–2396 [View Article][PubMed]
    [Google Scholar]
  28. Hamaguchi T., Ito T., Inoue Y., Limpaseni T., Pongsawasdi P., Ito K. ( 2010). Purification, characterization and molecular cloning of a novel endo-β-N-acetylglucosaminidase from the basidiomycete, Flammulina velutipes . Glycobiology 20:420–432 [View Article][PubMed]
    [Google Scholar]
  29. Hartl L., Gastebois A., Aimanianda V., Latgé J. P. ( 2011). Characterization of the GPI-anchored endo β-1,3-glucanase Eng2 of Aspergillus fumigatus . Fungal Genet Biol 48:185–191 [View Article][PubMed]
    [Google Scholar]
  30. Ishida T., Fushinobu S., Kawai R., Kitaoka M., Igarashi K., Samejima M. ( 2009). Crystal structure of glycoside hydrolase family 55 β-1,3-glucanase from the basidiomycete Phanerochaete chrysosporium . J Biol Chem 284:10100–10109 [View Article][PubMed]
    [Google Scholar]
  31. Itoh T., Ochiai A., Mikami B., Hashimoto W., Murata K. ( 2006). A novel glycoside hydrolase family 105: the structure of family 105 unsaturated rhamnogalacturonyl hydrolase complexed with a disaccharide in comparison with family 88 enzyme complexed with the disaccharide. J Mol Biol 360:573–585 [View Article][PubMed]
    [Google Scholar]
  32. Jäger G., Girfoglio M., Dollo F., Rinaldi R., Bongard H., Commandeur U., Fischer R., Spiess A. C., Büchs J. ( 2011). How recombinant swollenin from Kluyveromyces lactis affects cellulosic substrates and accelerates their hydrolysis. Biotechnol Biofuels 4:33 [View Article][PubMed]
    [Google Scholar]
  33. Jaques A. K., Fukamizo T., Hall D., Barton R. C., Escott G. M., Parkinson T., Hitchcock C. A., Adams D. J. ( 2003). Disruption of the gene encoding the ChiB1 chitinase of Aspergillus fumigatus and characterization of a recombinant gene product. Microbiology 149:2931–2939 [View Article][PubMed]
    [Google Scholar]
  34. Jørgensen T. R., Nitsche B. M., Lamers G. E., Arentshorst M., van den Hondel C. A., Ram A. F. ( 2010). Transcriptomic insights into the physiology of Aspergillus niger approaching a specific growth rate of zero. Appl Environ Microbiol 76:5344–5355 [View Article][PubMed]
    [Google Scholar]
  35. Jørgensen T. R., Park J., Arentshorst M., van Welzen A. M., Lamers G., Vankuyk P. A., Damveld R. A., van den Hondel C. A., Nielsen K. F. & other authors ( 2011). The molecular and genetic basis of conidial pigmentation in Aspergillus niger . Fungal Genet Biol 48:544–553 [View Article][PubMed]
    [Google Scholar]
  36. Karlsson M., Stenlid J. ( 2008). Comparative evolutionary histories of the fungal chitinase gene family reveal non-random size expansions and contractions due to adaptive natural selection. Evol Bioinform Online 4:47–60[PubMed]
    [Google Scholar]
  37. Kitagaki H., Wu H., Shimoi H., Ito K. ( 2002). Two homologous genes, DCW1 (YKL046c) and DFG5, are essential for cell growth and encode glycosylphosphatidylinositol (GPI)-anchored membrane proteins required for cell wall biogenesis in Saccharomyces cerevisiae . Mol Microbiol 46:1011–1022 [View Article][PubMed]
    [Google Scholar]
  38. Krijgsheld P., Bleichrodt R., van Veluw G. J., Wang F., Müller W. H., Dijksterhuis J., Wösten H. A. ( 2013). Development in Aspergillus . Stud Mycol 74:1–29 [View Article][PubMed]
    [Google Scholar]
  39. Kuranda M. J., Robbins P. W. ( 1991). Chitinase is required for cell separation during growth of Saccharomyces cerevisiae . J Biol Chem 266:19758–19767[PubMed]
    [Google Scholar]
  40. 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 115–22 [View Article][PubMed]
    [Google Scholar]
  41. Lee J. I., Choi J. H., Park B. C., Park Y. H., Lee M. Y., Park H. M., Maeng P. J. ( 2004). Differential expression of the chitin synthase genes of Aspergillus nidulans, chsA, chsB, and chsC, in response to developmental status and environmental factors. Fungal Genet Biol 41:635–646 [View Article][PubMed]
    [Google Scholar]
  42. Levin A. M., de Vries R. P., Conesa A., de Bekker C., Talon M., Menke H. H., van Peij N. N. M. E., Wösten H. A. B. ( 2007). Spatial differentiation in the vegetative mycelium of Aspergillus niger . Eukaryot Cell 6:2311–2322 [View Article][PubMed]
    [Google Scholar]
  43. Maddi A., Fu C., Free S. J. ( 2012). The Neurospora crassa dfg5 and dcw1 genes encode α-1,6-mannanases that function in the incorporation of glycoproteins into the cell wall. PLoS ONE 7:e38872 [View Article][PubMed]
    [Google Scholar]
  44. Martens-Uzunova E. S., Schaap P. J. ( 2009). Assessment of the pectin degrading enzyme network of Aspergillus niger by functional genomics. Fungal Genet Biol 46:Suppl 1S170–S179 [View Article][PubMed]
    [Google Scholar]
  45. Maubon D., Park S., Tanguy M., Huerre M., Schmitt C., Prévost M. C., Perlin D. S., Latgé J. P., Beauvais A. ( 2006). AGS3, an α(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]
  46. Meyer V., Ram A. F., Punt P. J. ( 2010). Genetics, genetic manipulation and approaches to strain improvement of filamentous fungi. Manual of Industrial Microbiology and Biotechnology, 3rd edn.318–329 Baltz R. H., Demain A. L., Davies J. E. New York: Wiley;
    [Google Scholar]
  47. Meyer V., Wanka F., van Gent J., Arentshorst M., van den Hondel C. A., Ram A. F. ( 2011). Fungal gene expression on demand: an inducible, tunable, and metabolism-independent expression system for Aspergillus niger . Appl Environ Microbiol 77:2975–2983 [View Article][PubMed]
    [Google Scholar]
  48. Mouyna I., Hartland R. P., Fontaine T., Diaquin M., Simenel C., Delepierre M., Henrissat B., Latgé J. P. ( 1998). A 1,3-beta-glucanosyltransferase isolated from the cell wall of Aspergillus fumigatus is a homologue of the yeast Bgl2p. Microbiology 144:3171–3180 [View Article][PubMed]
    [Google Scholar]
  49. Mouyna I., Fontaine T., Vai M., Monod M., Fonzi W. A., Diaquin M., Popolo L., Hartland R. P., Latgé J. P. ( 2000). Glycosylphosphatidylinositol-anchored glucanosyltransferases play an active role in the biosynthesis of the fungal cell wall. J Biol Chem 275:14882–14889 [View Article][PubMed]
    [Google Scholar]
  50. Mouyna I., Morelle W., Vai M., Monod M., Léchenne B., Fontaine T., Beauvais A., Sarfati J., Prévost M. C. & other authors ( 2005). Deletion of GEL2 encoding for a β(1-3)glucanosyltransferase affects morphogenesis and virulence in Aspergillus fumigatus . Mol Microbiol 56:1675–1688 [View Article][PubMed]
    [Google Scholar]
  51. Nitsche B. M., Jørgensen T. R., Akeroyd M., Meyer V., Ram A. F. ( 2012). The carbon starvation response of Aspergillus niger during submerged cultivation: insights from the transcriptome and secretome. BMC Genomics 13:380 [View Article][PubMed]
    [Google Scholar]
  52. Oda K., Kasahara S., Yamagata Y., Abe K., Nakajima T. ( 2002). Cloning and expression of the exo-β-d-1,3-glucanase gene (exgS) from Aspergillus saitoi . Biosci Biotechnol Biochem 66:1587–1590 [View Article][PubMed]
    [Google Scholar]
  53. Pel H. J., de Winde J. H., Archer D. B., Dyer P. S., Hofmann G., Schaap P. J., Turner G., de Vries R. P., Albang R. & other authors ( 2007). Genome sequencing and analysis of the versatile cell factory Aspergillus niger CBS 513.88. Nat Biotechnol 25:221–231 [View Article][PubMed]
    [Google Scholar]
  54. Punt P. J., Oliver R. P., Dingemanse M. A., Pouwels P. H., van den Hondel C. A. ( 1987). Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli . Gene 56:117–124 [View Article][PubMed]
    [Google Scholar]
  55. Pusztahelyi T., Molnár Z., Emri T., Klement E., Miskei M., Kerékgyárto J., Balla J., Pócsi I. ( 2006). Comparative studies of differential expression of chitinolytic enzymes encoded by chiA, chiB, chiC and nagA genes in Aspergillus nidulans . Folia Microbiol (Praha) 51:547–554 [View Article][PubMed]
    [Google Scholar]
  56. Ragni E., Coluccio A., Rolli E., Rodriguez-Peña J. M., Colasante G., Arroyo J., Neiman A. M., Popolo L. ( 2007a). GAS2 and GAS4, a pair of developmentally regulated genes required for spore wall assembly in Saccharomyces cerevisiae . Eukaryot Cell 6:302–316 [View Article][PubMed]
    [Google Scholar]
  57. Ragni E., Fontaine T., Gissi C., Latgè J. P., Popolo L. ( 2007b). The Gas family of proteins of Saccharomyces cerevisiae: characterization and evolutionary analysis. Yeast 24:297–308 [View Article][PubMed]
    [Google Scholar]
  58. Ram A. F., Klis F. M. ( 2006). Identification of fungal cell wall mutants using susceptibility assays based on Calcofluor white and Congo red. Nat Protoc 1:2253–2256 [View Article][PubMed]
    [Google Scholar]
  59. Riou C., Salmon J. M., Vallier M. J., Günata Z., Barre P. ( 1998). Purification, characterization, and substrate specificity of a novel highly glucose-tolerant beta-glucosidase from Aspergillus oryzae . Appl Environ Microbiol 64:3607–3614[PubMed]
    [Google Scholar]
  60. Sambrook J., Frisch E. F., Maniatis T. ( 1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  61. Stals I., Samyn B., Sergeant K., White T., Hoorelbeke K., Coorevits A., Devreese B., Claeyssens M., Piens K. ( 2010). Identification of a gene coding for a deglycosylating enzyme in Hypocrea jecorina . FEMS Microbiol Lett 303:9–17 [View Article][PubMed]
    [Google Scholar]
  62. Stals I., Karkehabadi S., Kim S., Ward M., Van Landschoot A., Devreese B., Sandgren M. ( 2012). High resolution crystal structure of the endo-N-acetyl-β-d-glucosaminidase responsible for the deglycosylation of Hypocrea jecorina cellulases. PLoS ONE 7:e40854 [View Article][PubMed]
    [Google Scholar]
  63. Stolz J., Munro S. ( 2002). The components of the Saccharomyces cerevisiae mannosyltransferase complex M-Pol I have distinct functions in mannan synthesis. J Biol Chem 277:44801–44808 [View Article][PubMed]
    [Google Scholar]
  64. Tamano K., Satoh Y., Ishii T., Terabayashi Y., Ohtaki S., Sano M., Takahashi T., Koyama Y., Mizutani O. & other authors ( 2007). The β-1,3-exoglucanase gene exgA (exg1) of Aspergillus oryzae is required to catabolize extracellular glucan, and is induced in growth on a solid surface. Biosci Biotechnol Biochem 71:926–934 [View Article][PubMed]
    [Google Scholar]
  65. Tjoelker L. W., Gosting L., Frey S., Hunter C. L., Trong H. L., Steiner B., Brammer H., Gray P. W. ( 2000). Structural and functional definition of the human chitinase chitin-binding domain. J Biol Chem 275:514–520 [View Article][PubMed]
    [Google Scholar]
  66. Tusher V. G., Tibshirani R., Chu G. ( 2001). Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98:5116–5121 [View Article][PubMed]
    [Google Scholar]
  67. Ujita M., Sakai K., Hamazaki K., Yoneda M., Isomura S., Hara A. ( 2003). Carbohydrate binding specificity of the recombinant chitin-binding domain of human macrophage chitinase. Biosci Biotechnol Biochem 67:2402–2407 [View Article][PubMed]
    [Google Scholar]
  68. Vaaje-Kolstad G., Horn S. J., van Aalten D. M., Synstad B., Eijsink V. G. ( 2005). The non-catalytic chitin-binding protein CBP21 from Serratia marcescens is essential for chitin degradation. J Biol Chem 280:28492–28497 [View Article][PubMed]
    [Google Scholar]
  69. Vaaje-Kolstad G., Westereng B., Horn S. J., Liu Z., Zhai H., Sørlie M., Eijsink V. G. ( 2010). An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330:219–222 [View Article][PubMed]
    [Google Scholar]
  70. van den Burg H. A., Harrison S. J., Joosten M. H., Vervoort J., de Wit P. J. ( 2006). Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant Microbe Interact 19:1420–1430 [View Article][PubMed]
    [Google Scholar]
  71. van der Kaaij R. M., Yuan X. L., Franken A., Ram A. F., Punt P. J., van der Maarel M. J., Dijkhuizen L. ( 2007). Two novel, putatively cell wall-associated and glycosylphosphatidylinositol-anchored α-glucanotransferase enzymes of Aspergillus niger . Eukaryot Cell 6:1178–1188 [View Article][PubMed]
    [Google Scholar]
  72. van Esse H. P., Bolton M. D., Stergiopoulos I., de Wit P. J., Thomma B. P. ( 2007). The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol Plant Microbe Interact 20:1092–1101 [View Article][PubMed]
    [Google Scholar]
  73. van Gorcom R. F., van den Hondel C. A. ( 1988). Expression analysis vectors for Aspergillus niger . Nucleic Acids Res 16:9052 [View Article][PubMed]
    [Google Scholar]
  74. van Hartingsveldt W., Mattern I. E., van Zeijl C. M. J., Pouwels P. H., van den Hondel C. A. M. J. J. ( 1987). Development of a homologous transformation system for Aspergillus niger based on the pyrG gene. Mol Gen Genet 206:71–75 [View Article][PubMed]
    [Google Scholar]
  75. van Leeuwen M. R., Krijgsheld P., Bleichrodt R., Menke H., Stam H., Stark J., Wösten H. A., Dijksterhuis J. ( 2013). Germination of conidia of Aspergillus niger is accompanied by major changes in RNA profiles. Stud Mycol 74:59–70 [View Article][PubMed]
    [Google Scholar]
  76. van Munster J. M., van der Kaaij R. M., Dijkhuizen L., van der Maarel M. J. E. C. ( 2012). Biochemical characterization of Aspergillus niger CfcI, a glycoside hydrolase family 18 chitinase that releases monomers during substrate hydrolysis. Microbiology 158:2168–2179 [View Article][PubMed]
    [Google Scholar]
  77. Vinck A., de Bekker C., Ossin A., Ohm R. A., de Vries R. P., Wösten H. A. B. ( 2011). Heterogenic expression of genes encoding secreted proteins at the periphery of Aspergillus niger colonies. Environ Microbiol 13:216–225 [View Article][PubMed]
    [Google Scholar]
  78. Wei H., Scherer M., Singh A., Liese R., Fischer R. ( 2001). Aspergillus nidulans α-1,3 glucanase (mutanase), mutA, is expressed during sexual development and mobilizes mutan. Fungal Genet Biol 34:217–227 [View Article][PubMed]
    [Google Scholar]
  79. Yamazaki H., Yamazaki D., Takaya N., Takagi M., Ohta A., Horiuchi H. ( 2007). A chitinase gene, chiB, involved in the autolytic process of Aspergillus nidulans . Curr Genet 51:89–98 [View Article][PubMed]
    [Google Scholar]
  80. Yamazaki H., Tanaka A., Kaneko J., Ohta A., Horiuchi H. ( 2008). Aspergillus nidulans ChiA is a glycosylphosphatidylinositol (GPI)-anchored chitinase specifically localized at polarized growth sites. Fungal Genet Biol 45:963–972 [View Article][PubMed]
    [Google Scholar]
  81. Yuan X. L., van der Kaaij R. M., van den Hondel C. A., Punt P. J., van der Maarel M. J., Dijkhuizen L., Ram A. F. ( 2008). Aspergillus niger genome-wide analysis reveals a large number of novel alpha-glucan acting enzymes with unexpected expression profiles. Mol Genet Genomics 279:545–561 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.067967-0
Loading
/content/journal/micro/10.1099/mic.0.067967-0
Loading

Data & Media loading...

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