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Molecular Genetics of Emericella nidulans Sexual Development

  • Han, Kap-Hoon (Department of Pharmaceutical Engineering, Woosuk University)
  • Published : 2009.09.30

Abstract

Many aspergilli that belongs to ascomycetes have sexuality. In a homothallic or self-fertile fungus, a number of fruiting bodies or cleistothecia are formed in a thallus grown from a single haploid conidia or ascospores. Genome-sequencing project revealed that two mating genes (MAT) encoding the regulatory proteins that are necessary for controlling partner recognition in heterothallic fungi were conserved in most aspergilli. The MAT gene products in some self-fertile species were not required for recognition of mating partner at pheromone-signaling stage but required at later stages of sexual development. Various environmental factors such as nutritional status, culture conditions and several stresses, influence the decision or progression of sexual reproduction. A large number of genes are expected to be involved in sexual development of Emericella nidulans (anamorph: Aspergillus nidulans), a genetic and biological model organism in aspergilli. The sexual development process can be grouped into several development stages, including the decision of sexual reproductive cycle, mating process, growth of fruiting body, karyogamy followed by meiosis, and sporulation process. Complicated regulatory networks, such as signal transduction pathways and gene expression controls, may work in each stage and stage-to-stage linkages. In this review, the components joining in the regulatory pathways of sexual development, although they constitute only a small part of the whole regulatory networks, are briefly mentioned. Some of them control sexual development positively and some do negatively. Regarding the difficulties for studying sexual differentiation compare to asexual one, recent progresses in molecular genetics of E. nidulans enlarge the boundaries of understanding sexual development in the non-fertile species as well as in fertile fungi.

Keywords

References

  1. Axelrod, D.E., Gealt, M. and Pastushok, M. 1973. Gene control of dovelopmental competence in Aspergillus nidulans. Dev. Biol. 34:9-15 https://doi.org/10.1016/0012-1606(73)90335-7
  2. Blumenstein, A., Vienken, K., Tasler, R., Purschwitz, J., Veith, D., Frankenbergdinkel, N. and Fischer, R. 2005. The phytochrome FphA represses sexual development in red light. Curr. Biol. 15:1833-1838 https://doi.org/10.1016/j.cub.2005.08.061
  3. 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, pp.215-244.Ed.H.D.Osiewacz,CRC Press, Boca Raton,FL
  4. Busby, T.M., Miller, K.Y. and Miller, B.L. 1996. Suppression and enhancement of the Aspergillus nidulans medusa mutationby altered dosage of the bristle and stunted genes. Genetics 143:155-163
  5. Busch, S., Eckert, S.E., Krappmann, S. and Braus, G.H. 2003. The COP9 signalosome is an essential regulator of develop- ment in the filamentous fungus Aspergillus nidulans. Mol.Microbiol. 49:717-730 https://doi.org/10.1046/j.1365-2958.2003.03612.x
  6. Calvo, A.M., Bok, J., Brooks, W. and keller,. N.P. 2004.veA is required for toxin and sclerotial production in Aspergillus parasiticus. Appl. Environ. Microbiol. 70:4733-4739. https://doi.org/10.1128/AEM.70.8.4733-4739.2004
  7. Cary, J.W., GR, 0.B., Nielsen, D.M., Nierman, W., Harris-Coward, P., Yu, J., Bhatnagar, D., Cleveland, T.E., Payne, G.A. and calvo, A.M. 2007. Elucidation of veA-dependent genes associated with aflatoxin and sclerotial production in Aspergillus Flavus by functional genomics. Appl. microbiol. Biotechnol. 76:1107-1118 https://doi.org/10.1007/s00253-007-1081-y
  8. Champe, S.P., Kurtz, M.B., Yager, L.N., Butnick, N.J. and Axelrod, D.E. 1981. Spore formation in Aspergillus nidulans:competence and other developmental processes. In: The fungal spore: morphogenetic controls, pp. 63-91. Eds. G. Turian and H.R. Hohl, Academic Press, New York, NY
  9. Champe, S.P., Nagle, D.L. and Yager, L.N. 1994. Sexual sporu1ation. In: Aspergillus: 50 Years On, Progress in lndustrial Microbiology, pp. 429-454. Eds. S. D. Martinelli and J.R. Kinghorn, Elsevier, Amsterdam
  10. Clutterbuck, A.J. 1969. A mutational analysis of conidial development in Aspergillus nidulans. Genetics 63:317-327
  11. Durna, R.M., Cary, J.W. and Calvo, A.M. 2007. Production of cyclopiazonic acid, aflatrem, and aflatoxin by Aspergillus flavus is regulated by veA, a gene necessary for sclerotial formation. Appl. Microbiol. Biotechnol. 73:1158-1168. https://doi.org/10.1007/s00253-006-0581-5
  12. Dutton, J.R., Johns, S. and Miller, B.L. 1997. StuAp is a sequence-specific transcription factor that regulates develop-mental complexity in Aspergillus nidulans. EMBO J. 16:5710-5721 https://doi.org/10.1093/emboj/16.18.5710
  13. Eckert, S.E., Hoffmann, B., Wanke, C. and Braus, G.H. 1999. Sexual development of Aspergillus nidulans in tiuptophan auxotrophic strains. Arch. Microbiol. 172:157-166 https://doi.org/10.1007/s002030050755
  14. Galagan, J.E., Calvo, S.E., Cuomo, C., Ma, L.J., Wortman, J.R., Batzoglou, S., Lee,S.I., Basturkmen, M., Spevak, C.C., Clutterbuck, J., et al. 2005. Sequencing of Aspergillus nidulans and comparaive analysis with A. fumigatus and A oryzae.Nature 438:1105-1115 https://doi.org/10.1038/nature04341
  15. Galbraith, J.C. and Smith, J.E. 1969. Sporulation of Aspergillus niger in submerged liquid culture. J. Gen. Microbiol. 59:31-45
  16. Glass, N.L. and Lorimer, I. 1991. Ascomycete mating types. In: More Gene Nanipulations in Fungi, pp. 193-216. Eds. J. W. Bennett and L.S.Lasure, Academic Press, San Diego, CA
  17. Han, D.M., Han, Y.J., Chae, K.S., Jahng, K.Y. and Lee, Y,H. 1994a. Effects of various carbon sources on the development of Aspergillus nidulans Wiht velA or velA1 allele. Korean J. Mycol. 22:332-337
  18. Han, D.M., Han, Y,J., Kim, J.H., Jahng, K.Y., Chung, Y,S., Chung, J.H. and Chae, K.S. 1994b. Isolation and characterization of NSD mutants in Aspergillus nidulans. Korean J.Mycol. 22:1-7
  19. Han, D.M., Han, Y.J., Lee, Y,H., Jahng, K.Y., Jahng, S.H. and Chae, K.S. 1990. Inhibitory conditions of sexual development and their application for the screening of mutants defective in sexual development. Korean J. Mycol. 18:225-232
  20. Han, K.H., Cheong, S.S., Hoe, H.S. and Han, D.M. 1998. Characterization of several NSD mutants of Aspergillus nidulansthat never undergo sexual development. Korean J. Genet.20:257-264
  21. Han, K.H., Han, K.Y., Kim, H.S., Lee, D.B., Kim, J.H., Chae, S.K., Chae, K.S. and Han, D.M. 2003a. Regulation of nsdD expression in Aspergillus nidulans. J. microbiol. 41:259-261
  22. 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 https://doi.org/10.1046/j.1365-2958.2001.02472.x
  23. Han, K.H., Lee, D.B., Kim, J.H., Kim, M.S., Han, K.Y., Kim, W.S., Park, Y.S., Kim, H.B. and Han, D.M. 2003b. Environ-mental factors affecting development of Aspergillus nidulans. J. Microbiol. 41:34-40
  24. Han, K.H. and Prade, R.A. 2002. Osmotics stress-coupled maintenance of polar growth in Aspergillus nidulans. Mol. Microbiol. 43:1065-1078 https://doi.org/10.1046/j.1365-2958.2002.02774.x
  25. Hermann, T.E., Kurtz, M.B. and Champe, S.P. 1983. Laccase localized in hulle cells and cleistothecial primordia of Aspergillus nidulans J. bacteriol. 154:955-964
  26. Hoffmann, B., Wanke, C., Lapaglia, S.K. and Braus, G.H. 2000. c-Jun and RACK1 homologues regulate a controI point forsexual development in Aspergillus nidulans. Mol. Microbiol. 37:28-41 https://doi.org/10.1046/j.1365-2958.2000.01954.x
  27. Hondmann, D.H. and Visser, J. 1994. Carbon metabolism. Prog.Ind. Microbiol. 29:61-139
  28. Kafer, E. 1965. Origins of translocations in Aspergillus nidulans.Genetics 52:217-232
  29. Kafer, E. 1977. Meiotic and mitotic recombination in Aspergillus and its chromosomal aberrations. Adv. Genet 19:33-131 https://doi.org/10.1016/S0065-2660(08)60245-X
  30. Kato, N., Brooks, W. and Calvo, A.M. 2003. The expression of sterigmatocystin and penicillin genes in Aspergillus nidulans is controlled by veA, a gene required for sexual development. Eukaryot. Cell 2:1178-1186 https://doi.org/10.1128/EC.2.6.1178-1186.2003
  31. Kawasaki, L., Sanchez, O., Shiozaki, K. and Aguirre, J. 2002. SakA MAP kinase is involved in stress signal transduction, sexual development and spore viability in Aspergillus nidulansMol. Microbiol. 45:1153-1163
  32. Kehoe, D.M. and Grossman, A.R. 1996. Similarity of a coromatic adaptation sensor to phytochrome and ethylene receptors. Science 273:1409-1412 https://doi.org/10.1126/science.273.5280.1409
  33. Keleher, C.A., Redd, M.J., Schultz, J., Carlson, M. and Johnson, A.D. 1992. Ssn6-Tupl is a general repressor of transcription in yeast. Cell 68:709-719 https://doi.org/10.1016/0092-8674(92)90146-4
  34. Kim, H., Han, K., Kim, K., Han, D., Jahng, K. and Chae, K. 2002. The veA gene activates sexual development in Aspergillus nidulansFungal Genet. Biol. 37:72-80
  35. Kim, H.R., Chae, K.S. ,Han, K.H. and Han, D.M. (2009) The nsdC gene encoding a putative C2H2-type transcription factor is a key activator of sexual development in Aspergillus nidulans Genetics 182:771-783
  36. Lambeth, J.D. 2004. NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol 4:181-189 https://doi.org/10.1038/nri1312
  37. Lara-Ortiz, T., Riveros-Rosas, H. and Aguirre, J. 2003. Reactive oxygen species generated by microbial NADPH oxidase NoxA regulate sexual development in Aspergillus nidulans. Mol. Microbiol. 50:1241-1255 https://doi.org/10.1046/j.1365-2958.2003.03800.x
  38. Lee, J., Lee, T., Lee, Y,W., Yun, S.H. and Turgeon, B.G. 2003. Shifting fungal reproductive mode by manipulation of mating type genes: obligatoty heterothallism of Gibberella zeae. Mol. Microbiol. 50:145-152 https://doi.org/10.1046/j.1365-2958.2003.03694.x
  39. Martinelli, S.D. 1979. Phenotypes of double conidiation mutants of Aspergillus nidulans. J. Gen. Microbiol. 114:277-287
  40. Martinelli, S.D. and Clutterbuck, A.J. 1971. A quantitative survey of conidiation mutants in Aspergillus nidulans. J. Gen. Microbiol. 69:261-268
  41. Masloff, S., Poggeler, S. and kuck, U. 1999. The pro1(+) gene from Srdaria macrospora encodes a C6 zinc finger transcription factor required for fruiting body development. Genetics 152:191-199
  42. Miller, K.Y., Nowell, A. and Miller, B.L. 2005. Differential reg ulation of fruitbody development and meiosis by the unlinked Aspergillus nidulans mating type loci. Fungal Genet. Newslett 52:184
  43. Miller, K.Y., Wu, J. and Miller, B.L. 1992. StuA is required for celI pattern formation in Aspergillus. Genes Dev. 6:1770-1782 https://doi.org/10.1101/gad.6.9.1770
  44. Min, J.Y., Kim, H.R., Han, K.H. and Han, D.M. 2007. Isolation and characterization of Aspergillus nidulans mutants which undergo sexual development in light exposure. Korean J. Microbiol. 43:77-82
  45. Mooney, J.L. and yager,L.N. 1990. Light is required for conidiation in Aspergillus nidulans. Genes Dev. 4:1473-1482 https://doi.org/10.1101/gad.4.9.1473
  46. Ng, A.M.L., Smith, J.E. and Mclntosh, A.F. 1973. Changes in activity of tricarboxic acid cycle and glyoxylate cycle enzymes during synchronous development of Aspergillus nidulans. Trans. Brif. Mycol. Soc. 61:12-20
  47. O'Gorman, C.M., Fuller, H.T. and Dyer, P. 2008. Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457:471-474 https://doi.org/10.1038/nature07528
  48. Paoletti, M., Seymour, F., Alcocer, M., Kaur, N., Calvo, A., Archer, D. and Dyer, P. 2007. Mating Type and the Genetic Basis of self-Fertility in the Model Fungus Aspergillus nidulans. Curr. Biol. 17:1384-1389 https://doi.org/10.1016/j.cub.2007.07.012
  49. Pascon, R.C. and Miller, B.L. 2000. Morphogenesis in Aspergillus nidulans requires Dopey(DopA), a member of a novel family of leucine zipper-like proteins conserved from yeast to humans. Mol. Microbiol. 36:1250-1264 https://doi.org/10.1046/j.1365-2958.2000.01950.x
  50. 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 https://doi.org/10.1016/S0065-2660(08)60408-3
  51. Raper, K.B. and Fennell, D.I. 1965. The Genus Aspergillus (Baltimore, The Williams and Wilkins co)
  52. Samson, R.A. 1994. Current systematics of the genus Aspergillus In: The genus Aspergillus: from taxonomy and genetics to industrial application, pp. 261-276. Eds. K.A. Powell, A. Ren-wick, and J.F. Peberdy, Plenum press, London
  53. Scazzocchio, C. 2006. Aspergillus genomes: secret sex and the secrets of sex. Trends in Genetics 22:521-525 https://doi.org/10.1016/j.tig.2006.08.004
  54. Scherer, M. and Fischer, R. 1998. Purification and characterization of laccase Ⅱ of Aspergillus nidulans. Arch. Microbiol. 170:78-84 https://doi.org/10.1007/s002030050617
  55. Soberer, M., Wei, H., Liese, R. and Fischer, R. 2002. Aspergillus nidulans catalase-peroxidase gene (cpeA) is transcriptionally induced during sexual development through the transcription factor StuA. Eukaryot. Cell 1:725-735 https://doi.org/10.1128/EC.1.5.725-735.2002
  56. Seo, J., Han, K. and Yu, J. 2004. The gprA and gprB genes encode putative G protein-coupled receptors required for self-fertilization in Aspergillus nidulans. Mol. Microbiol. 53:1611-1623 https://doi.org/10.1111/j.1365-2958.2004.04232.x
  57. Serlupi-Crescenzi, O., Kurtz, M.B. and Champe, S.P. 1983. Developmental defects resulting from arginine auxotrophy in Aspergillus nidulans. J. Gen. Microbiol. 129:3535-3544.
  58. Sohn, K. T. and Yoon, K. S. 2002. Ultrastructural study on the cleistothecium development in Aspergillus nidulans. Mycobiotogy 30:117-120
  59. Song, M. H., Nah, J. Y., Han, Y. S., Han, D. M. and Chae, K. S. 2001. Promotion of conidial head formation in Aspergillus oryzae by a salt. Biotechnol. Lett. 23:689-691 https://doi.org/10.1023/A:1010308601469
  60. Stinnett, S. M., Espeso, E. A., Cobeno, L., Araujo-Bazan, L. and Calvo, A. M. 2007. Aspergillus nidulans VeA subcellular 1ocalization is dependent on the importin alpha carrier and on light. MoI. MicrobioI. 63:242-255 https://doi.org/10.1111/j.1365-2958.2006.05506.x
  61. Tan, K. K. 1978. Light induced fungal development, In: The Filamentous Fungi, pp. 334-357. Eds. J. E. Smith and D. R. Berry, Wiley, New York, NY
  62. Urey, J. C. 1971. Enzyme patterns and protein synthesis during synchronous conidiation in Neurospora crassa. Dev. BioI. 26:17-27 https://doi.org/10.1016/0012-1606(71)90103-5
  63. Vallim, M. A., Miller, K. Y. and Miller, B. L. 2000. Aspergillu sSteA (steri1e12-1ike) is a homeodomain-C2/H2-Zn+2 finger transcription factor required for sexual reproduction. Mol. Microbiot. 36:290-301 https://doi.org/10.1046/j.1365-2958.2000.01874.x
  64. Vienken, K. and Fischer, R. 2006. The Zn(II)2Cys6 putative transcription factor NosA controls fruiting body formation in Aspergillus nidulans. MoI. Microbiol. 61:544-554. https://doi.org/10.1111/j.1365-2958.2006.05257.x
  65. 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 lowcarbon conditions and in submersed culture. Genetics 169:619-630 https://doi.org/10.1534/genetics.104.030767
  66. Wei, H., Requena, N. and Fischer, R. 2003. The MAPKK kinase SteC regulates conidiophore morphology and is essential for heterokaryon formation and sexual development in the homothallic fungus Aspergillus nidulans. Mol. Microbiol. 47:1577-1588 https://doi.org/10.1046/j.1365-2958.2003.03405.x
  67. Wu, J. and Miller, B. L. 1997. Aspergillus asexual reproduction and sexual reproduction are differentially affected by transcriptional and translational mechanisms regulating stunted gene expression. Mol. Cell BioI. 17:6191-6201
  68. Yager, L. N. 1992. Early developmental events during asexual and sexual sporulation in Aspergillus nidulans. Biotechnology 23:19-41 https://doi.org/10.1016/0168-1656(92)90097-S
  69. Yeh, K. C., Wu, S. H., Murphy, J. T. and Lagarias, J. C. 1997. A cyanobacterial phytochrome two-component light sensory System. Science 277:1505-1508 https://doi.org/10.1126/science.277.5331.1505
  70. Yun, S. H., Berbee, M. L., Yoder, O. C. and Turgeon, B. G. 1999. .Evolution of the fungal self-fertile reproductive life style from self-sterile ancestors. Proc. Natl. Acad. Sci. USA 96:5592-5597 https://doi.org/10.1073/pnas.96.10.5592
  71. Zonneveld, B. J. 1977. Biochemistry and ultrastructure of sexual development in Aspergillus nidulans. In: Genetics and Physiology of Aspergillus, pp. 59-80. Eds. J. E. Smith and J. A. Pateman, Academic Press, London

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