Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2001 Mar;157(3):957–967. doi: 10.1093/genetics/157.3.957

Accumulation of stress and inducer-dependent plant-cell-wall-degrading enzymes during asexual development in Aspergillus nidulans.

R A Prade 1, P Ayoubi 1, S Krishnan 1, S Macwana 1, H Russell 1
PMCID: PMC1461545  PMID: 11238386

Abstract

Determination and interpretation of fungal gene expression profiles based on digital reconstruction of expressed sequenced tags (ESTs) are reported. A total of 51,524 DNA sequence files processed with PipeOnline resulted in 9775 single and 5660 contig unique ESTs, 31.2% of a typical fungal transcriptome. Half of the unique ESTs shared homology with genes in public databases, 35.8% of which are functionally defined and 64.2% are unclear or unknown. In Aspergillus nidulans 86% of transcripts associate with intermediate metabolism functions, mainly related to carbohydrate, amino acid, protein, and peptide biosynthesis. During asexual development, A. nidulans unexpectedly accumulates stress response and inducer-dependent transcripts in the absence of an inducer. Stress response genes in A. nidulans ESTs total 1039 transcripts, contrasting with 117 in Neurospora crassa, a 14.3-fold difference. A total of 5.6% of A. nidulans ESTs implicate inducer-dependent cell wall degradation or amino acid acquisition, 3.5-fold higher than in N. crassa. Accumulation of stress response and inducer-dependent transcripts suggests general derepression of cis-regulation during terminal asexual development.

Full Text

The Full Text of this article is available as a PDF (345.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alwine J. C., Kemp D. J., Stark G. R. Method for detection of specific RNAs in agarose gels by transfer to diazobenzyloxymethyl-paper and hybridization with DNA probes. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5350–5354. doi: 10.1073/pnas.74.12.5350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aramayo R., Timberlake W. E. Sequence and molecular structure of the Aspergillus nidulans yA (laccase I) gene. Nucleic Acids Res. 1990 Jun 11;18(11):3415–3415. doi: 10.1093/nar/18.11.3415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Audic S., Claverie J. M. The significance of digital gene expression profiles. Genome Res. 1997 Oct;7(10):986–995. doi: 10.1101/gr.7.10.986. [DOI] [PubMed] [Google Scholar]
  4. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  5. Carle-Urioste J. C., Escobar-Vera J., El-Gogary S., Henrique-Silva F., Torigoi E., Crivellaro O., Herrera-Estrella A., El-Dorry H. Cellulase induction in Trichoderma reesei by cellulose requires its own basal expression. J Biol Chem. 1997 Apr 11;272(15):10169–10174. doi: 10.1074/jbc.272.15.10169. [DOI] [PubMed] [Google Scholar]
  6. Chen T., Skiena S. S. A case study in genome-level fragment assembly. Bioinformatics. 2000 Jun;16(6):494–500. doi: 10.1093/bioinformatics/16.6.494. [DOI] [PubMed] [Google Scholar]
  7. Cho R. J., Campbell M. J. Transcription, genomes, function. Trends Genet. 2000 Sep;16(9):409–415. doi: 10.1016/s0168-9525(00)02065-5. [DOI] [PubMed] [Google Scholar]
  8. Doebley J., Lukens L. Transcriptional regulators and the evolution of plant form. Plant Cell. 1998 Jul;10(7):1075–1082. doi: 10.1105/tpc.10.7.1075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ewing R. M., Ben Kahla A., Poirot O., Lopez F., Audic S., Claverie J. M. Large-scale statistical analyses of rice ESTs reveal correlated patterns of gene expression. Genome Res. 1999 Oct;9(10):950–959. doi: 10.1101/gr.9.10.950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ewing R. M., Claverie J. M. EST databases as multi-conditional gene expression datasets. Pac Symp Biocomput. 2000:430–442. doi: 10.1142/9789814447331_0041. [DOI] [PubMed] [Google Scholar]
  11. Harold F. M. In pursuit of the whole hypha. Fungal Genet Biol. 1999 Jul-Aug;27(2-3):128–133. doi: 10.1006/fgbi.1999.1124. [DOI] [PubMed] [Google Scholar]
  12. Häfker T., Techel D., Steier G., Rensing L. Differential expression of glucose-regulated (grp78) and heat-shock-inducible (hsp70) genes during asexual development of Neurospora crassa. Microbiology. 1998 Jan;144(Pt 1):37–43. doi: 10.1099/00221287-144-1-37. [DOI] [PubMed] [Google Scholar]
  13. Kamada T., Bracker C. E., Bartnicki-Garcia S. Chitosomes and chitin synthetase in the asexual life cycle of Mucor rouxii: spores, mycelium and yeast cells. J Gen Microbiol. 1991 Jun;137(6):1241–1252. doi: 10.1099/00221287-137-6-1241. [DOI] [PubMed] [Google Scholar]
  14. Kaminskyj S. G., Hamer J. E. hyp loci control cell pattern formation in the vegetative mycelium of Aspergillus nidulans. Genetics. 1998 Feb;148(2):669–680. doi: 10.1093/genetics/148.2.669. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Karos M., Fischer R. hymA (hypha-like metulae), a new developmental mutant of Aspergillus nidulans. Microbiology. 1996 Nov;142(Pt 11):3211–3218. doi: 10.1099/13500872-142-11-3211. [DOI] [PubMed] [Google Scholar]
  16. Kawasaki L., Wysong D., Diamond R., Aguirre J. Two divergent catalase genes are differentially regulated during Aspergillus nidulans development and oxidative stress. J Bacteriol. 1997 May;179(10):3284–3292. doi: 10.1128/jb.179.10.3284-3292.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kelkar H. S., Griffith J., Case M. E., Covert S. F., Hall R. D., Keith C. H., Oliver J. S., Orbach M. J., Sachs M. S., Wagner J. R. The Neurospora crassa genome: cosmid libraries sorted by chromosome. Genetics. 2001 Mar;157(3):979–990. doi: 10.1093/genetics/157.3.979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kozian D. H., Kirschbaum B. J. Comparative gene-expression analysis. Trends Biotechnol. 1999 Feb;17(2):73–78. doi: 10.1016/s0167-7799(98)01292-x. [DOI] [PubMed] [Google Scholar]
  19. Kubicek C. P. Involvement of a conidial endoglucanase and a plasma-membrane-bound beta-glucosidase in the induction of endoglucanase synthesis by cellulose in Trichoderma reesei. J Gen Microbiol. 1987 Jun;133(6):1481–1487. doi: 10.1099/00221287-133-6-1481. [DOI] [PubMed] [Google Scholar]
  20. Kupfer D. M., Reece C. A., Clifton S. W., Roe B. A., Prade R. A. Multicellular ascomycetous fungal genomes contain more than 8000 genes. Fungal Genet Biol. 1997 Jun;21(3):364–372. doi: 10.1006/fgbi.1997.0982. [DOI] [PubMed] [Google Scholar]
  21. Messner R., Kubicek-Pranz E. M., Gsur A., Kubicek C. P. Cellobiohydrolase II is the main conidial-bound cellulase in Trichoderma reesei and other Trichoderma strains. Arch Microbiol. 1991;155(6):601–606. doi: 10.1007/BF00245356. [DOI] [PubMed] [Google Scholar]
  22. Navarro R. E., Aguirre J. Posttranscriptional control mediates cell type-specific localization of catalase A during Aspergillus nidulans development. J Bacteriol. 1998 Nov;180(21):5733–5738. doi: 10.1128/jb.180.21.5733-5738.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Navarro R. E., Stringer M. A., Hansberg W., Timberlake W. E., Aguirre J. catA, a new Aspergillus nidulans gene encoding a developmentally regulated catalase. Curr Genet. 1996 Mar;29(4):352–359. [PubMed] [Google Scholar]
  24. Noventa-Jordão M. A., Couto R. M., Goldman M. H., Aguirre J., Iyer S., Caplan A., Terenzi H. F., Goldman G. H. Catalase activity is necessary for heat-shock recovery in Aspergillus nidulans germlings. Microbiology. 1999 Nov;145(Pt 11):3229–3234. doi: 10.1099/00221287-145-11-3229. [DOI] [PubMed] [Google Scholar]
  25. Ohlrogge J., Benning C. Unraveling plant metabolism by EST analysis. Curr Opin Plant Biol. 2000 Jun;3(3):224–228. [PubMed] [Google Scholar]
  26. Overbeek R., Larsen N., Pusch G. D., D'Souza M., Selkov E., Jr, Kyrpides N., Fonstein M., Maltsev N., Selkov E. WIT: integrated system for high-throughput genome sequence analysis and metabolic reconstruction. Nucleic Acids Res. 2000 Jan 1;28(1):123–125. doi: 10.1093/nar/28.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Prade R. A., Timberlake W. E. The Aspergillus nidulans brlA regulatory locus consists of overlapping transcription units that are individually required for conidiophore development. EMBO J. 1993 Jun;12(6):2439–2447. doi: 10.1002/j.1460-2075.1993.tb05898.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Prade R. A., Timberlake W. E. The Penicillium chrysogenum and Aspergillus nidulans wetA developmental regulatory genes are functionally equivalent. Mol Gen Genet. 1994 Sep 1;244(5):539–547. doi: 10.1007/BF00583905. [DOI] [PubMed] [Google Scholar]
  29. Richmond T., Somerville S. Chasing the dream: plant EST microarrays. Curr Opin Plant Biol. 2000 Apr;3(2):108–116. doi: 10.1016/s1369-5266(99)00049-7. [DOI] [PubMed] [Google Scholar]
  30. Schmitt A. O., Specht T., Beckmann G., Dahl E., Pilarsky C. P., Hinzmann B., Rosenthal A. Exhaustive mining of EST libraries for genes differentially expressed in normal and tumour tissues. Nucleic Acids Res. 1999 Nov 1;27(21):4251–4260. doi: 10.1093/nar/27.21.4251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Schuler G. D., Epstein J. A., Ohkawa H., Kans J. A. Entrez: molecular biology database and retrieval system. Methods Enzymol. 1996;266:141–162. doi: 10.1016/s0076-6879(96)66012-1. [DOI] [PubMed] [Google Scholar]
  32. Selkov E., Jr, Grechkin Y., Mikhailova N., Selkov E. MPW: the Metabolic Pathways Database. Nucleic Acids Res. 1998 Jan 1;26(1):43–45. doi: 10.1093/nar/26.1.43. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Seoighe C., Wolfe K. H. Extent of genomic rearrangement after genome duplication in yeast. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4447–4452. doi: 10.1073/pnas.95.8.4447. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Skromne I., Sánchez O., Aguirre J. Starvation stress modulates the expression of the Aspergillus nidulans brlA regulatory gene. Microbiology. 1995 Jan;141(Pt 1):21–28. doi: 10.1099/00221287-141-1-21. [DOI] [PubMed] [Google Scholar]
  35. Stringer M. A., Dean R. A., Sewall T. C., Timberlake W. E. Rodletless, a new Aspergillus developmental mutant induced by directed gene inactivation. Genes Dev. 1991 Jul;5(7):1161–1171. doi: 10.1101/gad.5.7.1161. [DOI] [PubMed] [Google Scholar]
  36. Timberlake W. E. Temporal and spatial controls of Aspergillus development. Curr Opin Genet Dev. 1991 Oct;1(3):351–357. doi: 10.1016/s0959-437x(05)80299-0. [DOI] [PubMed] [Google Scholar]
  37. Torigoi E., Henrique-Silva F., Escobar-Vera J., Carle-Urioste J. C., Crivellaro O., El-Dorry H., El-Gogary S. Mutants of Trichoderma reesei are defective in cellulose induction, but not basal expression of cellulase-encoding genes. Gene. 1996 Sep 16;173(2):199–203. doi: 10.1016/0378-1119(96)00219-3. [DOI] [PubMed] [Google Scholar]
  38. Wieser J., Lee B. N., Fondon J. w., 3rd, Adams T. H. Genetic requirements for initiating asexual development in Aspergillus nidulans. Curr Genet. 1994 Dec;27(1):62–69. doi: 10.1007/BF00326580. [DOI] [PubMed] [Google Scholar]
  39. Ye X. S., Lee S. L., Wolkow T. D., McGuire S. L., Hamer J. E., Wood G. C., Osmani S. A. Interaction between developmental and cell cycle regulators is required for morphogenesis in Aspergillus nidulans. EMBO J. 1999 Dec 15;18(24):6994–7001. doi: 10.1093/emboj/18.24.6994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Yu J. H., Wieser J., Adams T. H. The Aspergillus FlbA RGS domain protein antagonizes G protein signaling to block proliferation and allow development. EMBO J. 1996 Oct 1;15(19):5184–5190. [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES