Advertisement

Current Genetics

, Volume 44, Issue 3, pp 124–131 | Cite as

The Aa-Pri4 gene, specifically expressed during fruiting initiation in the Agrocybe aegerita complex, contains an unusual CT-rich leader intron within the 5′ uncoding region.

  • Pascal Sirand-Pugnet
  • Cruz Santos
  • Jacques LabarèreEmail author
Research Article

Abstract

The Aa1-Pri4 gene was cloned from the edible mushroom Agrocybe aegerita. The gene, specifically expressed during fruiting initiation, encodes a glycine-rich protein of 116 amino acids, with no homology to already known proteins. Homologous genes were amplified from two other strains belonging to the Agr. aegerita complex and originating from South-East Asia; and a comparison of the three genes revealed a high conservation of the coding sequences (72.8–97.8%). The PRI4 putative protein sequences were highly similar (87.5–100.0%); and all of them contained two protein kinase C sites, suggesting a potential supplementary regulation by phosphorylation at the protein level. The 5′ uncoding regions all presented a leader intron, very variable in sequence (45.7% identity), but with a high C+T content (74.5–79.0%). The presence of such CT-rich sequences previously described in the promoter of highly expressed fungal genes suggests that the leader intron of the Aa1-Pri4 gene could be involved in the high-level, stage-specific expression.

Keywords

Basidiomycota Fungi Fruiting initiation Leader intron CT-rich sequence 

Notes

Acknowledgements

This research was supported by grants from the European Community (Fonds Européen de Développement Régional), the Conseil Scientifique de l′Université Victor Ségalen Bordeaux 2, Monsieur le Préfet de la Région Aquitaine Préfet de la Gironde (Fonds National d′Aménagement et de Développement du Territoire), the Conseil Régional d′Aquitaine and the Institut National de la Recherche Agronomique. We thank Prof. Jorge Wright and Dr. E. Alberto (Argentina), Dr. R. de Leon (Guatemala) and Dr. P. Pitakpaivan (Thailand) for kindly providing strains, and S. Chideh Soliman, C. Mulot and A.S. Scheuer for technical help.

References

  1. Altschul SF, et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedGoogle Scholar
  2. Ando A, Harada A, Miura K, Tamai Y (2001) A gene encoding a hydrophobin, fvh1, is specifically expressed after the induction of fruiting in the edible mushroom Flammulina velutipes. Curr Genet 39:190–197CrossRefPubMedGoogle Scholar
  3. Baunsgaard L, Dalboge H, Houen G, Rasmussen EM, Welinder KG (1993) Amino acid sequence of Coprinus macrorhizus peroxidase and cDNA sequence encoding Coprinus cinereus peroxidase. A new family of fungal peroxidases. Eur J Biochem 213:605–611PubMedGoogle Scholar
  4. Berne S, Krizaj I, Pohleven F, Turk T, Macek P, Sepcic K (2002) Pleurotus and Agrocybe hemolysins, new proteins hypothetically involved in fungal fruiting. Biochim Biophys Acta 1570:153–159CrossRefPubMedGoogle Scholar
  5. Boulianne RP, Liu Y, Aebi M, Lu BC, Kues U (2000) Fruiting body development in Coprinus cinereus: regulated expression of two galectins secreted by a non-classical pathway. Microbiology 146:1841–1853PubMedGoogle Scholar
  6. Bucher P, Bairoch A (1994) A generalized profile syntax for biomolecular sequence motifs and its function in automatic sequence interpretation. Ismb 2:53–61PubMedGoogle Scholar
  7. Curie C, Axelos M, Bardet C, Atanassova R, Chaubet N, Lescure B (1993) Modular organization and development activity of an Arabidopsis thaliana EF-1 alpha gene promoter. Mol Gen Genet 238:428–436PubMedGoogle Scholar
  8. De Groot PW, Roeven RT, Van Griensven LJ, Visser J, Schaap PJ (1999) Different temporal and spatial expression of two hydrophobin-encoding genes of the edible mushroom Agaricus bisporus. Microbiology 145:1105–1113PubMedGoogle Scholar
  9. Endo H, Kajiwara S, Tsunoka O, Shishido K (1994) A novel cDNA, priBc, encoding a protein with a Zn(II)2Cys6 zinc cluster DNA-binding motif, derived from the basidiomycete Lentinus edodes. Gene 139:117–121PubMedGoogle Scholar
  10. Esser K, Saleh F, Meinhardt F (1979) Genetic of fruit body production in higher basidiomycetes. 2. Monokaryotic and dikaryotic fruiting in Schizophyllum commune. Curr Genet 1:85–88Google Scholar
  11. Fernandez Espinar MT, Labarère J (1997) Cloning and sequencing of the Aa-Pri1 gene specifically expressed during fruiting initiation in the edible mushroom Agrocybe aegerita, and analysis of the predicted amino-acid sequence. Curr Genet 32:420–424CrossRefPubMedGoogle Scholar
  12. Fu H, Kim SY, Park WD (1995) A potato Sus3 sucrose synthase gene contains a context-dependent 3′ element and a leader intron with both positive and negative tissue-specific effects. Plant Cell 7:1395–1403Google Scholar
  13. Gurr SJ, Unkles SE, Kinghorn JR (1987) The structure and organization of nuclear genes in filamentous fungi. In: Kinghorn JL (ed) Gene structure in eukaryotic microbes. IRL Press, London, pp 93–139Google Scholar
  14. Kajiwara S, et al (1992) Isolation and sequence of a developmentally regulated putative novel gene, priA, from the basidiomycete Lentinus edodes. Gene 114:173–178PubMedGoogle Scholar
  15. Kim D, Azuma T (1999) Cloning of a gene specifically expressed during early stage of fruiting body formation in Flammulina velutipes. Korean J Mycol 27:187–190Google Scholar
  16. Kim D, et al (1999) Cloning and sequence analysis of a cDNA for the gene FVFD30, specifically expressed during fruiting body development in Flammulina velutipes. Mushroom Sci Biotechnol 7:95–99Google Scholar
  17. Lee SH, et al (2002) Comparative analysis of sequences expressed during the liquid-cultured mycelia and fruit body stages of Pleurotus ostreatus. Fungal Genet Biol 35:115–134CrossRefPubMedGoogle Scholar
  18. Leung GS, Zhang M, Xie WJ, Kwan HS (2000) Identification by RNA fingerprinting of genes differentially expressed during the development of the basidiomycete Lentinula edodes. Mol Gen Genet 262:977–990PubMedGoogle Scholar
  19. Lugones LG, Scholtmeijer K, Klootwijk R, Wessels JG (1999) Introns are necessary for mRNA accumulation in Schizophyllum commune. Mol Microbiol 32:681–689PubMedGoogle Scholar
  20. Mehrel T, et al (1990) Identification of a major keratinocyte cell envelope protein, loricrin. Cell 61:1103–1112PubMedGoogle Scholar
  21. Meinhardt F, Esser K (1981) Genetic studies of the basidiomycete Agrocybe aegerita. 2. Genetic control of fruit body formation and its practical implications. Theor Appl Genet 60:265–268Google Scholar
  22. Morello L, Bardini M, Sala F, Breviario D (2002) A long leader intron of the Ostub16 rice beta-tubulin gene is required for high-level gene expression and can autonomously promote transcription both in vivo and in vitro. Plant J 29:33–44CrossRefPubMedGoogle Scholar
  23. Mukherjee A, Cui Y, Liu Y, Chatterjee AK (1997) Molecular characterization and expression of the Erwinia carotovora hrpNEcc gene, which encodes an elicitor of the hypersensitive reaction. Mol Plant Microbe Interact 10:462–471PubMedGoogle Scholar
  24. Naqvi SM, Park KS, Yi SY, Lee HW, Bok SH, Choi D (1998) A glycine-rich RNA-binding protein gene is differentially expressed during acute hypersensitive response following tobacco mosaic virus infection in tobacco. Plant Mol Biol 37:571–576CrossRefPubMedGoogle Scholar
  25. Ng WL, Ng TP, Kwan HS (2000) Cloning and characterization of two hydrophobin genes differentially expressed during fruit body development in Lentinula edodes. FEMS Microbiol Lett 185:139–145CrossRefPubMedGoogle Scholar
  26. Noël T, Labarère J (1989) Isolation of DNA from Agrocybe aegerita for the construction of a genomic library in Escherichia coli. Mushroom Sci 12:187–201Google Scholar
  27. Ospina-Giraldo MD, Collopy PD, Romaine CP, Royse DJ (2000) Classification of sequences expressed during the primordial and basidiome stages of the cultivated mushroom Agaricus bisporus. Fungal Genet Biol 29:81–94CrossRefPubMedGoogle Scholar
  28. Punt PJ, Dingemanse MA, Jacobs-Meijsing BJ, Pouwels PH, Hondel CA van den (1988) Isolation and characterization of the glyceraldehyde-3-phosphate dehydrogenase gene of Aspergillus nidulans. Gene 69:49–57PubMedGoogle Scholar
  29. Ramakrishnan L, Federspiel NA, Falkow S (2000) Granuloma-specific expression of Mycobacterium virulence proteins from the glycine-rich PE-PGRS family. Science 288:1436–1439CrossRefPubMedGoogle Scholar
  30. Raper CA, Raper JR, Miller RE (1972) Genetic analysis of the life cycle of Agaricus bisporus. Mycologia 64:108–117Google Scholar
  31. Saloheimo M, et al (1988) EGIII, a new endoglucanase from Trichoderma reesei: the characterization of both gene and enzyme. Gene 63:11–22PubMedGoogle Scholar
  32. Salvado JC, Labarère J (1991) Isolation of transcripts preferentially expressed during fruit body primordia differentiation in the basidiomycete Agrocybe aegerita. Curr Genet 20:205–210PubMedGoogle Scholar
  33. Sambrook J, Fristsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.Google Scholar
  34. Santos C, Labarère J (1999) Aa-Pri2, a single-copy gene from Agrocybe aegerita, specifically expressed during fruiting initiation, encodes a hydrophobin with a leucine-zipper domain. Curr Genet 35:564–570CrossRefPubMedGoogle Scholar
  35. Schillberg S, Gross P, Tiburzy R (1995) Isolation and characterization of the EF-1 alpha gene of the filamentous fungus Puccinia graminis f. sp. tritici. Curr Genet 27:367–372PubMedGoogle Scholar
  36. Sepcic K, Berne S, Potrich C, Turk T, Macek P, Menestrina G (2003) Interaction of ostreolysin, a cytolytic protein from the edible mushroom Pleurotus ostreatus, with lipid membranes and modulation by lysophospholipids. Eur J Biochem 270:1199–1210PubMedGoogle Scholar
  37. Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9–23PubMedGoogle Scholar
  38. Sirand-Pugnet P, Labarère J (2002) Molecular characterization of the Pri3 gene encoding a cysteine-rich protein, specifically expressed during fruiting initiation within the Agrocybe aegerita complex. Curr Genet 41:31–42CrossRefPubMedGoogle Scholar
  39. Sirand-Pugnet P, Gonzalez P, Labarère J (2000) Phylogeny and evolution of mitochondrial sequences in mushrooms. In: Van Griensven LJLD (ed) Science and cultivation of edible fungi. Balkema, Rotterdam, pp 223–235Google Scholar
  40. Sweigard JA, Carroll AM, Kang S, Farrall L, Chumley FG, Valent B (1995) Identification, cloning, and characterization of PWL2, a gene for host species specificity in the rice blast fungus. Plant Cell 7:1221–1233CrossRefPubMedGoogle Scholar
  41. Tarkka MT, Vasara R, Gorfer M, Raudaskoski M (2000) Molecular characterization of actin genes from homobasidiomycetes: two different actin genes from Schizophyllum commune and Suillus bovinus. Gene 251:27–35CrossRefPubMedGoogle Scholar
  42. Templeton MD, Rikkerink EH, Solon SL, Crowhurst RN (1992) Cloning and molecular characterization of the glyceraldehyde-3-phosphate dehydrogenase-encoding gene and cDNA from the plant pathogenic fungus Glomerella cingulata. Gene 122:225–230PubMedGoogle Scholar
  43. Thompson JD, Higgins DG, Gibson TJ (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 22:4673–4680PubMedGoogle Scholar
  44. Wessels JG (1993) Fruiting in the higher fungi. Adv Microb Physiol 34:147–202PubMedGoogle Scholar
  45. White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR protocols—a guide to methods and applications. Academic Press, New York, pp 315–322Google Scholar
  46. Wu J, Saupe SJ, Glass NL (1998) Evidence for balancing selection operating at the het-c heterokaryon incompatibility locus in a group of filamentous fungi. Proc Natl Acad Sci USA 95:12398–12403CrossRefPubMedGoogle Scholar
  47. Yamazaki T, Hasebe T, Kajiwara S, Shishido K (2000) Structure and function of a pyrimidine/purine-biased sequence from the 5′-flanking region of the basidiomycete Lentinus edodes gene priA. Mol Gen Genet 263:262–270PubMedGoogle Scholar
  48. Yamazaki T, Yasuda T, Miyazaki Y, Okada K, Kajiwara S, Shishido K (2002) A promoter activity in Saccharomyces cerevisiae of the 39-noncoding region of the basidiomycetous mushroom gene. J Gen Appl Microbiol 48:223–231PubMedGoogle Scholar
  49. Zhu W, MaGbanua MM, White FF (2000) Identification of two novel hrp-associated genes in the hrp gene cluster of Xanthomonas oryzae pv. oryzae. J Bacteriol 182:1844–1853CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Pascal Sirand-Pugnet
    • 1
  • Cruz Santos
    • 1
  • Jacques Labarère
    • 1
    Email author
  1. 1.Laboratoire de Génétique et d′Amélioration des Champignons CultivésUniversity Victor Segalen, Bordeaux 2 INRA, C.R.A. de BordeauxVillenave d′Ornon CedexFrance

Personalised recommendations