1887

Abstract

The eukaryotic basic leucine zipper (bZIP) transcription factors play critical roles in the organismal response to the environment. Recently, a novel YAP-like bZIP, restorer of secondary metabolism A (RsmA), was found in a suppressor screen of an secondary metabolism (SM) mutant in which overexpression of was found to partially remediate loss of SM in Velvet Complex mutants. The Velvet Complex is a conserved fungal transcriptional heteromer that couples SM with sexual development in fungi. Here we characterized and contrasted SM in mutants of RsmA and four other bZIP proteins (NapA, ZipA, ZipB and ZipC) with predicted DNA binding motifs similar to RsmA. Only two overexpression mutants exhibited both SM and sexual abnormalities that were noteworthy:  : :  resulted in a 100-fold increase in sterigmatocystin and a near loss of meiotic spore production.  : :  displayed decreased production of sterigmatocystin, emericellin, asperthecin, shamixanthone and epishamixanthone, coupled with a shift from sexual to asexual development. Quantification of bZIP homodimer and heterodimer formation using fluorescence resonance energy transfer (FRET) suggested that these proteins preferentially self-associate.

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2013-01-01
2019-10-19
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References

  1. Asano Y., Hagiwara D., Yamashino T., Mizuno T.. ( 2007;). Characterization of the bZip-type transcription factor NapA with reference to oxidative stress response in Aspergillus nidulans. . Biosci Biotechnol Biochem 71:, 1800–1803. [CrossRef][PubMed]
    [Google Scholar]
  2. Ashenberg O., Rozen-Gagnon K., Laub M. T., Keating A. E.. ( 2011;). Determinants of homodimerization specificity in histidine kinases. . J Mol Biol 413:, 222–235. [CrossRef][PubMed]
    [Google Scholar]
  3. Balázs A., Pócsi I., Hamari Z., Leiter E., Emri T., Miskei M., Oláh J., Tóth V., Hegedűs N.. & other authors ( 2010;). AtfA bZIP-type transcription factor regulates oxidative and osmotic stress responses in Aspergillus nidulans. . Mol Genet Genomics 283:, 289–303. [CrossRef][PubMed]
    [Google Scholar]
  4. Bayram O., Braus G. H.. ( 2012;). Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. . FEMS Microbiol Rev 36:, 1–24. [CrossRef][PubMed]
    [Google Scholar]
  5. Bayram O., Krappmann S., Ni M., Bok J. W., Helmstaedt K., Valerius O., Braus-Stromeyer S., Kwon N. J., Keller N. P.. & other authors ( 2008;). VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. . Science 320:, 1504–1506. [CrossRef][PubMed]
    [Google Scholar]
  6. Bok J. W., Keller N. P.. ( 2004;). LaeA, a regulator of secondary metabolism in Aspergillus spp. . Eukaryot Cell 3:, 527–535. [CrossRef][PubMed]
    [Google Scholar]
  7. Bok J. W., Keller N. P.. ( 2012;). Fast and Easy Method for Construction of Plasmid Vectors Using Modified Quick-Change Mutagenesis. Humana Press;. [CrossRef]
    [Google Scholar]
  8. Bok J. W., Hoffmeister D., Maggio-Hall L. A., Murillo R., Glasner J. D., Keller N. P.. ( 2006;). Genomic mining for Aspergillus natural products. . Chem Biol 13:, 31–37. [CrossRef][PubMed]
    [Google Scholar]
  9. Bok J. W., Chiang Y.-M., Szewczyk E., Reyes-Dominguez Y., Davidson A. D., Sanchez J. F., Lo H.-C., Watanabe K., Strauss J.. & other authors ( 2009;). Chromatin-level regulation of biosynthetic gene clusters. . Nat Chem Biol 5:, 462–464. [CrossRef][PubMed]
    [Google Scholar]
  10. Chiu D. T., Stults F. H., Tappel A. L.. ( 1976;). Purification and properties of rat lung soluble glutathione peroxidase. . Biochim Biophys Acta 445:, 558–566. [CrossRef][PubMed]
    [Google Scholar]
  11. Cho J. H., Yun S. S., Jang Y. K., Cha M. J., Kwon N. J., Chae S. K.. ( 2003;). Identification and cloning of jipA encoding a polypeptide that interacts with a homolog of yeast Rad6, UVSJ in Aspergillus nidulans. . J Microbiol 41:, 46–51.
    [Google Scholar]
  12. 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]
  13. Emri T., Pócsi I., Szentirmai A.. ( 1997;). Glutathione metabolism and protection against oxidative stress caused by peroxides in Penicillium chrysogenum. . Free Radic Biol Med 23:, 809–814. [CrossRef][PubMed]
    [Google Scholar]
  14. 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]
  15. Ferguson H. A., Goodrich J. A.. ( 2001;). Expression and purification of recombinant human c-Fos/c-Jun that is highly active in DNA binding and transcriptional activation in vitro. . Nucleic Acids Res 29:, e98. [CrossRef][PubMed]
    [Google Scholar]
  16. Gunst K., Chinnici J. P., Llewellyn G. C.. ( 1982;). Effects of aflatoxin B, aflatoxin B, aflatoxin G and sterigmatocystin on viability, rates of development, and body length in two strains of Drosophila melanogaster (Diptera). . J Invertebr Pathol 39:, 388–394. [CrossRef][PubMed]
    [Google Scholar]
  17. Guo M., Chen Y., Du Y., Dong Y., Guo W., Zhai S., Zhang H., Dong S., Zhang Z.. & other authors ( 2011;). The bZIP transcription factor MoAP1 mediates the oxidative stress response and is critical for pathogenicity of the rice blast fungus Magnaporthe oryzae. . PLoS Pathog 7:, e1001302. [CrossRef][PubMed]
    [Google Scholar]
  18. Hagiwara D., Asano Y., Marui J., Furukawa K., Kanamaru K., Kato M., Abe K., Kobayashi T., Yamashino T., Mizuno T.. ( 2007;). The SskA and SrrA response regulators are implicated in oxidative stress responses of hyphae and asexual spores in the phosphorelay signaling network of Aspergillus nidulans. . Biosci Biotechnol Biochem 71:, 1003–1014. [CrossRef][PubMed]
    [Google Scholar]
  19. Hagiwara D., Asano Y., Yamashino T., Mizuno T.. ( 2008;). Characterization of bZip-type transcription factor AtfA with reference to stress responses of conidia of Aspergillus nidulans. . Biosci Biotechnol Biochem 72:, 2756–2760. [CrossRef][PubMed]
    [Google Scholar]
  20. Halliwell B., Gutteridge J. M. C.. ( 2007;). Chapter 5. Measurement of Reactive Species. . In Free Radicals in Biology and Medicine, , 4th edn., pp. 268–330. Oxford:: Oxford University Press;.
    [Google Scholar]
  21. Jayashree T., Subramanyam C.. ( 1999;). Antiaflatoxigenic activity of eugenol is due to inhibition of lipid peroxidation. . Lett Appl Microbiol 28:, 179–183. [CrossRef][PubMed]
    [Google Scholar]
  22. 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]
  23. 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]
  24. Lee J., Myong K., Kim J. E., Kim H. K., Yun S. H., Lee Y. W.. ( 2012;). FgVelB globally regulates sexual reproduction, mycotoxin production and pathogenicity in the cereal pathogen Fusarium graminearum. . Microbiology 158:, 1723–1733. [CrossRef][PubMed]
    [Google Scholar]
  25. Lessing F., Kniemeyer O., Wozniok I., Loeffler J., Kurzai O., Haertl A., Brakhage A. A.. ( 2007;). The Aspergillus fumigatus transcriptional regulator AfYap1 represents the major regulator for defense against reactive oxygen intermediates but is dispensable for pathogenicity in an intranasal mouse infection model. . Eukaryot Cell 6:, 2290–2302. [CrossRef][PubMed]
    [Google Scholar]
  26. Li M. Z., Elledge S. J.. ( 2007;). Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC. . Nat Methods 4:, 251–256. [CrossRef][PubMed]
    [Google Scholar]
  27. Matasyoh J. C., Dittrich B., Schueffler A., Laatsch H.. ( 2011;). Larvicidal activity of metabolites from the endophytic Podospora sp. against the malaria vector Anopheles gambiae. . Parasitol Res 108:, 561–566. [CrossRef][PubMed]
    [Google Scholar]
  28. Moye-Rowley W. S., Harshman K. D., Parker C. S.. ( 1989;). Yeast YAP1 encodes a novel form of the jun family of transcriptional activator proteins. . Genes Dev 3:, 283–292. [CrossRef][PubMed]
    [Google Scholar]
  29. Pontecorvo G., Roper J. A., Chemmons L. M., MacDonald K. D., Bufton A. W.. ( 1953;). The genetics of Aspergillus nidulans. . Adv Genet 5:, 141–238. [CrossRef][PubMed]
    [Google Scholar]
  30. Qiao J., Kontoyiannis D. P., Calderone R., Li D., Ma Y., Wan Z., Li R., Liu W.. ( 2008;). Afyap1, encoding a bZip transcriptional factor of Aspergillus fumigatus, contributes to oxidative stress response but is not essential to the virulence of this pathogen in mice immunosuppressed by cyclopthosphamide and triamcinolone. . Med Mycol 46:, 773–782. [CrossRef][PubMed]
    [Google Scholar]
  31. Reverberi M., Zjalic S., Punelli F., Ricelli A., Fabbri A. A., Fanelli C.. ( 2007;). Apyap1 affects aflatoxin biosynthesis during Aspergillus parasiticus growth in maize seeds. . Food Addit Contam 24:, 1070–1075. [CrossRef][PubMed]
    [Google Scholar]
  32. Reverberi M., Zjalic S., Ricelli A., Punelli F., Camera E., Fabbri C., Picardo M., Fanelli C., Fabbri A. A.. ( 2008;). Modulation of antioxidant defense in Aspergillus parasiticus is involved in aflatoxin biosynthesis: a role for the ApyapA gene. . Eukaryot Cell 7:, 988–1000. [CrossRef][PubMed]
    [Google Scholar]
  33. Reverberi M., Gazzetti K., Punelli F., Scarpari M., Zjalic S., Ricelli A., Fabbri A. A., Fanelli C.. ( 2012;). Aoyap1 regulates OTA synthesis by controlling cell redox balance in Aspergillus ochraceus. . Appl Microbiol Biotechnol 95:, 1293–1304. [CrossRef][PubMed]
    [Google Scholar]
  34. Rodrigues-Pousada C., Menezes R. A., Pimentel C.. ( 2010;). The Yap family and its role in stress response. . Yeast 27:, 245–258. [CrossRef][PubMed]
    [Google Scholar]
  35. Roggenkamp R., Sahm H., Wagner F.. ( 1974;). Microbial assimilation of methanol induction and function of catalase in Candida boidinii. . FEBS Lett 41:, 283–286. [CrossRef][PubMed]
    [Google Scholar]
  36. Roze L. V., Chanda A., Wee J., Awad D., Linz J. E.. ( 2011;). Stress-related transcription factor AtfB integrates secondary metabolism with oxidative stress response in aspergilli. . J Biol Chem 286:, 35137–35148. [CrossRef][PubMed]
    [Google Scholar]
  37. Sakamoto K., Iwashita K., Yamada O., Kobayashi K., Mizuno A., Akita O., Mikami S., Shimoi H., Gomi K.. ( 2009;). Aspergillus oryzae atfA controls conidial germination and stress tolerance. . Fungal Genet Biol 46:, 887–897. [CrossRef][PubMed]
    [Google Scholar]
  38. Sambrook J., Fritsch E. F., Maniatis T.. ( 1989;). Molecular Cloning: a Laboratory Manual, , 2nd edn.. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  39. Shaaban M. I., Bok J. W., Lauer C., Keller N. P.. ( 2010;). Suppressor mutagenesis identifies a velvet complex remediator of Aspergillus nidulans secondary metabolism. . Eukaryot Cell 9:, 1816–1824. [CrossRef][PubMed]
    [Google Scholar]
  40. Shimizu K., Keller N. P.. ( 2001;). Genetic involvement of a cAMP-dependent protein kinase in a G protein signaling pathway regulating morphological and chemical transitions in Aspergillus nidulans. . Genetics 157:, 591–600.[PubMed]
    [Google Scholar]
  41. Shwab E. K., Bok J. W., Tribus M., Galehr J., Graessle S., Keller N. P.. ( 2007;). Histone deacetylase activity regulates chemical diversity in Aspergillus. . Eukaryot Cell 6:, 1656–1664. [CrossRef][PubMed]
    [Google Scholar]
  42. Thön M., Al Abdallah Q., Hortschansky P., Scharf D. H., Eisendle M., Haas H., Brakhage A. A.. ( 2010;). The CCAAT-binding complex coordinates the oxidative stress response in eukaryotes. . Nucleic Acids Res 38:, 1098–1113. [CrossRef][PubMed]
    [Google Scholar]
  43. Tian C., Li J., Glass N. L.. ( 2011;). Exploring the bZIP transcription factor regulatory network in Neurospora crassa. . Microbiology 157:, 747–759. [CrossRef][PubMed]
    [Google Scholar]
  44. Tsitsigiannis D. I., Kowieski T. M., Zarnowski R., Keller N. P.. ( 2004a;). Endogenous lipogenic regulators of spore balance in Aspergillus nidulans. . Eukaryot Cell 3:, 1398–1411. [CrossRef][PubMed]
    [Google Scholar]
  45. Tsitsigiannis D. I., Zarnowski R., Keller N. P.. ( 2004b;). The lipid body protein, PpoA, coordinates sexual and asexual sporulation in Aspergillus nidulans. . J Biol Chem 279:, 11344–11353. [CrossRef][PubMed]
    [Google Scholar]
  46. Vinson C., Acharya A., Taparowsky E. J.. ( 2006;). Deciphering B-ZIP transcription factor interactions in vitro and in vivo. . Biochim Biophys Acta 1759:, 4–12. [CrossRef][PubMed]
    [Google Scholar]
  47. Yin W. B., Amaike S., Wohlbach D. J., Gasch A. P., Chiang Y. M., Wang C. C., Bok J. W., Rohlfs M., Keller N. P.. ( 2012;). An Aspergillus nidulans bZIP response pathway hardwired for defensive secondary metabolism operates through aflR. . Mol Microbiol 83:, 1024–1034. [CrossRef][PubMed]
    [Google Scholar]
  48. Yu J. H., Hamari Z., Han K. H., Seo J. A., Reyes-Domínguez Y., Scazzocchio C.. ( 2004;). Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. . Fungal Genet Biol 41:, 973–981. [CrossRef][PubMed]
    [Google Scholar]
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