Skip to main content

Advertisement

SpringerLink
Log in

Transcriptome analysis of candidate genes and signaling pathways associated with light-induced brown film formation in Lentinula edodes

  • Genomics, transcriptomics, proteomics
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

High-throughput Illumina RNA-seq was used for deep sequencing analysis of the transcriptome of poly(A)+ RNA from mycelium grown under three different conditions: 30 days darkness (sample 118), 80 days darkness (313W), and 30 days darkness followed by 50 days in the light (313C), in order to gain insight into the molecular mechanisms underlying the process of light-induced brown film (BF) formation in the edible mushroom, Lentinula edodes. Of the three growth conditions, BF formation occurred in 313C samples only. Approximately 159.23 million reads were obtained, trimmed, and de novo assembled into 31,511 contigs with an average length of 1,746 bp and an N 50 of 2,480 bp. Based on sequence orientations determined by a BLASTX search against the NR, Swiss-Prot, COG, and KEGG databases, 24,246 (76.9 %) contigs were assigned putative descriptions. Comparison of 313C/118 and 313C/313W expression profiles revealed 3,958 and 5,651 significantly differentially expressed contigs (DECs), respectively. Annotation using the COG database revealed that candidate genes for light-induced BF formation encoded proteins linked to light reception (e.g., WC-1, WC-2, phytochrome), light signal transduction pathways (e.g., two-component phosphorelay system, mitogen-activated protein kinase pathway), and pigment formation (e.g., polyketide synthase, O-methyltransferase, laccase, P450 monooxygenase, oxidoreductase). Several DECs were validated using quantitative real-time polymerase chain reaction. Our report is the first to identify genes associated with light-induced BF formation in L. edodes and represents a valuable resource for future genomic studies on this commercially important mushroom.

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

Access this article

Log in via an institution

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Aleksandrova EA, Zav’yalova LA, Tereshina VM, Garibova LV, Feofilova EP (1998) Obtaining of fruiting bodies and submerged mycelium of Lentinus edodes (Berk.) Sing [Lentinula edodes (Berk.) Pegler]. Microbiology 67:535–539

    CAS  Google Scholar 

  • Atoui A, Bao DP, Kaur N, Grayburn WS, Calvo AM (2008) Aspergillus nidulans natural product biosynthesis is regulated by mpkB, a putative pheromone response mitogen-activated protein kinase. Appl Environ Microbiol 74:3596–3600

    Article  CAS  Google Scholar 

  • Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995

    CAS  Google Scholar 

  • Ballario P, Vittorioso P, Magrelli A, Talora C, Cabibbo A, Macinol G (1996) White collar-1, a central regulator of blue light responses in Neurospora, is a zinc finger protein. EMBO J 15:1650–1657

    CAS  Google Scholar 

  • Bayram Ö, Braus GH (2012) Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol Rev 36:1–24

    Article  CAS  Google Scholar 

  • Bayram Ö, Krappmann S, Ni M, Bok JW, Helmstaedt K, Valerius O, Braus-Stromeyer S, Kwon NJ, Keller NP, Yu JH, Braus GH (2008) VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320:1504–1506

    Article  CAS  Google Scholar 

  • Bayram Ö, Bayram ÖS, Ahmed YL, Maruyama JI, Valerius O, Rizzoli SO, Ficner R, Irniger S, Braus GH (2012) The Aspergillus nidulans MAPK module AnSte11-Ste50-Ste7-Fus3 controls development and secondary metabolism. PLoS Genet 8:e1002816

    Article  CAS  Google Scholar 

  • Bhatnagar D, Ehrlich KC, Cleveland TE (2003) Molecular genetic analysis and regulation of aflatoxin biosynthesis. Appl Microbiol Biotechnol 61:83–93

    CAS  Google Scholar 

  • Blumenstein A, Vienken K, Tasler R, Purschwitz J, Veith D, Nicole FD, Fischer R (2005) The Aspergillus nidulans phytochrome fphA represses sexual development in red light. Curr Biol 15:1833–1838

    Article  CAS  Google Scholar 

  • Chen RE, Thorner J (2007) Function and regulation in MAPK signaling pathways: lessons learned from the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1773:1311–1340

    Article  CAS  Google Scholar 

  • Chen SC, Ge W, Buswell JA (2004) Molecular cloning of a new laccase from the edible straw mushroom Volvariella volvacea: possible involvement in fruit body development. FEMS Microbiol Lett 230:171–176

    Article  CAS  Google Scholar 

  • Chum WWY, Ng KTP, Shih RSM, Au CH, Kwan HS (2008) Gene expression studies of the dikaryotic mycelium and primordium of Lentinula edodes by serial analysis of gene expression. Mycol Res 112:950–964

    Article  CAS  Google Scholar 

  • Chum WWY, Kwan HS, Au CH, Kwok ISW, Fung YW (2011) Cataloging and profiling genes expressed in Lentinula edodes fruiting body by massive cDNA pyrosequencing and LongSAGE. Fungal Genet Biol 48:359–369

    Article  CAS  Google Scholar 

  • de Paula RM, Lamb TM, Bennett L, Bell-Pedersen D (2008) A connection between MAPK pathways and circadian clocks. Cell Cycle 7:2630–2634

    Article  Google Scholar 

  • Drepper T, Krauss U, Meyer zu Berstenhorst S, Pietruszka J, Jaeger KE (2011) Lights on and action! Controlling microbial gene expression by light. Appl Microbiol Biotechnol 90:23–40

    Article  CAS  Google Scholar 

  • Estrada AF, Avalos J (2008) The White Collar protein WcoA of Fusarium fujikuroi is not essential for photocarotenogenesis, but is involved in the regulation of secondary metabolism and conidiation. Fungal Genet Biol 45:705–718

    Article  CAS  Google Scholar 

  • Frandsen RJN, Nielsen NJ, Maolanon N, Sørensen JC, Olsson S, Nielsen J, Giese H (2006) The biosynthetic pathway for aurofusarin in Fusarium graminearum reveals a close link between the naphthoquinones and naphthopyrones. Mol Microbiol 61:1069–1080

    Article  CAS  Google Scholar 

  • Froehlich AC, Noh B, Vierstra RD, Loros J, Dunlap JC (2005) Genetic and molecular analysis of phytochromes from the filamentous fungus Neurospora crassa. Eukaryot Cell 4:2140–2152

    Article  CAS  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng QD, Chen ZH, Mauceli E, Hacohen N, Gnirke A, Rhind N, Palma FD, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652

    Article  CAS  Google Scholar 

  • Hoffmeister D, Keller NP (2007) Natural products of filamentous fungi: enzymes, genes, and their regulation. Nat Prod Rep 24:393–416

    Article  CAS  Google Scholar 

  • Huang JW, Chen WC, Huang TK, Fu PS, Lai PL, Tsai CF, Hung CC (2011) Using a spectrophotometric study of human gingival color distribution to develop a shade guide. J Dent 39:e11–e16

    Article  Google Scholar 

  • Idnurm A, Heitman J (2005) Light controls growth and development via a conserved pathway in the fungal kingdom. PLos Biol 3:e95

    Article  Google Scholar 

  • Kanehisa M, Goto S (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28:27–30

    Article  CAS  Google Scholar 

  • Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M (2012) KEGG for integration and interpretation of large-scale molecular datasets. Nucleic Acids Res 40:109–114

    Article  Google Scholar 

  • Keller NP, Hohn TM (1997) Metabolic pathway gene clusters in filamentous fungi. Fungal Genet Biol 21:17–29

    Article  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  CAS  Google Scholar 

  • Kuratani M, Tanaka K, Terashima K, Muraguchi H, Nakazawa T, Nakahori K, Kamada T (2010) The dst2 gene essential for photomorphogenesis of Coprinopsis cinerea encodes a protein with a putative FAD-binding-4 domain. Fungal Genet Biol 47:152–158

    Article  CAS  Google Scholar 

  • Leatham G, Stahmann MA (1981) Studies on the laccase of Lentinus edodes: specificity, localization and association with the development of fruiting bodies. J Gen Microbiol 125:147–157

    CAS  Google Scholar 

  • Lee SS, Hong SW, Kim SH, Kim BC (2001) Several genes expressed during morphogenesis of Lentinus edodes (ImHyup-1). Mycobiology 29:135–141

    CAS  Google Scholar 

  • Li HY, Dong YY, Yang J, Liu XM, Wang YF, Yao N, Guan LL, Wang N, Wu JY, Li XK (2012) De novo transcriptome of safflower and the identification of putative genes for oleosin and the biosynthesis of flavonoids. PLoS One 7:e30987

    Article  CAS  Google Scholar 

  • Linden H, 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

    Article  CAS  Google Scholar 

  • Linnemannstöns P, Schulte J, del Mar PM, Proctor RH, Avalos J, Tudzynski B (2002) The polyketide synthase gene pks4 from Gibberella fujikuroi encodes a key enzyme in the biosynthesis of the red pigment bikaverin. Fungal Genet Biol 37:134–148

    Article  Google Scholar 

  • Liu WW, Soulié MC, Perrino C, Fillinger S (2011) The osmosensing signal transduction pathway from Botrytis cinerea regulates cell wall integrity and MAP kinase pathways control melanin biosynthesis with influence of light. Fungal Genet Biol 48:377–387

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  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  CAS  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  Google Scholar 

  • Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320:1344–1349

    Article  CAS  Google Scholar 

  • Ohga S, Cho NS, Thurston CF, Wood DA (2000) Transcriptional regulation of laccase and cellulase in relation to fruit body formation in the mycelium of Lentinula edodes on a sawdust-based substrate. Mycoscience 41:149–153

    Article  CAS  Google Scholar 

  • Pertea G, Huang XQ, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, Tsai J, Quackenbush J (2003) TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19:651–652

    Article  CAS  Google Scholar 

  • Purschwitz J, Müller S, Kastner C, Schöser M, Haas H, Espeso EA, Atoui A, Calvo AM, Fischer R (2008) Functional and physical interaction of blue- and red-light sensors in Aspergillus nidulans. Curr Biol 18:255–259

    Article  CAS  Google Scholar 

  • Rodgers CJ, Blanford CF, Giddens SR, Skamnioti P, Armstrong FA, Gurr SJ (2010) Designer laccases: a vogue for high-potential fungal enzymes. Trends Biotechnol 28:63–72

    Article  CAS  Google Scholar 

  • Sakamoto Y, Nakade K, Sato T (2009) Characterization of the post-harvest changes in gene transcription in the gill of the Lentinula edodes fruiting body. Curr Genet 55:409–423

    Article  CAS  Google Scholar 

  • Sano H, Narikiyo T, Kaneko S, Yamazaki T, Shishido K (2007) Sequence analysis and expression of a blue-light photoreceptor gene, Le.phrA from the basidiomycetous mushroom Lentinula edodes. Biosci Biotech Biochem 71:2206–2213

    Article  CAS  Google Scholar 

  • Sano H, Kaneko S, Sakamoto Y, Sato T, Shishido K (2009) The basidiomycetous mushroom Lentinula edodes white collar-2 homolog PHRB, a partner of putative blue-light photoreceptor PHRA, binds to a specific site in the promoter region of the L. edodes tyrosinase gene. Fungal Genet Biol 46:333–341

    Article  CAS  Google Scholar 

  • Suizu T, Zhou GL, Oowatari Y, Kawamukai M (2008) Analysis of expressed sequence tags (ESTs) from Lentinula edodes. Appl Microbiol Biotechnol 79:461–470

    Article  CAS  Google Scholar 

  • Szeto CYY, Wong QWL, Leung GS, Kwan HS (2008) Isolation and transcript analysis of two-component histidine kinase gene Le.nik1 in Shiitake mushroom, Lentinula edodes. Mycol Res 112:108–116

    Article  CAS  Google Scholar 

  • Takano Y, Kikuchi T, Kubo Y, Hamer JE, Mise K, Furusawa I (2000) The Colletotrichum lagenarium MAP kinase gene CMK1 regulates diverse aspects of fungal pathogenesis. Mol Plant Microbe Interact 13:374–383

    Article  CAS  Google Scholar 

  • Terashima K, Yuki K, Muraguchi H, Akiyama M, Kamada T (2005) The dst1 gene involved in mushroom photomorphogenesis of Coprinus cinereus encodes a putative photoreceptor for blue light. Genetics 171:101–108

    Article  CAS  Google Scholar 

  • Tisch D, Schmoll M (2010) Light regulation of metabolic pathways in fungi. Appl Microbiol Biotechnol 85:1259–1277

    Article  CAS  Google Scholar 

  • Tsivileva OM, Pankratov AN, Nikitina VE, Garibova LV (2005) Effect of media components on the mycelial film formation in submerged culture of Lentinus edodes (Shiitake). Food Technol Biotech 43:227–234

    CAS  Google Scholar 

  • Wang B, Guo GW, Wang C, Lin Y, Wang XN, Zhao MM, Guo Y, He MH, Zhang Y, Pan L (2010a) Survey of the transcriptome of Aspergillus oryzae via massively parallel mRNA sequencing. Nucleic Acids Res 38:5075–5087

    Article  CAS  Google Scholar 

  • Wang XW, Luan JB, Li JM, Bao YY, Zhang CX, Liu SS (2010b) De novo characterization of a whitefly transcriptome and analysis of its gene expression during development. BMC Genomics 11:400

    Article  Google Scholar 

  • West AH, Stock AM (2001) Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem Sci 26:369–376

    Article  CAS  Google Scholar 

  • Wong MML, Cannon CH, Wickneswari R (2011) Identification of lignin genes and regulatory sequences involved in secondary cell wall formation in Acacia auriculiformis and Acacia mangium via de novo transcriptome sequencing. BMC Genomics 12:342

    Article  CAS  Google Scholar 

  • Wu T, Qin ZW, Zhou XY, Feng Z, Du YL (2010) Transcriptome profile analysis of floral sex determination in cucumber. J Plant Physiol 167:905–913

    Article  CAS  Google Scholar 

  • Yu JJ, Fedorova ND, Montalbano BG, Bhatnagar D, Cleveland TE, Bennett JW, Nierman WC (2011) Tight control of mycotoxin biosynthesis gene expression in Aspergillus flavus by temperature as revealed by RNA-Seq. FEMS Microbiol Lett 322:145–149

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Yin-bing Bian, Huazhong Agriculture University, for the culture experiments and technical support and Dr. John Buswell, Institute of Edible Fungi, Shanghai Academy of Agricultural Sciences, for the linguistic revision of the manuscript. This research was supported by the National Natural Science Foundation of China (grant no. 31170098), the Science and Technology Commission of the Shanghai Municipality (grant no. 10391900900), the China National Key Basic Research Program (no. 2012CB721005), and Special Capital (Edible Fungi) for the Construction of a Modern Agriculture Industry Technical System, Ministry of Agriculture of China.

Author information

Authors and Affiliations

  1. State Key Laboratory of Microbial Metabolism, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, 800 Dongchuan Road, Shanghai, 200240, People’s Republic of China

    Li-hua Tang, Hua-hua Jian, Da-qiang Wu & Xue-hong Zhang

  2. National Engineering Research Center of Edible Fungi, Key Laboratory of Edible Fungi Resources and Utilization (South), Ministry of Agriculture, Institute of Edible Fungi, Shanghai Academy of Agricultural Sciences, 1000 Jinqi Road, Shanghai, 201403, People’s Republic of China

    Li-hua Tang, Chun-yan Song, Da-peng Bao, Xiao-dong Shang & Qi Tan

Authors
  1. Li-hua Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hua-hua Jian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chun-yan Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Da-peng Bao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiao-dong Shang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Da-qiang Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Qi Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xue-hong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Qi Tan or Xue-hong Zhang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(PDF 281 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tang, Lh., Jian, Hh., Song, Cy. et al. Transcriptome analysis of candidate genes and signaling pathways associated with light-induced brown film formation in Lentinula edodes . Appl Microbiol Biotechnol 97, 4977–4989 (2013). https://doi.org/10.1007/s00253-013-4832-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-013-4832-y

Keywords

Search

Navigation