1887

Abstract

Carbon starvation is a common stress for micro-organisms both in nature and in industry. The carbon starvation stress response (CSSR) involves the regulation of several important processes including programmed cell death and reproduction of fungi, secondary metabolite production and extracellular hydrolase formation. To gain insight into the physiological events of CSSR, DNA microarray analyses supplemented with real-time RT-PCR (rRT-PCR) experiments on 99 selected genes were performed. These data demonstrated that carbon starvation induced very complex changes in the transcriptome. Several genes contributing to protein synthesis were upregulated together with genes involved in the unfolded protein stress response. The balance between biosynthesis and degradation moved towards degradation in the case of cell wall, carbohydrate, lipid and nitrogen metabolism, which was accompanied by the production of several hydrolytic enzymes and the induction of macroautophagy. These processes provide the cultures with long-term survival by liberating nutrients through degradation of the cell constituents. The induced synthesis of secondary metabolites, antifungal enzymes and proteins as well as bacterial cell wall-degrading enzymes demonstrated that carbon-starving fungi should have marked effects on the micro-organisms in their surroundings. Due to the increased production of extracellular and vacuolar enzymes during carbon starvation, the importance of the endoplasmic reticulum increased considerably.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.062935-0
2013-01-01
2019-10-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/159/1/176.html?itemId=/content/journal/micro/10.1099/mic.0.062935-0&mimeType=html&fmt=ahah

References

  1. Adams T. H. , Boylan M. T. , Timberlake W. E. . ( 1988; ). brlA is necessary and sufficient to direct conidiophore development in Aspergillus nidulans . . Cell 54:, 353–362. [CrossRef] [PubMed]
    [Google Scholar]
  2. 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]
  3. Alfonso C. , Nuero O. M. , Santamaría F. , Reyes F. . ( 1995; ). Purification of a heat-stable chitin deacetylase from Aspergillus nidulans and its role in cell wall degradation. . Curr Microbiol 30:, 49–54. [CrossRef] [PubMed]
    [Google Scholar]
  4. Barratt R. W. , Johnson G. B. , Ogata W. N. . ( 1965; ). Wild-type and mutant stocks of Aspergillus nidulans . . Genetics 52:, 233–246.[PubMed]
    [Google Scholar]
  5. Basten D. E. , Moers A. P. , Ooyen A. J. , Schaap P. J. . ( 2005; ). Characterisation of Aspergillus niger prolyl aminopeptidase. . Mol Genet Genomics 272:, 673–679. [CrossRef] [PubMed]
    [Google Scholar]
  6. 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. [CrossRef] [PubMed]
    [Google Scholar]
  7. Bendtsen J. D. , Nielsen H. , von Heijne G. , Brunak S. . ( 2004; ). Improved prediction of signal peptides: SignalP 3.0. . J Mol Biol 340:, 783–795. [CrossRef] [PubMed]
    [Google Scholar]
  8. Bernardo S. M. , Gray K. A. , Todd R. B. , Cheetham B. F. , Katz M. E. . ( 2007; ). Characterization of regulatory non-catalytic hexokinases in Aspergillus nidulans . . Mol Genet Genomics 277:, 519–532. [CrossRef] [PubMed]
    [Google Scholar]
  9. Birse C. E. , Clutterbuck A. J. . ( 1990; ). N-Acetyl-6-hydroxytryptophan oxidase, a developmentally controlled phenol oxidase from Aspergillus nidulans . . J Gen Microbiol 136:, 1725–1730. [CrossRef] [PubMed]
    [Google Scholar]
  10. Borgia P. T. , Iartchouk N. , Riggle P. J. , Winter K. R. , Koltin Y. , Bulawa C. E. . ( 1996; ). The chsB gene of Aspergillus nidulans is necessary for normal hyphal growth and development. . Fungal Genet Biol 20:, 193–203. [CrossRef] [PubMed]
    [Google Scholar]
  11. Brown D. W. , Adams T. H. , Keller N. P. . ( 1996; ). Aspergillus has distinct fatty acid synthases for primary and secondary metabolism. . Proc Natl Acad Sci U S A 93:, 14873–14877. [CrossRef] [PubMed]
    [Google Scholar]
  12. Bussink H. J. , Osmani S. A. . ( 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] [CrossRef]
    [Google Scholar]
  13. Cebollero E. , Gonzalez R. . ( 2006; ). Induction of autophagy by second-fermentation yeasts during elaboration of sparkling wines. . Appl Environ Microbiol 72:, 4121–4127. [CrossRef] [PubMed]
    [Google Scholar]
  14. Cheng J. , Park T. S. , Chio L. C. , Fischl A. S. , Ye X. S. . ( 2003; ). Induction of apoptosis by sphingoid long-chain bases in Aspergillus nidulans . . Mol Cell Biol 23:, 163–177. [CrossRef] [PubMed]
    [Google Scholar]
  15. Choi C. J. , Ju H. J. , Park B. H. , Qin R. , Jahng K. Y. , Han D. M. , Chae K. S. . ( 2005; ). Isolation and characterization of the Aspergillus nidulans eglC gene encoding a putative β-1,3-endoglucanase. . Fungal Genet Biol 42:, 590–600. [CrossRef] [PubMed]
    [Google Scholar]
  16. Chomczynski P. . ( 1993; ). A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. . Biotechniques 15:, 532–534, 536–537.[PubMed]
    [Google Scholar]
  17. Colabardini A. C. , De Castro P. A. , De Gouvêa P. F. , Savoldi M. , Malavazi I. , Goldman M. H. , Goldman G. H. . ( 2010; ). Involvement of the Aspergillus nidulans protein kinase C with farnesol tolerance is related to the unfolded protein response. . Mol Microbiol 78:, 1259–1279. [CrossRef] [PubMed]
    [Google Scholar]
  18. d’Enfert C. , Fontaine T. . ( 1997; ). Molecular characterization of the Aspergillus nidulans treA gene encoding an acid trehalase required for growth on trehalose. . Mol Microbiol 24:, 203–216. [CrossRef] [PubMed]
    [Google Scholar]
  19. da Silva Ferreira M. E. , Savoldi M. , Sueli Bonato P. , Goldman M. H. , Goldman G. H. . ( 2006; ). Fungal metabolic model for tyrosinemia type 3: molecular characterization of a gene encoding a 4-hydroxy-phenyl pyruvate dioxygenase from Aspergillus nidulans . . Eukaryot Cell 5:, 1441–1445. [CrossRef] [PubMed]
    [Google Scholar]
  20. de Groot P. W. , Brandt B. W. , Horiuchi H. , Ram A. F. , de Koster C. G. , Klis F. M. . ( 2009; ). Comprehensive genomic analysis of cell wall genes in Aspergillus nidulans . . Fungal Genet Biol 46: (Suppl. 1), S72–S81. [CrossRef] [PubMed]
    [Google Scholar]
  21. De Marco J. L. , Felix C. R. . ( 2002; ). Characterization of a protease produced by a Trichoderma harzianum isolate which controls cocoa plant witches’ broom disease. . BMC Biochem 3:, 3. [CrossRef] [PubMed]
    [Google Scholar]
  22. Dinamarco T. M. , Figueiredo Pimentel B. C. , Savoldi M. , Malavazi I. , Soriani F. M. , Uyemura S. A. , Ludovico P. , Goldman M. H. S. , Goldman G. H. . ( 2010; ). The roles played by Aspergillus nidulans apoptosis-inducing factor (AIF)-like mitochondrial oxidoreductase (AifA) and NADH-ubiquinone oxidoreductases (NdeA-B and NdiA) in farnesol resistance. . Fungal Genet Biol 47:, 1055–1069. [CrossRef] [PubMed]
    [Google Scholar]
  23. Dixon D. M. , Szaniszlo P. J. , Polak A. . ( 1991; ). Dihydroxynaphthalene (DHN) melanin and its relationship with virulence in the early stages of phaeohyphomycosis. . In The Fungal Spore and Disease Initiation in Plants and Animals, pp. 297–318. Edited by Cole G. T. , Hoch H. C. . . New York:: Plenum Press;.[CrossRef]
    [Google Scholar]
  24. Eades C. J. , Hintz W. E. . ( 2000; ). Characterization of the class I α-mannosidase gene family in the filamentous fungus Aspergillus nidulans . . Gene 255:, 25–34. [CrossRef] [PubMed]
    [Google Scholar]
  25. Edlayne G. , Simone A. , Felicio J. D. . ( 2009; ). Chemical and biological approaches for mycotoxin control: a review. . Recent Pat Food Nutr Agric 1:, 155–161. [CrossRef] [PubMed]
    [Google Scholar]
  26. Eigentler A. , Pócsi I. , Marx F. . ( 2012; ). The anisin1 gene encodes a defensin-like protein and supports the fitness of Aspergillus nidulans . . Arch Microbiol 194:, 427–437. [CrossRef] [PubMed]
    [Google Scholar]
  27. Elad Y. . ( 2000; ). Biological control of foliar pathogens by means of Trichoderma harzianum and potential modes of action. . Crop Prot 19:, 709–714. [CrossRef]
    [Google Scholar]
  28. Emri T. , Pócsi I. , Szentirmai A. . ( 1999; ). Analysis of the oxidative stress response of Penicillium chrysogenum to menadione. . Free Radic Res 30:, 125–132. [CrossRef] [PubMed]
    [Google Scholar]
  29. Emri T. , Molnár Zs. , Pusztahelyi T. , Pócsi I. . ( 2004; ). Physiological and morphological changes in autolyzing Aspergillus nidulans cultures. . Folia Microbiol (Praha) 49:, 277–284. [CrossRef] [PubMed]
    [Google Scholar]
  30. Emri T. , Molnár Z. , Pócsi I. . ( 2005; ). The appearances of autolytic and apoptotic markers are concomitant but differently regulated in carbon-starving Aspergillus nidulans cultures. . FEMS Microbiol Lett 251:, 297–303. [CrossRef] [PubMed]
    [Google Scholar]
  31. Emri T. , Molnár Zs. , Szilágyi M. , Pócsi I. . ( 2008; ). Regulation of autolysis in Aspergillus nidulans . . Appl Biochem Biotechnol 151:, 211–220. [CrossRef] [PubMed]
    [Google Scholar]
  32. Emri T. , Szilágyi M. , László K. , M-Hamvas M. , Pócsi I. . ( 2009; ). PepJ is a new extracellular proteinase of Aspergillus nidulans . . Folia Microbiol (Praha) 54:, 105–109. [CrossRef] [PubMed]
    [Google Scholar]
  33. 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. [CrossRef] [PubMed]
    [Google Scholar]
  34. Fillinger S. , Chaveroche M. K. , van Dijck P. , de Vries R. , Ruijter G. , Thevelein J. , d’Enfert C. . ( 2001; ). Trehalose is required for the acquisition of tolerance to a variety of stresses in the filamentous fungus Aspergillus nidulans . . Microbiology 147:, 1851–1862.[PubMed]
    [Google Scholar]
  35. Fischer R. , Kües U. . ( 2006; ). Asexual sporulation in mycelial fungi. . In The Mycota, Growth, Differentiation and Sexuality, vol. 1, pp. 263–292. Edited by Fischer R. , Kües U. . . Berlin:: Springer-Verlag;. [CrossRef]
    [Google Scholar]
  36. Fitzgibbon G. J. , Morozov I. Y. , Jones M. G. , Caddick M. X. . ( 2005; ). Genetic analysis of the TOR pathway in Aspergillus nidulans . . Eukaryot Cell 4:, 1595–1598. [CrossRef] [PubMed]
    [Google Scholar]
  37. Flipphi M. , Sun J. , Robellet X. , Karaffa L. , Fekete E. , Zeng A.-P. , Kubiecek C. P. . ( 2009; ). Biodiversity and evolution of primary carbon metabolism in Aspergillus nidulans and other Aspergillus spp. . Fungal Genet Biol 46: (Suppl. 1), S19–S44. [CrossRef] [PubMed]
    [Google Scholar]
  38. Forment J. V. , Flipphi M. , Ramón D. , Ventura L. , Maccabe A. P. . ( 2006; ). Identification of the mstE gene encoding a glucose-inducible, low affinity glucose transporter in Aspergillus nidulans . . J Biol Chem 281:, 8339–8346. [CrossRef] [PubMed]
    [Google Scholar]
  39. Fridovich I. . ( 1998; ). Oxygen toxicity: a radical explanation. . J Exp Biol 201:, 1203–1209.[PubMed]
    [Google Scholar]
  40. Fujioka T. , Mizutani O. , Furukawa K. , Sato N. , Yoshimi A. , Yamagata Y. , Nakajima T. , Abe K. . ( 2007; ). MpkA-dependent and -independent cell wall integrity signaling in Aspergillus nidulans . . Eukaryot Cell 6:, 1497–1510. [CrossRef] [PubMed]
    [Google Scholar]
  41. García-Lepe R. , Nuero O. M. , Reyes F. , Santamaría F. . ( 1997; ). Lipases in autolysed cultures of filamentous fungi. . Lett Appl Microbiol 25:, 127–130. [CrossRef] [PubMed]
    [Google Scholar]
  42. Girardin H. , Paris S. , Rault J. , Bellon-Fontaine M. N. , Latgé J. P. . ( 1999; ). The role of the rodlet structure on the physicochemical properties of Aspergillus conidia. . Lett Appl Microbiol 29:, 364–369. [CrossRef] [PubMed]
    [Google Scholar]
  43. Han K. H. , Seo J. A. , Yu J. H. . ( 2004; ). Regulators of G-protein signalling in Aspergillus nidulans: RgsA downregulates stress response and stimulates asexual sporulation through attenuation of GanB (Gα) signalling. . Mol Microbiol 53:, 529–540. [CrossRef] [PubMed]
    [Google Scholar]
  44. Hansberg W. , de Groot H. , Sies H. . ( 1993; ). Reactive oxygen species associated with cell differentiation in Neurospora crassa . . Free Radic Biol Med 14:, 287–293. [CrossRef] [PubMed]
    [Google Scholar]
  45. Hegedüs N. , Leiter E. , Kovács B. , Tomori V. , Kwon N. J. , Emri T. , Marx F. , Batta G. , Csernoch L. . & other authors ( 2011; ). The small molecular mass antifungal protein of Penicillium chrysogenum – a mechanism of action oriented review. . J Basic Microbiol 51:, 561–571. [CrossRef] [PubMed]
    [Google Scholar]
  46. Horiuchi H. . ( 2009; ). Functional diversity of chitin synthases of Aspergillus nidulans in hyphal growth, conidiophore development and septum formation. . Med Mycol 47: (Suppl. 1), S47–S52. [CrossRef] [PubMed]
    [Google Scholar]
  47. Hortschansky P. , Eisendle M. , Al-Abdallah Q. , Schmidt A. D. , Bergmann S. , Thön M. , Kniemeyer O. , Abt B. , Seeber B. . & other authors ( 2007; ). Interaction of HapX with the CCAAT-binding complex—a novel mechanism of gene regulation by iron. . EMBO J 26:, 3157–3168. [CrossRef] [PubMed]
    [Google Scholar]
  48. Jakubowski W. , Biliński T. , Bartosz G. . ( 2000; ). Oxidative stress during aging of stationary cultures of the yeast Saccharomyces cerevisiae . . Free Radic Biol Med 28:, 659–664. [CrossRef] [PubMed]
    [Google Scholar]
  49. Jayashree T. , Subramanyam C. . ( 2000; ). Oxidative stress as a prerequisite for aflatoxin production by Aspergillus parasiticus . . Free Radic Biol Med 29:, 981–985. [CrossRef] [PubMed]
    [Google Scholar]
  50. Johnstone I. L. , McCabe P. C. , Greaves P. , Gurr S. J. , Cole G. E. , Brow M. A. , Unkles S. E. , Clutterbuck A. J. , Kinghorn J. R. , Innis M. A. . ( 1990; ). Isolation and characterisation of the crnA-niiA-niaD gene cluster for nitrate assimilation in Aspergillus nidulans . . Gene 90:, 181–192. [CrossRef] [PubMed]
    [Google Scholar]
  51. Jorge J. A. , Polizeli M. L. , Thevelein J. M. , Terenzi H. F. . ( 1997; ). Trehalases and trehalose hydrolysis in fungi. . FEMS Microbiol Lett 154:, 165–171. [CrossRef] [PubMed]
    [Google Scholar]
  52. Katz M. E. , Gray K. A. , Cheetham B. F. . ( 2006; ). The Aspergillus nidulans xprG (phoG) gene encodes a putative transcriptional activator involved in the response to nutrient limitation. . Fungal Genet Biol 43:, 190–199. [CrossRef] [PubMed]
    [Google Scholar]
  53. Katz M. E. , Bernardo S. M. , Cheetham B. F. . ( 2008; ). The interaction of induction, repression and starvation in the regulation of extracellular proteases in Aspergillus nidulans: evidence for a role for CreA in the response to carbon starvation. . Curr Genet 54:, 47–55. [CrossRef] [PubMed]
    [Google Scholar]
  54. Kawasaki L. , Aguirre J. . ( 2001; ). Multiple catalase genes are differentially regulated in Aspergillus nidulans . . J Bacteriol 183:, 1434–1440. [CrossRef] [PubMed]
    [Google Scholar]
  55. Kawasaki L. , Wysong D. , Diamond R. , Aguirre J. . ( 1997; ). Two divergent catalase genes are differentially regulated during Aspergillus nidulans development and oxidative stress. . J Bacteriol 179:, 3284–3292.[PubMed]
    [Google Scholar]
  56. Keller N. P. , Turner G. , Bennett J. W. . ( 2005; ). Fungal secondary metabolism – from biochemistry to genomics. . Nat Rev Microbiol 3:, 937–947. [CrossRef] [PubMed]
    [Google Scholar]
  57. Kelly R. , Register E. , Hsu M. J. , Kurtz M. , Nielsen J. . ( 1996; ). Isolation of a gene involved in 1,3-β-glucan synthesis in Aspergillus nidulans and purification of the corresponding protein. . J Bacteriol 178:, 4381–4391.[PubMed]
    [Google Scholar]
  58. Kiel J. A. , van der Klei I. J. . ( 2009; ). Proteins involved in microbody biogenesis and degradation in Aspergillus nidulans . . Fungal Genet Biol 46: (Suppl. 1), S62–S71. [CrossRef] [PubMed]
    [Google Scholar]
  59. Kim S. , Matsuo I. , Ajisaka K. , Nakajima H. , Kitamoto K. . ( 2002; ). Cloning and characterization of the nagA gene that encodes β-N-acetylglucosaminidase from Aspergillus nidulans and its expression in Aspergillus oryzae . . Biosci Biotechnol Biochem 66:, 2168–2175. [CrossRef] [PubMed]
    [Google Scholar]
  60. Kim Y. , Islam N. , Moss B. J. , Nandakumar M. P. , Marten M. R. . ( 2011; ). Autophagy induced by rapamycin and carbon-starvation have distinct proteome profiles in Aspergillus nidulans . . Biotechnol Bioeng 108:, 2705–2715. [CrossRef] [PubMed]
    [Google Scholar]
  61. Klich M. , Mendoza C. , Mullaney E. , Keller N. , Bennett J. W. . ( 2001; ). A new sterigmatocystin-producing Emericella variant from agricultural desert soils. . Syst Appl Microbiol 24:, 131–138. [CrossRef] [PubMed]
    [Google Scholar]
  62. Koibuchi K. , Nagasaki H. , Yuasa A. , Kataoka J. , Kitamoto K. . ( 2000; ). Molecular cloning and characterization of a gene encoding glutaminase from Aspergillus oryzae . . Appl Microbiol Biotechnol 54:, 59–68. [CrossRef] [PubMed]
    [Google Scholar]
  63. Kuo M. J. , Alexander M. . ( 1967; ). Inhibition of the lysis of fungi by melanins. . J Bacteriol 94:, 624–629.[PubMed]
    [Google Scholar]
  64. Lara-Ortíz T. , Riveros-Rosas H. , Aguirre J. . ( 2003; ). Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans . . Mol Microbiol 50:, 1241–1255. [CrossRef] [PubMed]
    [Google Scholar]
  65. Madeo F. , Herker E. , Wissing S. , Jungwirth H. , Eisenberg T. , Fröhlich K. U. . ( 2004; ). Apoptosis in yeast. . Curr Opin Microbiol 7:, 655–660. [CrossRef] [PubMed]
    [Google Scholar]
  66. Molnár Zs. , Mészáros E. , Szilágyi Zs. , Rosén S. , Emri T. , Pócsi I. . ( 2004; ). Influence of fadAG203R and ΔflbA mutations on morphology and physiology of submerged Aspergillus nidulans cultures. . Appl Biochem Biotechnol 118:, 349–360. [CrossRef] [PubMed]
    [Google Scholar]
  67. Molnár Zs. , Emri T. , Zavaczki E. , Pusztahelyi T. , Pócsi I. . ( 2006; ). Effects of mutations in the GanB/RgsA G protein mediated signalling on the autolysis of Aspergillus nidulans . . J Basic Microbiol 46:, 495–503. [CrossRef] [PubMed]
    [Google Scholar]
  68. Mori K. , Kawahara T. , Yoshida H. , Yanagi H. , Yura T. . ( 1996; ). Signalling from endoplasmic reticulum to nucleus: transcription factor with a basic-leucine zipper motif is required for the unfolded protein-response pathway. . Genes Cells 1:, 803–817. [CrossRef] [PubMed]
    [Google Scholar]
  69. Nahlik K. . ( 2007; ). The COP9 signalosome of Aspergillus nidulans: regulation of protein degradation and transcriptional pathways in sexual development. PhD thesis, Georg August University Göttingen.
    [Google Scholar]
  70. Nakamura T. , Maeda Y. , Tanoue N. , Makita T. , Kato M. , Kobayashi T. . ( 2006; ). Expression profile of amylolytic genes in Aspergillus nidulans . . Biosci Biotechnol Biochem 70:, 2363–2370. [CrossRef] [PubMed]
    [Google Scholar]
  71. Navarro R. E. , Stringer M. A. , Hansberg W. , Timberlake W. E. , Aguirre J. . ( 1996; ). catA, a new Aspergillus nidulans gene encoding a developmentally regulated catalase. . Curr Genet 29:, 352–359.[PubMed]
    [Google Scholar]
  72. 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. [CrossRef] [PubMed]
    [Google Scholar]
  73. Oberegger H. , Zadra I. , Schoeser M. , Haas H. . ( 2000; ). Iron starvation leads to increased expression of Cu/Zn-superoxide dismutase in Aspergillus . . FEBS Lett 485:, 113–116. [CrossRef] [PubMed]
    [Google Scholar]
  74. Park B. W. , Han K. H. , Lee C. Y. , Lee C. H. , Maeng P. J. . ( 1997; ). Cloning and characterization of the citA gene encoding the mitochondrial citrate synthase of Aspergillus nidulans . . Mol Cells 7:, 290–295.[PubMed]
    [Google Scholar]
  75. Pateman J. A. , Doy C. H. , Olsen J. E. , Norris U. , Creaser E. H. , Hynes M. . ( 1983; ). Regulation of alcohol dehydrogenase (ADH) and aldehyde dehydrogenase (AldDH) in Aspergillus nidulans . . Proc R Soc Lond B Biol Sci 217:, 243–264. [CrossRef] [PubMed]
    [Google Scholar]
  76. Peña-Montes C. , González A. , Castro-Ochoa D. , Farrés A. . ( 2008; ). Purification and biochemical characterization of a broad substrate specificity thermostable alkaline protease from Aspergillus nidulans . . Appl Microbiol Biotechnol 78:, 603–612. [CrossRef] [PubMed]
    [Google Scholar]
  77. Pócsi I. , Pusztahelyi T. , Sámi L. , Emri T. . ( 2003; ). Autolysis of Penicillium chrysogenum – a holistic approach. . Indian J Biotechnol 2:, 293–301.
    [Google Scholar]
  78. Pócsi I. , Prade R. A. , Penninckx M. J. . ( 2004; ). Glutathione, altruistic metabolite in fungi. . Adv Microb Physiol 49:, 1–76. [CrossRef] [PubMed]
    [Google Scholar]
  79. Pócsi I. , Leiter É. , Kwon N. J. , Shin K. S. , Pusztahelyi T. , Emri T. , Abuknesha R. , Price R. , Yu J. H. . ( 2009; ). Asexual sporulation signalling regulates autolysis of Aspergillus nidulans via modulating the chitinase ChiB production. . J Appl Microbiol 107:, 514–523.[PubMed] [CrossRef]
    [Google Scholar]
  80. Pollack J. K. , Harris S. D. , Marten M. R. . ( 2009; ). Autophagy in filamentous fungi. . Fungal Genet Biol 46:, 1–8. [CrossRef] [PubMed]
    [Google Scholar]
  81. Punt P. J. , Dingemanse M. A. , Jacobs-Meijsing B. J. , Pouwels P. H. , van den Hondel C. A. . ( 1988; ). Isolation and characterization of the glyceraldehyde-3-phosphate dehydrogenase gene of Aspergillus nidulans . . Gene 69:, 49–57. [CrossRef] [PubMed]
    [Google Scholar]
  82. Pusztahelyi T. , Klement E. , Szajli E. , Klem J. , Miskei M. , Karányi Z. , Emri T. , Kovács S. , Orosz G. . & other authors ( 2011; ). Comparison of transcriptional and translational changes caused by long-term menadione exposure in Aspergillus nidulans . . Fungal Genet Biol 48:, 92–103. [CrossRef] [PubMed]
    [Google Scholar]
  83. Read N. D. . ( 2011; ). Exocytosis and growth do not occur only at hyphal tips. . Mol Microbiol 81:, 4–7. [CrossRef] [PubMed]
    [Google Scholar]
  84. Reino J. L. , Guerrero R. F. , Hernández-Galán R. , Collado I. G. . ( 2008; ). Secondary metabolites from species of the biocontrol agent Trichoderma . . Phytochem Rev 7:, 89–123. [CrossRef]
    [Google Scholar]
  85. Reyes F. , Villanueva P. , Alfonso C. . ( 1990; ). Nucleases in the autolysis of filamentous fungi. . FEMS Microbiol Lett 69:, 67–72. [CrossRef] [PubMed]
    [Google Scholar]
  86. Richie D. L. , Hartl L. , Aimanianda V. , Winters M. S. , Fuller K. K. , Miley M. D. , White S. , McCarthy J. W. , Latgé J. P. . & other authors ( 2009; ). A role for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus fumigatus . . PLoS Pathog 5:, e1000258. [CrossRef] [PubMed]
    [Google Scholar]
  87. Robson G. D. . ( 2006; ). Programmed cell death in the aspergilli and other filamentous fungi. . Med Mycol 44: (s1), 109–114. [CrossRef]
    [Google Scholar]
  88. Saloheimo M. , Valkonen M. , Penttilä M. . ( 2003; ). Activation mechanisms of the HAC1-mediated unfolded protein response in filamentous fungi. . Mol Microbiol 47:, 1149–1161. [CrossRef] [PubMed]
    [Google Scholar]
  89. Sámi L. , Emri T. , Pócsi I. . ( 2001; ). Autolysis and aging of Penicillium chrysogenum cultures under carbon starvation: glutathione metabolism and formation of reactive oxygen species. . Mycol Res 105:, 1246–1250. [CrossRef]
    [Google Scholar]
  90. Savoldi M. , Malavazi I. , Soriani F. M. , Capellaro J. L. , Kitamoto K. , da Silva Ferreira M. E. , Goldman M. H. , Goldman G. H. . ( 2008; ). Farnesol induces the transcriptional accumulation of the Aspergillus nidulans apoptosis-inducing factor (AIF)-like mitochondrial oxidoreductase. . Mol Microbiol 70:, 44–59. [CrossRef] [PubMed]
    [Google Scholar]
  91. Schneider T. , Gerrits B. , Gassmann R. , Schmid E. , Gessner M. O. , Richter A. , Battin T. , Eberl L. , Riedel K. . ( 2010; ). Proteome analysis of fungal and bacterial involvement in leaf litter decomposition. . Proteomics 10:, 1819–1830. [CrossRef] [PubMed]
    [Google Scholar]
  92. Semighini C. P. , Savoldi M. , Goldman G. H. , Harris S. D. . ( 2006; ). Functional characterization of the putative Aspergillus nidulans poly(ADP-ribose) polymerase homolog PrpA. . Genetics 173:, 87–98. [CrossRef] [PubMed]
    [Google Scholar]
  93. Sharon A. , Finkelstein A. , Shlezinger N. , Hatam I. . ( 2009; ). Fungal apoptosis: function, genes and gene function. . FEMS Microbiol Rev 33:, 833–854. [CrossRef] [PubMed]
    [Google Scholar]
  94. Skromne I. , Sánchez O. , Aguirre J. . ( 1995; ). Starvation stress modulates the expression of the Aspergillus nidulans brlA regulatory gene. . Microbiology 141:, 21–28. [CrossRef] [PubMed]
    [Google Scholar]
  95. Stinnett S. M. , Espeso E. A. , Cobeño L. , Araújo-Bazán L. , Calvo A. M. . ( 2007; ). Aspergillus nidulans VeA subcellular localization is dependent on the importin α carrier and on light. . Mol Microbiol 63:, 242–255. [CrossRef] [PubMed]
    [Google Scholar]
  96. Stringer M. A. , Dean R. A. , Sewall T. C. , Timberlake W. E. . ( 1991; ). Rodletless, a new Aspergillus developmental mutant induced by directed gene inactivation. . Genes Dev 5:, 1161–1171. [CrossRef] [PubMed]
    [Google Scholar]
  97. Suzuki Y. , Murray S. L. , Wong K. H. , Davis M. A. , Hynes M. J. . ( 2012; ). Reprogramming of carbon metabolism by the transcriptional activators AcuK and AcuM in Aspergillus nidulans . . Mol Microbiol 84:, 942–964. [CrossRef] [PubMed]
    [Google Scholar]
  98. Szilágyi M. , Kwon N. J. , Dorogi C. , Pócsi I. , Yu J. H. , Emri T. . ( 2010; ). The extracellular β-1,3-endoglucanase EngA is involved in autolysis of Aspergillus nidulans . . J Appl Microbiol 109:, 1498–1508.[PubMed]
    [Google Scholar]
  99. Szilágyi M. , Kwon N. J. , Bakti F. , M-Hamvas M. , Jámbrik K. , Park H. , Pócsi I. , Yu J. H. , Emri T. . ( 2011; ). Extracellular proteinase formation in carbon starving Aspergillus nidulans cultures – physiological function and regulation. . J Basic Microbiol 51:, 625–634. [CrossRef] [PubMed]
    [Google Scholar]
  100. Szilágyi M. , Anton F. , Forgács K. , Yu J. H. , Pócsi I. , Emri T. . ( 2012; ). Antifungal activity of extracellular hydrolases produced by autolysing Aspergillus nidulans cultures. . J Microbiol 50:, 849–854. [CrossRef] [PubMed]
    [Google Scholar]
  101. Terabayashi Y. , Shimizu M. , Kitazume T. , Masuo S. , Fujii T. , Takaya N. . ( 2012; ). Conserved and specific responses to hypoxia in Aspergillus oryzae and Aspergillus nidulans determined by comparative transcriptomics. . Appl Microbiol Biotechnol 93:, 305–317. [CrossRef] [PubMed]
    [Google Scholar]
  102. von Döhren H. . ( 2009; ). A survey of nonribosomal peptide synthetase (NRPS) genes in Aspergillus nidulans . . Fungal Genet Biol 46: (Suppl. 1), S45–S52. [CrossRef] [PubMed]
    [Google Scholar]
  103. Wang Y. , Song J. Z. , Yang Q. , Liu Z. H. , Huang X. M. , Chen Y. . ( 2010; ). Cloning of a heat-stable chitin deacetylase gene from Aspergillus nidulans and its functional expression in Escherichia coli . . Appl Biochem Biotechnol 162:, 843–854. [CrossRef] [PubMed]
    [Google Scholar]
  104. 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. [CrossRef] [PubMed]
    [Google Scholar]
  105. Wei H. , Vienken K. , Weber R. , Bunting S. , Requena N. , Fischer R. . ( 2004; ). A putative high affinity hexose transporter, hxtA, of Aspergillus nidulans is induced in vegetative hyphae upon starvation and in ascogenous hyphae during cleistothecium formation. . Fungal Genet Biol 41:, 148–156. [CrossRef] [PubMed]
    [Google Scholar]
  106. White S. , McIntyre M. , Berry D. R. , McNeil B. . ( 2002; ). The autolysis of industrial filamentous fungi. . Crit Rev Biotechnol 22:, 1–14. [CrossRef] [PubMed]
    [Google Scholar]
  107. Winderickx J. , Holsbeeks I. , Lagatie O. , Giots F. , Thevelein J. , de Winde H. . ( 2003; ). From feast to famine; adaptation to nutrient availability in yeast. . Top Curr Genet 1:, 305–386. [CrossRef]
    [Google Scholar]
  108. 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. [CrossRef] [PubMed]
    [Google Scholar]
  109. Yang Z. , Huang J. , Geng J. , Nair U. , Klionsky D. J. . ( 2006; ). Atg22 recycles amino acids to link the degradative and recycling functions of autophagy. . Mol Biol Cell 17:, 5094–5104. [CrossRef] [PubMed]
    [Google Scholar]
  110. Yu J. H. , Butchko R. A. , Fernandes M. , Keller N. P. , Leonard T. J. , Adams T. H. . ( 1996; ). Conservation of structure and function of the aflatoxin regulatory gene aflR from Aspergillus nidulans and A. flavus . . Curr Genet 29:, 549–555. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.062935-0
Loading
/content/journal/micro/10.1099/mic.0.062935-0
Loading

Data & Media loading...

Supplements

Table S1 and legend for Table S2 

PDF

Table S2 

EXCEL
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