Skip to main content
Log in

The fruiting-specific Le.flp1 gene, encoding a novel fungal fasciclin-like protein, of the basidiomycetous mushroom Lentinula edodes

  • Research Article
  • Published:
Current Genetics Aims and scope Submit manuscript

Abstract

To understand the molecular mechanisms of fruiting body formation of basidiomycetous mushrooms, we have isolated over a 100 of developmentally regulated genes that were specifically transcribed during fruiting body development in Lentinula edodes (Shiitake-mushroom) by a subtractive hybridization, cDNA-RDA (cDNA representational difference analysis). One of these genes, named Le.flp1, was isolated from the primordial cDNA library of L. edodes, and the expression product of Le.flp1 and putative fungal homologues contained a characteristic region, homologous to the Fas domain of fasciclin family proteins, which are capable of promoting cell adhesion through Fas domain-mediated homophilic interactions in various organisms. RT-PCR analyses suggested that Le.flp1 was specifically expressed in primordia and mature fruiting bodies. In situ hybridization indicated that Le.flp1 transcripts were distributed distinctly in the following tissues: the inside of gills of fruiting bodies, especially at the boundary between the subhymenium and trama, where there is active proliferation of basidium cells for producing basidiospores; peripheral regions of the primordium, pileus and stipe; and both inner tissue and outer regions of the stipe. Our results suggest the hypothesis that Le.flp1 plays a role in cellular differentiation and development in ubiquitous tissues during fruiting body formation in L. edodes, possibly through cell adhesion.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Altschul SF, Madden TL, SchaVer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Bairoch A, Bucher P, Hofmann K (1997) The PROSITE database, its status in 1997. Nucleic Acids Res 25:217–221

    Article  PubMed  CAS  Google Scholar 

  • Carr MD, Bloemink MJ, Dentten E, Whelan AO, Gordon SV, Kelly G, Frenkiel TA, Hewinson RG, Williamson RA (2003) Solution structure of the Mycobacterium tuberculosis complex protein MPB70: from tuberculosis pathogenesis to inherited human corneal desease. J Biol Chem 278:43736–43743

    Article  PubMed  CAS  Google Scholar 

  • Chang ST, Miles PG (1991) Recent trends in world production of cultivated mushrooms. Mush J 503:15–18

    Google Scholar 

  • Chiu SW, Moore D (1990) Sporulation in Coprinus cinereus: use of an in vitro assay to establish the major landmarks in differentiation. Mycol Res 94:249–253

    Article  Google Scholar 

  • Dahiya P, Findlay K, Roberts K, McCann MC (2006) A fasciclin-domain containing gene, ZeFLA11, is expressed exclusively in xylem elements that have reticulate wall thickenings in the stem vascular system of Zinnia elegans cv Envy. Planta 223:1281–1291

    Article  PubMed  CAS  Google Scholar 

  • Eisenhaber B, Wildpaner M, Schultz CJ, Borner GHH, Dupree P, Eisenhaber F (2003) Glycosylphosphatidylinositol lipid anchoring of plant proteins: sensitive prediction from sequence- and genome-wide studies for Arabidopsis and rice. Plant Physiol 133:1691–1701

    Article  PubMed  CAS  Google Scholar 

  • Elkins T, Hortsch M, Bieber AJ, Snow PM, Goodman CS (1990a) Drosophila fasciclin I is a novel homophilic adhesion molecule that along with fasciclin III can mediate cell sorting. J Cell Biol 110:1825–1832

    Article  PubMed  CAS  Google Scholar 

  • Elkins T, Zinn K, McAllister L, Hoffmann FM, Goodman CS (1990b) Genetic analysis of a Drosophila neural cell adhesion molecule: interaction of fasciclin I and abelson tyrosine kinase mutations. Cell 60:565–575

    Article  PubMed  CAS  Google Scholar 

  • 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 139:117–121

    Article  PubMed  CAS  Google Scholar 

  • Faik A, Abouzouhair J, Sarhan F (2006) Putative fasciclin-like arabinogalactan-proteins (FLA) in wheat (Triticum aestivum) and rice (Oryza sativa): identification and bioinformatic analyses. Mol Genet Genomics 276:478–494

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fitch WM (1977) On the problem of discovering the most parsimonious tree. Am Nat 111:223–257

    Article  Google Scholar 

  • Galagan JE, Calvo SE, Cuomo C, Ma LJ, Wortman JR, Batzoglou S, Lee SI, Basturkmen M, Spevak CC, Clutterbuck J, Kapitonov V, Jurka J, Scazzocchio C, Farman M, Butler J, Purcell S, Harris S, Braus GH, Draht O, Busch S, D’Enfert C, Bouchier C, Goldman GH, Bell-Pedersen D, Griffiths-Jones S, Doonan JH, Yu J, Vienken K, Pain A, Freitag M, Selker EU, Archer DB, Penalva MA, Oakley BR, Momany M, Tanaka T, Kumagai T, Asai K, Machida M, Nierman WC, Denning DW, Caddick M, Hynes M, Paoletti M, Fischer R, Miller B, Dyer P, Sachs MS, Osmani SA, Birren BW (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438:1105–1115

    Article  PubMed  CAS  Google Scholar 

  • Gaspar YM, Johnson KL, Mckenna JA, Bacic A, Schultz CJ (2001) The complex structures of arabinogalactan-proteins and the journey towards a function. Plant Mol Biol 47:161–176

    Article  PubMed  CAS  Google Scholar 

  • Han JH, Stratowa C, Rutter WJ (1987) Isolation of full-length putative rat lysophospholipase cDNA using improved methods for mRNA isolation and cDNA cloning. Biochemistry 26:1617–1625

    Article  PubMed  CAS  Google Scholar 

  • Hardtke CS (2006) Root development–branching into novel spheres. Curr Opin Plant Biol 9:66–71

    Article  PubMed  CAS  Google Scholar 

  • Hori K, Kajiwara S, Saito T, Miyazawa H, Katayose Y, Shishido K (1991) Cloning, sequence analysis and transcriptional expression of a ras gene of the edible basidiomycete Lentinus edodes. Gene 105:91–96

    Article  PubMed  CAS  Google Scholar 

  • Hubank M, Schatz DG (1994) Identifying differences in mRNA expression by representational difference analysis of cDNA. Nucleic Acids Res 22:5640–5648

    Article  PubMed  CAS  Google Scholar 

  • Huber O, Sumper M (1994) Algal-CAMs: isoforms of a cell adhesion molecule in embryos of the alga Volvox with homology to Drosophila fasciclin I. EMBO J 13:4212–4222

    PubMed  CAS  Google Scholar 

  • Johnson KL, Jones BJ, Bacic A, Schultz CJ (2003) The fasciclin-like arabinogalactan proteins of Arabidopsis. A multigene family of putative cell adhesion molecules. Plant Physiol 133:1911–1925

    Article  PubMed  CAS  Google Scholar 

  • Kajiwara S, Yamaoka K, Hori K, Miyazawa H, Saito T, Kanno T, Shishido K (1992) Isolation and sequence of a developmentally regulated putative novel gene, priA, from the basidiomycete Lentinus edodes. Gene 114:173–178

    Article  PubMed  CAS  Google Scholar 

  • Kaneko S, Shishido K (2001) Cloning and sequence analysis of the basidiomycete Lentinus edodes ribonucleotide reductase small subunit cDNA and expression of a corresponding gene in L. edodes. Gene 262:43–50

    Article  PubMed  CAS  Google Scholar 

  • Kawamoto T, Noshiro M, Shen M, Nakamasu K, Hashimoto K, Kawashima-Ohya Y, Gotoh O, Kato Y (1998) Structural and phylogenetic analyses of RGP-CAP/big-h3, a fasciclin-like adhesion protein expressed in chick chondrocytes. Biochim Biophys Acta 1395:288–292

    PubMed  CAS  Google Scholar 

  • Kim JE, Kim SJ, Lee BH, Park RW, Kim KS, Kim IS (2000) Identification of motifs for cell adhesion within the repeated domains of transforming growth factor-b-induced gene, big-h3. J Biol Chem 275:30907–30915

    Article  PubMed  CAS  Google Scholar 

  • Kondoh O, Muto A, Kajiwara S, Takagi J, Saito T, Shishido K (1995) A fruit body-specific cDNA mfbAc from the mushroom Lentinus edodes encodes a high-molecular-weight cell-adhesion protein containing an Arg-Gly-Asp motif. Gene 154:31–37

    Article  PubMed  CAS  Google Scholar 

  • Kües U (2000) Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiol Mol Biol Rev 64:316–353

    Article  PubMed  Google Scholar 

  • Lazdunski CJ, Benedetti H (1990) Insertion and translocation of proteins into and through membranes. FEBS Lett 268:408–414

    Article  PubMed  CAS  Google Scholar 

  • Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K, Arima T, Akita O, Kashiwagi Y, Abe K, Gomi K, Horiuchi H, Kitamoto K, Kobayashi T, Takeuchi M, Denning DW, Galagan JE, Nierman WC, Yu J, Archer DB, Bennett JW, Bhatnagar D, Cleveland TE, Fedorova ND, Gotoh O, Horikawa H, Hosoyama A, Ichinomiya M, Igarashi R, Iwashita K, Juvvadi PR, Kato M, Kato Y, Kin T, Kokubun A, Maeda H, Maeyama N, Maruyama J, Nagasaki H, Nakajima T, Oda K, Okada K, Paulsen I, Sakamoto K, Sawano T, Takahashi M, Takase K, Terabayashi Y, Wortman JR, Yamada O, Yamagata Y, Anazawa H, Hata Y, Koide Y, Komori T, Koyama Y, Minetoki T, Suharnan S, Tanaka A, Isono K, Kuhara S, Ogasawara N, Kikuchi H (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438:1157–1161

    Article  PubMed  Google Scholar 

  • Miyazaki Y, Jojima T, Ono T, Yamazaki T, Shishido K (2004a) A cDNA homologue of Schizosaccharomyces pombe cdc5 + from the mushroom Lentinula edodes: characterization of the cDNA and its expressed product. Biochim Biophys Acta 1680:93–102

    PubMed  CAS  Google Scholar 

  • Miyazaki Y, Nakamura M, Babasaki K (2005) Molecular cloning of developmentally specific genes by representational difference analysis during the fruiting body formation in the basidiomycete Lentinula edodes. Fungal Genet Biol 42:493–505

    Article  PubMed  CAS  Google Scholar 

  • Miyazaki Y, Sakuragi Y, Yamazaki T, Shishido K (2004b) Target genes of the developmental regulator PRIB of the mushroom Lentinula edodes. Biosci Biotechnol Biochem 68:1898–1905

    Article  PubMed  CAS  Google Scholar 

  • Miyazaki Y, Tsunoka O, Shishido K (1997) Determination of the DNA-binding sequences of the Zn(II)2Cys6 zinc-cluster-containing PRIB protein, derived from the basidiomycete Lentinus edodes gene. J Biochem 122:1088–1091

    PubMed  CAS  Google Scholar 

  • Nakai K, Horton P (1999) PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24:34–36

    Article  PubMed  CAS  Google Scholar 

  • Nakazawa T, Miyazaki Y, Kaneko S, Shishido K (2006) Developmental regulator Le.CDC5 of the mushroom Lentinula edodes: analyses of its amount in each of the stages of fruiting-body formation and its distribution in parts of the fruiting bodies. FEMS Microbiol Lett 261:60–63

    Article  PubMed  CAS  Google Scholar 

  • Ng WL, Ng TP, Kwan HS (2000) Cloning and characterization of two hydrophobin genes differentially expressed during fruiting body development in Lentinula edodes. FEMS Micobiol Lett 185:139–145

    Article  CAS  Google Scholar 

  • Nierman WC, Pain A, Anderson MJ, Wortman JR, Kim HS, Arroyo J, Berriman M, Abe K, Archer DB, Bermejo C, Bennett J, Bowyer P, Chen D, Collins M, Coulsen R, Davies R, Dyer PS, Farman M, Fedorova N, Fedorova N, Feldblyum TV, Fischer R, Fosker N, Fraser A, Garcia JL, Garcia MJ, Goble A, Goldman GH, Gomi K, Griffith-Jones S, Gwilliam R, Haas B, Haas H, Harris D, Horiuchi H, Huang J, Humphray S, Jimenez J, Keller N, Khouri H, Kitamoto K, Kobayashi T, Konzack S, Kulkarni R, Kumagai T, Lafon A, Latge JP, Li W, Lord A, Lu C, Majoros WH, May GS, Miller BL, Mohamoud Y, Molina M, Monod M, Mouyna I, Mulligan S, Murphy L, O’Neil S, Paulsen I, Penalva MA, Pertea M, Price C, Pritchard BL, Quail MA, Rabbinowitsch E, Rawlins N, Rajandream MA, Reichard U, Renauld H, Robson GD, Rodriguez de Cordoba S, Rodriguez-Pena JM, Ronning CM, Rutter S, Salzberg SL, Sanchez M, Sanchez-Ferrero JC, Saunders D, Seeger K, Squares R, Squares S, Takeuchi M, Tekaia F, Turner G, Vazquez de Aldana CR, Weidman J, White O, Woodward J, Yu JH, Fraser C, Galagan JE, Asai K, Machida M, Hall N, Barrell B, Denning DW (2005) Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438:1151–1156

    Article  PubMed  CAS  Google Scholar 

  • Nishizawa H, Miyazaki Y, Kaneko S, Shishido K (2002) Distribution of hydrophobin 1 gene transcript in developing fruiting bodies of Lentinula edodes. Biosci Biotechnol Biochem 66:1951–1954

    Article  PubMed  CAS  Google Scholar 

  • Paulsrud P, Lindblad P (2002) Fasciclin domain proteins are present in nostoc symbionts of lichens. Appl Environ Microbiol 68:2036–2039

    Article  PubMed  CAS  Google Scholar 

  • Reijnders AFM (1979) Developmental anatomy of Coprinus. Persoonia 10:383–424

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

    Google Scholar 

  • Takagi Y, Katayose Y, Shishido K (1988) Intracellular levels of cyclic AMP and adenylated cyclase activity during mycelial development in fruit body formation in L. edodes. FEMS Microbiol Lett 55:275–278

    Article  CAS  Google Scholar 

  • Tanaka Y, Kaneko S, Katsukawa S, Yamazaki T, Ohta A, Miyazaki Y, Shishido K (2005) Specific distribution in homobasidiomycete hymenophores of the transcripts of Ras protein and G-protein alpha-subunit genes. FEMS Microbiol Lett 242:169–175

    Article  PubMed  CAS  Google Scholar 

  • Tsivileva OM, Nikitina VE, Garibova LV, Ignatov VV (2001) Lectin activity of Lentinus edodes. Int Microbiol 4:41–45

    PubMed  CAS  Google Scholar 

  • von Heijne G (1986) A new method for predicting signal cleavage sites. Nucleic Acids Res 14:4683–4690

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by a Grant-in-Aid for Scientific Research (No. 17780068) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. The authors deeply appreciate Dr. Teruko Konishi, of the University of Ryukyus’ Faculty of Agriculture, for her useful and accurate comments on the experiments.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yasumasa Miyazaki.

Additional information

Communicated by U. Kües.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Miyazaki, Y., Kaneko, S., Sunagawa, M. et al. The fruiting-specific Le.flp1 gene, encoding a novel fungal fasciclin-like protein, of the basidiomycetous mushroom Lentinula edodes . Curr Genet 51, 367–375 (2007). https://doi.org/10.1007/s00294-007-0133-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00294-007-0133-2

Keywords

Navigation