More than a repair enzyme: Aspergillus nidulans photolyase-like CryA is a regulator of sexual development

Molecular Biology of the Cell

Volumn 19, Issue 8, 2008, Pages 3254-3262

  Bayram, Özgür ^a   Biesemann, Christoph ^a,c   Krappmann, Sven ^a,d   Galland, Paul ^b   Braus, Gerhard H ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^d UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBODIPYRIMIDINE PHOTOLYASE;

ARTICLE; ASPERGILLUS NIDULANS; CONTROLLED STUDY; CRYA GENE; DNA REPAIR; ESCHERICHIA COLI; FUNGAL GENE; GENE ACTIVITY; GENE DELETION; GENE OVEREXPRESSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTOINHIBITION; PHOTOREACTIVATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SEX DIFFERENTIATION; SEXUAL DEVELOPMENT; TRANSCRIPTION REGULATION; ULTRAVIOLET A RADIATION;

AMINO ACID SEQUENCE; ASPERGILLUS NIDULANS; DEOXYRIBODIPYRIMIDINE PHOTO-LYASE; DNA DAMAGE; DNA REPAIR; FLAVOPROTEINS; GENE DELETION; GENE EXPRESSION REGULATION, FUNGAL; GREEN FLUORESCENT PROTEINS; LIGHT; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; REPRODUCTION; SEQUENCE HOMOLOGY, AMINO ACID;

EMERICELLA NIDULANS; ESCHERICHIA COLI; FUNGI;

EID: 54249127534     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-01-0061     Document Type: Article

References (60)

1. Adams, T. H., Wieser, J. K., and Yu, J. H. (1998). Asexual sporulation in Aspergillus nidulans. Microbiol. Mol. Biol. Rev. 62, 35-54.
2. Ballario, P., Vittorioso, P., Magrelli, A., Talora, C., Cabibbo, A., and Macino, G. (1996). White collar-1, a central regulator of blue light responses in Neurospora, is a zinc finger protein. EMBO J. 15, 1650-1657.
3. Bayram, O., Krappmann, S., Seiler, S., Vogt, N., and Braus, G. H. (2008). Neurospora crassa ve-1 affects asexual conidiation. Fungal Genet. Biol. 45, 127-138.
4. Berrocal-Tito, G. M., Esquivel-Naranjo, E. U., Horwitz, B. A., and Herrera-Estrella, A. (2007). Trichoderma atroviride PHR1, a fungal photolyase responsible for DNA repair, autoregulates its own photoinduction. Eukaryot. Cell 6, 1682-1692.
5. Blumenstein, A., Vienken, K., Tasler, R., Purschwitz, J., Veith, D., Frankenberg-Dinkel, N., and Fischer, R. (2005). The Aspergillus nidulans phytochrome FphA represses sexual development in red light. Curr. Biol. 15, 1833-1838.
6. Braus, G. H., Krappmann, S., and Eckert, S. E. (2002). Sexual development in Ascomycetes-fruit body formation of Aspergillus nidulans. In: Molecular Biology of Fungal Development, Vol. 1, ed. H. D. Osiewacz, New York, Basel: Marcel Dekker, 215-244.
7. Brown, T., and Mackey, K. (1997). Analysis of RNA by Northern and slot blot hybridization. In: Current Protocols in Molecular Biology, New York: John Wiley & Sons, 4.9.1- 4.9.16.
8. Busch, S., Eckert, S. E., Krappmann, S., and Braus, G. H. (2003). The COP9 signalosome is an essential regulator of development in the filamentous fungus Aspergillus nidulans. Mol. Microbiol. 49, 717-730.
9. Corrochano, L. M. (2007). Fungal photoreceptors: sensory molecules for fungal development and behaviour. Photochem. Photobiol. Sci. 6, 725-736.
10. Creevey, C. J., and McInerney, J. O. (2005). Clann: investigating phylogenetic information through supertree analyses. Bioinformatics 21, 390-392.
11. Daiyasu, H., Ishikawa, T., Kuma, K., Iwai, S., Todo, T., and Toh, H. (2004). Identification of cryptochrome DASH from vertebrates. Genes Cells 9, 479-495.
12. Duda, R. O., Hart, P. E., and Stork, D. G. (2001). Pattern Classification, New York: John Wiley & Sons.
13. Dunlap, J. C., and Loros, J. J. (2004). The neurospora circadian system. J. Biol. Rhythms 19, 414-424.
14. Dunlap, J. C., and Loros, J. J. (2006). How fungi keep time: circadian system in Neurospora and other fungi. Curr. Opin. Microbiol. 9, 579-587.
15. Eker, A. P., Yajima, H., and Yasui, A. (1994). DNA photolyase from the fungus Neurospora crassa. Purification, characterization and comparison with other photolyases. Photochem. Photobiol. 60, 125-133.
16. Feinberg, A. P., and Vogelstein, B. (1983). A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6-13.
17. Froehlich, A. C., Liu, Y., Loros, J. J., and Dunlap, J. C. (2002). White Collar-1, a circadian blue light photoreceptor, binding to the frequency promoter. Science 297, 815-819.
18. Galagan, J. E. et al. (2005). Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438, 1105-1115.
19. Greene, A. V., Keller, N., Haas, H., and Bell-Pedersen, D. (2003). A circadian oscillator in Aspergillus spp. regulates daily development and gene expression. Eukaryot. Cell 2, 231-237.
20. Griffin, E. A., Jr., Staknis, D., and Weitz, C. J. (1999). Light-independent role of CRY1 and CRY2 in the mammalian circadian clock. Science 286, 768-771.
21. Guindon, S., and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704.
22. Guo, H., Mockler, T., Duong, H., and Lin, C. (2001). SUB1, an Arabidopsis Ca2+-binding protein involved in cryptochrome and phytochrome coaction. Science 291, 487-490.
23. Han, K. H., Han, K. Y., Yu, J. H., Chae, K. S., Jahng, K. Y., and Han, D. M. (2001). The nsdD gene encodes a putative GATA-type transcription factor necessary for sexual development of Aspergillus nidulans. Mol. Microbiol. 41, 299-309.
24. He, Q., Cheng, P., Yang, Y., Wang, L., Gardner, K. H., and Liu, Y. (2002). White collar-1, a DNA binding transcription factor and a light sensor. Science 297, 840-843.
25. Hitomi, K., Okamoto, K., Daiyasu, H., Miyashita, H., Iwai, S., Toh, H., Ishiura, M., and Todo, T. (2000). Bacterial cryptochrome and photolyase: characterization of two photolyase-like genes of Synechocystis sp. PCC6803. Nucleic Acids Res. 28, 2353-2362.
26. Hofmann, A. F., and Harris, S. D. (2000). The Aspergillus nidulans uvsB gene encodes an ATM-related kinase required for multiple facets of the DNA damage response. Genetics 154, 1577-1586.
27. Idnurm, A., and Heitman, J. (2005). Light controls growth and development via a conserved pathway in the fungal kingdom. PLoS Biol. 3, e95.
28. Idnurm, A., Rodriguez-Romero, J., Corrochano, L. M., Sanz, C., Iturriaga, E. A., Eslava, A. P., and Heitman, J. (2006). The Phycomyces madA gene encodes a blue-light photoreceptor for phototropism and other light responses. Proc. Natl. Acad. Sci. USA 103, 4546-4551.
29. Katoh, K., Kuma, K., Toh, H., and Miyata, T. (2005). MAFFT version 5, improvement in accuracy of multiple sequence alignment. Nucleic Acids Res. 33, 511-518.
30. Kim, H., Han, K., Kim, K., Han, D., Jahng, K., and Chae, K. (2002). The veA gene activates sexual development in Aspergillus nidulans. Fungal Genet Biol. 37, 72-80.
31. Kolar, M., Punt, P. J., van den Hondel, C. A., and Schwab, H. (1988). Transformation of Penicillium chrysogenum using dominant selection markers and expression of an Escherichia coli lacZ fusion gene. Gene 62, 127-134.
32. Krappmann, S., Helmstaedt, K., Gerstberger, T., Eckert, S., Hoffmann, B., Hoppert, M., Schnappauf, G., and Braus, G. H. (1999). The aroC gene of Aspergillus nidulans codes for a monofunctional, allosterically regulated chorismate mutase. J. Biol. Chem. 274, 22275-22282.
33. Krappmann, S., Jung, N., Medic, B., Busch, S., Prade, R. A., and Braus, G. H. (2006). The Aspergillus nidulans F-box protein GrrA links SCF activity to meiosis. Mol. Microbiol. 61, 76-88.
34. Lin, C., and Todo, T. (2005). The cryptochromes. Genome Biol. 6, 220.
35. Linden, H., and Macino, G. (1997). White collar 2, a partner in blue-light signal transduction, controlling expression of light-regulated genes in Neurospora crassa. EMBO J. 16, 98-109.
36. Liu, Y., He, Q., and Cheng, P. (2003). Photoreception in Neurospora: a tale of two White Collar proteins. Cell Mol. Life Sci. 60, 2131-2138.
37. Lu, Y. K., Sun, K. H., and Shen, W. C. (2005). Blue light negatively regulates the sexual filamentation via the Cwc1 and Cwc2 proteins in Cryptococcus neoformans. Mol. Microbiol. 56, 480-491.
38. Mooney, J. L., and Yager, L. N. (1990). Light is required for conidiation in Aspergillus nidulans. Genes Dev. 4, 1473-1482.
39. Muro-Pastor, M. I., Gonzalez, R., Strauss, J., Narendja, F., and Scazzocchio, C. (1999). The GATA factor AreA is essential for chromatin remodelling in a eukaryotic bidirectional promoter. EMBO J. 18, 1584-1597.
40. Notredame, C., Higgins, D. G., and Heringa, J. (2000). T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217.
41. Purschwitz, J., Muller, S., Kastner, C., and Fischer, R. (2006). Seeing the rainbow: light sensing in fungi. Curr. Opin. Microbiol. 9, 566-571.
42. Purschwitz, J., Muller, S., Kastner, C., Schoser, M., Haas, H., Espeso, E. A., Atoui, A., Calvo, A. M., and Fischer, R. (2008). Functional and physical interaction of blue- and red-light sensors in Aspergillus nidulans. Curr. Biol. 18, 255-259.
43. Saiki, R. K., Bugawan, T. L., Horn, G. T., Mullis, K. B., and Erlich, H. A. (1986). Analysis of enzymatically amplified beta-globin and HLA-DQ alpha DNA with allele-specific oligonucleotide probes. Nature 324, 163-166.
44. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, New York: Cold Spring Harbor Laboratory Press.
45. Sancar, A. (1994). Structure and function of DNA photolyase. Biochemistry 33, 2-9.
46. Sancar, A., Smith, F. W., and Sancar, G. B. (1984). Purification of Escherichia coli DNA photolyase. J. Biol. Chem. 259, 6028-6032.
47. Sancar, G. B. (1990). DNA photolyases: physical properties, action mechanism, and roles in dark repair. Mutat. Res. 236, 147-160.
48. Seiler, S., Vogt, N., Ziv, C., Gorovits, R., and Yarden, O. (2006). The STE20/ germinal center kinase POD6 interacts with the NDR kinase COT1 and is involved in polar tip extension in Neurospora crassa. Mol. Biol. Cell 17, 4080-4092.
49. Selby, C. P., and Sancar, A. (2006). A cryptochrome/photolyase class of enzymes with single-stranded DNA-specific photolyase activity. Proc. Natl. Acad. Sci. USA 103, 17696-17700.
50. Shalitin, D., Yang, H., Mockler, T. C., Maymon, M., Guo, H., Whitelam, G. C., and Lin, C. (2002). Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation. Nature 417, 763-767.
51. Shalitin, D., Yu, X., Maymon, M., Mockler, T., and Lin, C. (2003). Blue light-dependent in vivo and in vitro phosphorylation of Arabidopsis cryptochrome 1. Plant Cell 15, 2421-2429.
52. Southern, E. M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98, 503-517.
53. Swofford, D. L. (2003). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods); Sunderland, MA: Sinauer Associates.
54. Thielman, J., Senger, H., and Galland, P. (1991). Action spectra for photosynthetic adaptation in Scenedesmus obliquus. I. Chlorophyll biosynthesis under autotrophic conditions. Planta 183, 334-339.
55. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
56. Trooskens, G., De Beule, D., Decouttere, F., and Van Criekinge, W. (2005). Phylogenetic trees: visualizing, customizing and detecting incongruence. Bioinformatics 21, 3801-3802.
57. Vienken, K., Scherer, M., and Fischer, R. (2005). The Zn(II)2Cys6 putative Aspergillus nidulans transcription factor repressor of sexual development inhibits sexual development under low-carbon conditions and in submersed culture. Genetics 169, 619-630.
58. Vierstra, R. D., and Quail, P. H. (1983a). Photochemistry of 124 kilodalton Avena phytochrome in vitro. Plant Physiol. 72, 264-267.
59. Vierstra, R. D., and Quail, P. H. (1983b). Purification and initial characterization of 124-kilodalton phytochrome from Avena. Biochemistry 22, 2498-2505.
60. 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.