An Aspergillus nidulans bZIP response pathway hardwired for defensive secondary metabolism operates through aflR

Molecular Microbiology

Volumn 83, Issue 5, 2012, Pages 1024-1034

  Yin, Wen Bing ^a   Amaike, Saori ^a   Wohlbach, Dana J ^a   Gasch, Audrey P ^a   Chiang, Yi Ming ^b   Wang, Clay C C ^b   Bok, Jin Woo ^a   Rohlfs, Marko ^c   Keller, Nancy P ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ASPERTHECIN; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; FUNGAL PROTEIN; PROTEIN RSMA; STERIGMATOCYSTIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR C6; UNCLASSIFIED DRUG;

AFLR GENE; ARTICLE; ASPERGILLUS NIDULANS; BINDING SITE; CONTROLLED STUDY; DRUG RESISTANCE; FOLSOMIA CANDIDA; FRUGIVORE; FUNGAL GENE; FUNGAL METABOLISM; FUNGAL STRAIN; GENE OVEREXPRESSION; METABOLIC REGULATION; NONHUMAN; PREDATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RSMA GENE; TOXIN SYNTHESIS; WILD TYPE;

ANIMALS; ASPERGILLUS NIDULANS; BASIC-LEUCINE ZIPPER TRANSCRIPTION FACTORS; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; INSECTS; PROMOTER REGIONS, GENETIC; STERIGMATOCYSTIN; TRANSCRIPTION FACTORS;

EMERICELLA NIDULANS; EUKARYOTA; FOLSOMIA CANDIDA; FUNGI; HEXAPODA;

EID: 84862804476     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.07986.x     Document Type: Article

References (59)

1. Alarco, A.M., and Raymond, M. (1999) The bZip transcription factor Cap1p is involved in multidrug resistance and oxidative stress response in Candida albicans. J Bacteriol 181: 700-708.
2. Asano, Y., Hagiwara, D., Yamashino, T., and 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.
3. Bailey, T.L., and Elkan, C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymer. Proc Int Conf Intell Syst Mol Biol 2: 28-36.
4. Balazs, A., Pocsi, I., Hamari, Z., Leiter, E., Emri, T., Miskei, M., etal. (2010) AtfA bZIP-type transcription factor regulates oxidative and osmotic stress responses in Aspergillus nidulans. Mol Genet Genomics 283: 289-303.
5. Bayram, Ö., and Braus, G.H. (2012) Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol Rev 36: 1-24.
6. Bayram, Ö., Krappmann, S., Ni, M., Bok, J.W., Helmstaedt, K., Valerius, O., etal. (2008) VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320: 1504-1506.
7. Bergmann, S., Schumann, J., Scherlach, K., Lange, C., Brakhage, A.A., and Hertweck, C. (2007) Genomics-driven discovery of PKS-NRPS hybrid metabolites from Aspergillus nidulans. Nat Chem Biol 3: 213-217.
8. Bergmann, S., Funk, A.N., Scherlach, K., Schroeckh, V., Shelest, E., Horn, U., etal. (2010) Activation of a silent fungal polyketide biosynthesis pathway through regulatory cross talk with a cryptic nonribosomal peptide synthetase gene cluster. Appl Environ Microbiol 76: 8143-8149.
9. Bok, J.W., and Keller, N.P. (2004) LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell 3: 527-535.
10. Bok, J.W., Hoffmeister, D., Maggio-Hall, L.A., Murillo, R., Glasner, J.D., and Keller, N.P. (2006) Genomic mining for Aspergillus natural products. Chem Biol 13: 31-37.
11. Bok, J.W., Chiang, Y.M., Szewczyk, E., Reyes-Dominguez, Y., Davidson, A.D., Sanchez, J.F., etal. (2009) Chromatin-level regulation of biosynthetic gene clusters. Nat Chem Biol 5: 462-464.
12. Braus, G.H., Irniger, S., and Bayram, Ö. (2010) Fungal development and the COP9 signalosome. Curr Opin Microbiol 13: 672-676.
13. Brown, D.W., Yu, J.H., Kelkar, H.S., Fernandes, M., Nesbitt, T.C., Keller, N.P., etal. (1996) Twenty-five coregulated transcripts define a ST gene cluster in Aspergillus nidulans. Proc Natl Acad Sci USA 93: 1418-1422.
14. Calvo, A.M., Wilson, R.A., Bok, J.W., and Keller, N.P. (2002) Relationship between secondary metabolism and fungal development. Microbiol Mol Biol Rev 66: 447-459.
15. Chang, P.K. (2003) The Aspergillus parasiticus protein AFLJ interacts with the aflatoxin pathway-specific regulator AFLR. Mol Genet Genomics 268: 711-719.
16. Chang, P.K. (2008) Aspergillus parasiticus crzA, which encodes calcineurin response zinc-finger protein, is required for aflatoxin production under calcium stress. Int J Mol Sci 9: 2027-2043.
17. Chang, P.K., Ehrlich, K.C., Yu, J.J., Bhatnagar, D., and Cleveland, T.E. (1995) Increased expression of Aspergillus parasiticus AflR, encoding a sequence-specific DNA-binding protein, relieves nitrate inhibition of aflatoxin biosynthesis. Appl Environ Microbiol 61: 2372-2377.
18. Chiang, Y.M., Szewczyk, E., Davidson, A.D., Entwistle, R., Keller, N.P., Wang, C.C., etal. (2010) Characterization of the Aspergillus nidulans monodictyphenone gene cluster. Appl Environ Microbiol 76: 2067-2074.
19. Du, W., Obrian, G.R., and Payne, G.A. (2007) Function and regulation of aflJ in the accumulation of aflatoxin early pathway intermediate in Aspergillus flavus. Food Addit Contam 24: 1043-1050.
20. Fernandes, L., Rodrigues-Pousada, C., and Struhl, K. (1997) Yap, a novel family of eight bZIP proteins in Saccharomyces cerevisiae with distinct biological functions. Mol Cell Biol 17: 6982-6993.
21. Fernandes, M., Keller, N.P., and Adams, T.H. (1998) Sequence-specific binding by Aspergillus nidulans AflR, a C6 zinc cluster protein regulating mycotoxin biosynthesis. Mol Microbiol 28: 1355-1365.
22. Gasch, A.P. (2002) Yeast genomic expression studies using DNA microarrays. Methods Enzymol 350: 393-414.
23. Gautier, L., Cope, L., Bolstad, B.M., and Irizarry, R.A. (2004) affy - analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315.
24. Gentleman, R.C., Carey, V.J., Bates, D.M., Bolstad, B., Dettling, M., Dudoit, S., etal. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
25. Gunst, K., Chinnici, J.P., and Llewellyn, G.C. (1982) Effects of aflatoxin B1, aflatoxin B2, aflatoxin G and ST on viability, rates of development, and body length in two strains of Drosophila melanogaster (Diptera). J Invertebr Pathol 39: 388-394.
26. Hagiwara, D., Asano, Y., Yamashino, T., and 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.
27. Keller, N.P., and Hohn, T.M. (1997) Metabolic pathway gene clusters in filamentous fungi. Fungal Genet Biol 21: 17-29.
28. Labrousse, H., and Matile, L. (1996) Toxicological biotest on Diptera larvae to detect ciguatoxins and various other toxic substances. Toxicon 34: 881-891.
29. Lee, S.B., and Taylor, J.W. (1990) Isolation of DNA from fungal mycelia and single spores. In PCR Protocols: A Guide to Methods and Applications. Innis, M.A. (ed.). San Diego, CA: Academic Press, pp. 282-287.
30. Llewellyn, G.C., Gee, C.L., and Sherertz, P.C. (1988) Toxic responses of developing fifth instar milkweed bugs, Oncopeltus fasciatus (Hemiptera), to aflatoxin B1. Bull Environ Contam Toxicol 40: 332-338.
31. McDonald, T., Brown, D., Keller, N.P., and Hammond, T.M. (2005) RNA silencing of mycotoxin production in Aspergillus and Fusarium species. Mol Plant Microbe Interact 18: 539-545.
32. Matasyoh, J.C., Dittrich, B., Schueffler, A., and Laatsch, H. (2011) Larvicidal activity of metabolites from the endophytic Podospora sp. against the malaria vector Anopheles gambiae. Parasitol Res 108: 561-566.
33. Niu, G., Siegel, J., Schuler, M.A., and Berenbaum, M.R. (2009) Comparative toxicity of mycotoxins to navel orangeworm (Amyelois transitella) and corn earworm (Helicoverpa zea). J Chem Ecol 35: 951-957.
34. Pontecorvo, G., Roper, J.A., Hemmons, L.M., Macdonald, K.D., and Bufton, A.W. (1953) The genetics of Aspergillus nidulans. Adv Genet 5: 141-238.
35. Qiao, J.J., Kontoyiannis, D.P., Calderone, R., Li, D., Ma, Y., Wan, Z., etal. (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 cyclophosphamide and triamcinolone. Med Mycol 46: 773-782.
36. Rocco, C.J., Dennison, K.L., Klenchin, V.A., Rayment, I., and Escalante-Semerena, J.C. (2008) Construction and use of new cloning vectors for the rapid isolation of recombinant proteins from Escherichia coli. Plasmid 59: 231-237.
37. Rodrigues-Pousada, C., Menezes, R.A., and Pimentel, C. (2010) The Yap family and its role in stress response. Yeast 27: 245-258.
38. Rohlfs, M., Albert, M., Keller, N.P., and Kempken, F. (2007) Secondary chemicals protect mould from fungivory. Biol Lett 3: 523-525.
39. Roze, L.V., Chanda, A., Wee, J., Awad, D., and Linz, J.E. (2011) Stress-related transcription factor AtfB integrates secondary metabolism with the oxidative stress response in Aspergilli. J Biol Chem 286: 35137-35148.
40. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
41. Schroeckh, V., Scherlach, K., Nützmann, H.W., Shelest, E., Schmidt-Heck, W., Schuemann, J., etal. (2009) Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci USA 106: 14558-14563.
42. Shaaban, M.I., Bok, J.W., Lauer, C., and Keller, N.P. (2010) Suppressor mutagenesis identifies a Velvet complex remediator of Aspergillus nidulans secondary metabolism. Eukaryot Cell 9: 1816-1824.
43. Shimizu, K., and 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.
44. Shwab, E.K., Bok, J.W., Tribus, M., Galehr, J., Graessle, S., and Keller, N.P. (2007) Histone deacetylase activity regulates chemical diversity in Aspergillus. Eukaryot Cell 6: 1656-1664.
45. Smyth, G.K. (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
46. Staaden, S., Milcu, A., Rohlfs, M., and Scheu, S. (2010) Fungal toxins affect the fitness and stable isotope fractionation of Collembola. Soil Biol Biochem 42: 1766-1773.
47. Staaden, S., Milcu, A., Rohlfs, M., and Scheu, S. (2011) Olfactory cues associated with fungal grazing intensity and secondary metabolite pathway modulate Collembola foraging behaviour. Soil Biol Biochem 43: 1411-1416.
48. Storey, J.D., and Tibshirani, R. (2003) Statistical significance for genome wide studies. Proc Natl Acad Sci USA 100: 9440-9445.
49. Szewczyk, E., Chiang, Y.M., Oakley, C.E., Davidson, A.D., Wang, C.C., and Oakley, B.R. (2008) Identification and characterization of the asperthecin gene cluster of Aspergillus nidulans. Appl Environ Microbiol 74: 7607-7612.
50. Trienens, M., and Rohlfs, M. (2011) Experimental evolution of defense against a competitive mold confers reduced sensitivity to fungal toxins but no increased resistance in Drosophila larvae. BMC Evol Biol 11: 206.
51. Trienens, M., and Rohlfs, M. (2012) Insect-fungus interference competition - the potential role of global secondary metabolite regulation, pathway-specific mycotoxin expression and formation of oxylipins. Fungal Ecol (in press). doi: 10.1016/j.funeco.2011.07.009.
52. Trienens, M., Keller, N.P., and Rohlfs, M. (2010) Fruit, flies and filamentous fungi - experimental analysis of animal-microbe competition using Drosophila melanogaster and Aspergillus mould as a model system. Oikos 119: 1765-1775.
53. Tsitsigiannis, D.I., Zarnowski, R., and Keller, N.P. (2004a) The lipid body protein, PpoA, coordinates sexual and asexual sporulation in Aspergillus nidulans. J Biol Chem 279: 11344-11353.
54. Tsitsigiannis, D.I., Kowieski, T.M., Zarnowski, R., and Keller, N.P. (2004b) Lipogenic signals act as developmental regulators of spore balance in Aspergillus nidulans. Eukaryot Cell 3: 1398-1411.
55. Wieser, J., and Adams, T.H. (1995) flbD encodes a myb-like DNA binding protein that controls initiation of Aspergillus nidulans conidiophore development. Genes Dev 9: 491-502.
56. Wilkinson, H.H., Ramaswamy, A., Sim, S.C., and Keller, N.P. (2004) Increased conidiation associated with progression along the sterigmatocystin biosynthetic pathway. Mycologia 96: 1190-1198.
57. Yang, X., Talibi, D., Weber, S., Poisson, G., and Raymond, M. (2001) Functional isolation of the Candida albicans FCR3 gene encoding a bZip transcription factor homologous to Saccharomyces cerevisiae Yap3p. Yeast 30: 1217-1225.
58. Yin, W., and Keller, N.P. (2011) Transcriptional regulatory elements in fungal secondary metabolism. J Microbiol 49: 329-339.
59. Yu, J.H., Hamari, Z., Han, K.H., Seo, J.A., Reyes-Dominguez, Y., and Scazzocchio, C. (2004) Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol 41: 973-981.