Genome Sequence of the Edible Cultivated Mushroom Lentinula edodes (Shiitake) Reveals Insights into Lignocellulose Degradation

Lentinula edodes, one of the most popular, edible mushroom species with a high content of proteins and polysaccharides as well as unique aroma, is widely cultivated in many Asian countries, especially in China, Japan and Korea. As a white rot fungus with lignocellulose degradation ability, L. edodes has the potential for application in the utilization of agriculture straw resources. Here, we report its 41.8-Mb genome, encoding 14,889 predicted genes. Through a phylogenetic analysis with model species of fungi, the evolutionary divergence time of L. edodes and Gymnopus luxurians was estimated to be 39 MYA. The carbohydrate-active enzyme genes in L. edodes were compared with those of the other 25 fungal species, and 101 lignocellulolytic enzymes were identified in L. edodes, similar to other white rot fungi. Transcriptome analysis showed that the expression of genes encoding two cellulases and 16 transcription factor was up-regulated when mycelia were cultivated for 120 minutes in cellulose medium versus glucose medium. Our results will foster a better understanding of the molecular mechanism of lignocellulose degradation and provide the basis for partial replacement of wood sawdust with agricultural wastes in L. edodes cultivation.

[1]  C. P. Hong,et al.  Whole genome de novo sequencing and genome annotation of the world popular cultivated edible mushroom, Lentinula edodes. , 2016, Journal of biotechnology.

[2]  A. V. van Peer,et al.  Grouping of multicopper oxidases in Lentinula edodes by sequence similarities and expression patterns , 2015, AMB Express.

[3]  D. Cullen,et al.  Regulation of Gene Expression during the Onset of Ligninolytic Oxidation by Phanerochaete chrysosporium on Spruce Wood , 2015, Applied and Environmental Microbiology.

[4]  Y. Liu,et al.  A novel cysteine desulfurase influencing organosulfur compounds in Lentinula edodes , 2015, Scientific Reports.

[5]  U. Kües Fungal enzymes for environmental management. , 2015, Current opinion in biotechnology.

[6]  Bernard Henrissat,et al.  Convergent losses of decay mechanisms and rapid turnover of symbiosis genes in mycorrhizal mutualists , 2015, Nature Genetics.

[7]  Steven L Salzberg,et al.  HISAT: a fast spliced aligner with low memory requirements , 2015, Nature Methods.

[8]  Huaiyu Mi,et al.  The InterPro protein families database: the classification resource after 15 years , 2014, Nucleic Acids Res..

[9]  A. Pandey,et al.  A psychrotolerant strain of Serratia marcescens (MTCC 4822) produces laccase at wide temperature and pH range , 2015, AMB Express.

[10]  N. Bouqellah,et al.  Cultivation of oyster mushroom Pleurotus ostreatus on date-palm leaves mixed with other agro-wastes in Saudi Arabia. , 2014, Saudi journal of biological sciences.

[11]  G. Mata,et al.  Improvement of yield of the edible and medicinal mushroom Lentinula edodes on wheat straw by use of supplemented spawn , 2014, Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology].

[12]  A. Salamov,et al.  Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi , 2014, Proceedings of the National Academy of Sciences.

[13]  Seonwook Lee,et al.  Whole Genome and Global Gene Expression Analyses of the Model Mushroom Flammulina velutipes Reveal a High Capacity for Lignocellulose Degradation , 2014, PloS one.

[14]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[15]  M. Cheung,et al.  Constructing a new integrated genetic linkage map and mapping quantitative trait loci for vegetative mycelium growth rate in Lentinula edodes. , 2014, Fungal biology.

[16]  C. Au,et al.  The genetic structure of the A mating-type locus of Lentinula edodes. , 2014, Gene.

[17]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[18]  Peng Wei-hong,et al.  A preliminary screening of alternative substrate for cultivation of Flammulina velutipes. , 2014 .

[19]  Q. Tan,et al.  Cloning of the Lentinula edodes B mating-type locus and identification of the genetic structure controlling B mating. , 2013, Gene.

[20]  Monica C Munoz-Torres,et al.  Web Apollo: a web-based genomic annotation editing platform , 2013, Genome Biology.

[21]  Jianying Yuan,et al.  Estimation of genomic characteristics by analyzing k-mer frequency in de novo genome projects , 2013, 1308.2012.

[22]  Mira V. Han,et al.  Estimating gene gain and loss rates in the presence of error in genome assembly and annotation using CAFE 3. , 2013, Molecular biology and evolution.

[23]  I. Castellano,et al.  Gamma-Glutamyl Transpeptidases: Structure and Function , 2013 .

[24]  M. Cheung,et al.  A Novel Lentinula edodes Laccase and Its Comparative Enzymology Suggest Guaiacol-Based Laccase Engineering for Bioremediation , 2013, PloS one.

[25]  Shengyue Wang,et al.  Sequencing and Comparative Analysis of the Straw Mushroom (Volvariella volvacea) Genome , 2013, PloS one.

[26]  Baogui Xie,et al.  Composition and Expression of Genes Encoding Carbohydrate-Active Enzymes in the Straw-Degrading Mushroom Volvariella volvacea , 2013, PloS one.

[27]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[28]  Narmada Thanki,et al.  CDD: conserved domains and protein three-dimensional structure , 2012, Nucleic Acids Res..

[29]  Shilin Chen,et al.  FastUniq: A Fast De Novo Duplicates Removal Tool for Paired Short Reads , 2012, PloS one.

[30]  Vincent Lombard,et al.  Genome sequence of the button mushroom Agaricus bisporus reveals mechanisms governing adaptation to a humic-rich ecological niche , 2012, Proceedings of the National Academy of Sciences.

[31]  Alberto Policriti,et al.  GapFiller: a de novo assembly approach to fill the gap within paired reads , 2012, BMC Bioinformatics.

[32]  Albee Y. Ling,et al.  The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes , 2012, Science.

[33]  Mira V. Han,et al.  Genome sequence of the model medicinal mushroom Ganoderma lucidum , 2012, Nature Communications.

[34]  Xin Chen,et al.  dbCAN: a web resource for automated carbohydrate-active enzyme annotation , 2012, Nucleic Acids Res..

[35]  Steven L Salzberg,et al.  Fast gapped-read alignment with Bowtie 2 , 2012, Nature Methods.

[36]  David R. Kelley,et al.  Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks , 2012, Nature Protocols.

[37]  Mukesh Jain,et al.  NGS QC Toolkit: A Toolkit for Quality Control of Next Generation Sequencing Data , 2012, PloS one.

[38]  P. Y. Yip,et al.  Genome sequence and genetic linkage analysis of Shiitake mushroom Lentinula edodes , 2012 .

[39]  C. Au,et al.  Biodegradation of dyes and polyaromatic hydrocarbons by two allelic forms of Lentinula edodes laccase expressed from Pichia pastoris. , 2012, Bioresource technology.

[40]  A. Ben-Hur,et al.  METHOD Open Access , 2014 .

[41]  Brenda J. Smith,et al.  Differential effects of shiitake- and white button mushroom-supplemented diets on hepatic steatosis in C57BL/6 mice. , 2011, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[42]  Christina A Cuomo,et al.  Approaches to Fungal Genome Annotation , 2011, Mycology.

[43]  A. Salamov,et al.  The Plant Cell Wall–Decomposing Machinery Underlies the Functional Diversity of Forest Fungi , 2011, Science.

[44]  A. Gnirke,et al.  High-quality draft assemblies of mammalian genomes from massively parallel sequence data , 2010, Proceedings of the National Academy of Sciences.

[45]  Vincent Lombard,et al.  Genome sequence of the model mushroom Schizophyllum commune , 2010, Nature Biotechnology.

[46]  Adel Dayarian,et al.  SOPRA: Scaffolding algorithm for paired reads via statistical optimization , 2010, BMC Bioinformatics.

[47]  Matthew Berriman,et al.  Iterative Correction of Reference Nucleotides (iCORN) using second generation sequencing technology , 2010, Bioinform..

[48]  Q. Zeng,et al.  Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus) , 2010, Proceedings of the National Academy of Sciences.

[49]  Ning Ma,et al.  BLAST+: architecture and applications , 2009, BMC Bioinformatics.

[50]  Steven J. M. Jones,et al.  Abyss: a Parallel Assembler for Short Read Sequence Data Material Supplemental Open Access , 2022 .

[51]  Jill Gaskell,et al.  Transcriptome and Secretome Analyses of Phanerochaete chrysosporium Reveal Complex Patterns of Gene Expression , 2009, Applied and Environmental Microbiology.

[52]  A. Salamov,et al.  Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion , 2009, Proceedings of the National Academy of Sciences.

[53]  Brandi L. Cantarel,et al.  The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics , 2008, Nucleic Acids Res..

[54]  K. Martin,et al.  The effects of whole mushrooms during inflammation , 2009, BMC Immunology.

[55]  M. Borodovsky,et al.  Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. , 2008, Genome research.

[56]  M. Robles,et al.  University of Birmingham High throughput functional annotation and data mining with the Blast2GO suite , 2022 .

[57]  Yong-Hwan Lee,et al.  FTFD: an informatics pipeline supporting phylogenomic analysis of fungal transcription factors , 2008, Bioinform..

[58]  Y. Van de Peer,et al.  The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis , 2008, Nature.

[59]  Sofia M. C. Robb,et al.  MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. , 2007, Genome research.

[60]  H. Kwan,et al.  Isolation and transcript analysis of two-component histidine kinase gene Le.nik1 in Shiitake mushroom, Lentinula edodes. , 2008, Mycological research.

[61]  Peter F. Hallin,et al.  RNAmmer: consistent and rapid annotation of ribosomal RNA genes , 2007, Nucleic acids research.

[62]  M. Beltran-Garcia,et al.  Bioconversion of agrowastes by Lentinula edodes: the high potential of viticulture residues , 2005, Applied Microbiology and Biotechnology.

[63]  M. Mizuno,et al.  Characterization of the Lentinula edodesexg2 gene encoding a lentinan-degrading exo-β-1,3-glucanase , 2005, Current Genetics.

[64]  Burkhard Morgenstern,et al.  AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints , 2005, Nucleic Acids Res..

[65]  Sean R. Eddy,et al.  Rfam: annotating non-coding RNAs in complete genomes , 2004, Nucleic Acids Res..

[66]  G. Mata,et al.  Cultivation of the Dible Mushroom Lentinula edodes (Shiitake) in Pasteurized Wheat Straw – Alternative Use of Georthermal Energy in Mexico , 2004 .

[67]  Katherine H. Huang,et al.  Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78 , 2004, Nature Biotechnology.

[68]  Ian Korf,et al.  Gene finding in novel genomes , 2004, BMC Bioinformatics.

[69]  Amos Bairoch,et al.  Swiss-Prot: Juggling between evolution and stability , 2004, Briefings Bioinform..

[70]  M. Hiraide,et al.  The smell and odorous components of dried shiitake mushroom, Lentinula edodes I: relationship between sensory evaluations and amounts of odorous components , 2004, Journal of Wood Science.

[71]  Stephen M. Mount,et al.  Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. , 2003, Nucleic acids research.

[72]  Darren A. Natale,et al.  The COG database: an updated version includes eukaryotes , 2003, BMC Bioinformatics.

[73]  C. Stoeckert,et al.  OrthoMCL: identification of ortholog groups for eukaryotic genomes. , 2003, Genome research.

[74]  Michael J. Sanderson,et al.  R8s: Inferring Absolute Rates of Molecular Evolution, Divergence times in the Absence of a Molecular Clock , 2003, Bioinform..

[75]  Alexander E. Kel,et al.  TRANSFAC®: transcriptional regulation, from patterns to profiles , 2003, Nucleic Acids Res..

[76]  E. Albertó,et al.  Cultivation of shiitake using sawdust from Widely available local woods in Argentina , 2001 .

[77]  Wei Qian,et al.  Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. , 2000, Molecular biology and evolution.

[78]  Michael Y. Galperin,et al.  The COG database: a tool for genome-scale analysis of protein functions and evolution , 2000, Nucleic Acids Res..

[79]  Shu-Ting Chang World production of cultivated edible and medicinal mushrooms in 1997 with emphasis on Lentinus edodes (Berk.) Sing. in China. , 1999 .

[80]  S. Eddy,et al.  tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. , 1997, Nucleic acids research.

[81]  Akiyasu C. Yoshizawa,et al.  KAAS: an automatic genome annotation and pathway reconstruction server , 2007, Environmental health perspectives.

[82]  J. Buswell,et al.  Mushroom nutriceuticals , 1996, World journal of microbiology & biotechnology.

[83]  P. Morales,et al.  Cultivation of Lentinula edodes in Mexico. , 1990 .

[84]  H. Mitsuda,et al.  Enzyme-catalized Evolution of Lenthionine from Lentinic Acid , 1971 .