Mycological Progress

, Volume 17, Issue 8, pp 871–883 | Cite as

Comparative genome and transcriptome analysis reveal the medicinal basis and environmental adaptation of artificially cultivated Taiwanofungus camphoratus

  • Lingyu Yang
  • Rongliang Guan
  • Yixiang Shi
  • Jinmei Ding
  • Ronghua Dai
  • Weixing Ye
  • Ke Xu
  • Yu Chen
  • Li Shen
  • Yanyan Liu
  • Fangmei Ding
  • Chuan He
  • He Meng
Original Article


Taiwanofungus camphoratus is a widely used medicinal macrofungus unique to Taiwan, China, and it produces a diverse set of bioactive compounds. In this study, we resequenced the genome and transcriptome of artificially cultivated Taiwanofungus camphoratus and obtained its 29.7-Mb genome. Our aim was to elucidate the possible reasons for its medicinal value and its environmental adaptation from the genomic and evolutionary perspective. Compounds of triterpenoid family are highly abundant in Taiwanofungus camphoratus, and we identified 25 candidate genes that participated in the secondary metabolism leading to these valuable products. We observed fewer genes relating to the CAZymes family in Taiwanofungus camphoratus than in Ganoderma lucidum and Postia placenta, and these genes are considered beneficial for survival. Transcriptome sequencing revealed a large number of differentially expressed genes at various growth stages of Taiwanofungus camphoratus. Our data will be useful for studying the environmental adaptation of Taiwanofungus camphoratus and for developing a strategy to increase the production of its useful secondary metabolites.


Taiwanofungus camphoratus Genome Transcriptome Triterpenoid production Environment adaptation 



This study was supported by the National Science Foundation of China (grant No. 31572384) and the National High Technology Research and Development Program of China (grant No. 2011AA100901).

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  1. Al-Samarrai T, Schmid J (2000) A simple method for extraction of fungal genomic DNA. Lett Appl Microbiol 30:53–56CrossRefPubMedGoogle Scholar
  2. Amadou C et al (2008) Genome sequence of the β-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Res 18:1472–1483. CrossRefPubMedPubMedCentralGoogle Scholar
  3. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:1. CrossRefGoogle Scholar
  4. Andrew PJ, Mayer B (1999) Enzymatic function of nitric oxide synthases. Cardiovasc Res 43:521–531CrossRefPubMedGoogle Scholar
  5. Burge SW et al (2012) Rfam 11.0: 10 years of RNA families. Nucleic Acids Res 41:D226–D232CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cai TB, Lu D, Tang X, Zhang Y, Landerholm M, Wang PG (2005) New glycosidase activated nitric oxide donors: glycose and 3-morphorlinosydnonimine conjugates. J Org Chem 70:3518–3524. CrossRefPubMedGoogle Scholar
  7. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, Henrissat B (2009) The carbohydrate-active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 37:D233–D238CrossRefPubMedGoogle Scholar
  8. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552CrossRefPubMedGoogle Scholar
  9. Chaisson MJ, Pevzner PA (2008) Short read fragment assembly of bacterial genomes. Genome Res 18:324–330. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Chang T, Chou W (1995) Antrodia cinnamomea sp. nov. on Cinnamomum kanehirai in Taiwan. Mycol Res 99:756–758CrossRefGoogle Scholar
  11. Chang C-J et al (2015) Ganoderma lucidum reduces obesity in mice by modulating the composition of the gut microbiota. Nat Commun 6:7489. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Chen C-C et al (2006) Neuroprotective Diterpenes from the fruiting body of Antrodia camphorata. J Nat Prod 69:689–691CrossRefPubMedGoogle Scholar
  13. Chen Y-J, Cheng P-C, Lin C-N, Liao H-F, Chen Y-Y, Chen C-C, Lee K-M (2008) Polysaccharides from Antrodia camphorata mycelia extracts possess immunomodulatory activity and inhibits infection of Schistosoma mansoni. Int Immunopharmacol 8:458–467CrossRefPubMedGoogle Scholar
  14. Chen S et al (2012) Genome sequence of the model medicinal mushroom Ganoderma lucidum. Nat Commun 3:913. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Chen Y-T, Hong P-F, Wen L, Lin C-T (2014) Molecular cloning and characterization of a thioredoxin from Taiwanofungus camphorata. Bot Stud 55(1).
  16. Conesa A, Götz S (2008) Blast2GO: a comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics 2008:619832CrossRefPubMedGoogle Scholar
  17. Consortium GO (2004) The gene ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258–D261CrossRefGoogle Scholar
  18. Darling AC, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165CrossRefPubMedPubMedCentralGoogle Scholar
  20. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797CrossRefPubMedPubMedCentralGoogle Scholar
  21. Finn RD et al (2013) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230CrossRefPubMedPubMedCentralGoogle Scholar
  22. Fischer S et al (2011) Using OrthoMCL to assign proteins to OrthoMCL-DB groups or to cluster proteomes into new Ortholog groups. Curr Protoc Bioinformatics:6.12 11–16.12. 19.
  23. Fujiwara Y, Takeya M, Komohara Y (2014) A novel strategy for inducing the antitumor effects of triterpenoid compounds: blocking the protumoral functions of tumor-associated macrophages via STAT3 inhibition. Biomed Res Int 2014:348539PubMedPubMedCentralGoogle Scholar
  24. Gao Q et al (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet 7:e1001264CrossRefPubMedPubMedCentralGoogle Scholar
  25. Geethangili M, Tzeng Y-M (2011) Review of pharmacological effects of Antrodia camphorata and its bioactive compounds. Evid Based Complement Alternat Med 2011:212641CrossRefPubMedPubMedCentralGoogle Scholar
  26. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321CrossRefPubMedGoogle Scholar
  27. Haas BJ et al (2008) Automated eukaryotic gene structure annotation using EVidenceModeler and the program to assemble spliced alignments. Genome Biol 9:1. CrossRefGoogle Scholar
  28. Hahn MW, De Bie T, Stajich JE, Nguyen C, Cristianini N (2005) Estimating the tempo and mode of gene family evolution from comparative genomic data. Genome Res 15:1153–1160. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Han L-T, Li J, Huang F, Yu S-G, Fang N-B (2009) Triterpenoid saponins from Anemone flaccida induce apoptosis activity in HeLa cells. J Asian Nat Prod Res 11:122–127CrossRefPubMedGoogle Scholar
  30. Harris MA et al (2004) The gene ontology (GO) database and informatics resource. Nucleic Acids Res 32:D258–D261. CrossRefPubMedGoogle Scholar
  31. Hattori M, Sheu C-C (2006) Compounds from Antrodia camphorata having anti-inflammatory and anti-tumor activity. US PatentsGoogle Scholar
  32. Huang C-Y, Chen Y-T, Wen L, Sheu D-C, Lin C-T (2014) A peroxiredoxin cDNA from Taiwanofungus camphorata: role of Cys31 in dimerization. Mol Biol Rep 41:155–164. CrossRefPubMedGoogle Scholar
  33. Huber W et al (2015) Orchestrating high-throughput genomic analysis with Bioconductor. Nat Methods 12:115–121. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Jones MG (2007) The first filamentous fungal genome sequences: aspergillus leads the way for essential everyday resources or dusty museum specimens? Microbiology 153:1–6. CrossRefPubMedGoogle Scholar
  35. Jones P et al (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240CrossRefPubMedPubMedCentralGoogle Scholar
  36. Kanehisa M, Goto S (2000) KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Kapitonov VV, Jurka J (2008) A universal classification of eukaryotic transposable elements implemented in Repbase. Nat Rev Genet 9:411–412. CrossRefPubMedGoogle Scholar
  38. Lagesen K, Hallin P, Rødland EA, Stærfeldt H-H, Rognes T, Ussery DW (2007) RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 35:3100–3108. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:1. CrossRefGoogle Scholar
  40. Lee C-L et al (2011) First total synthesis of antrocamphin a and its analogs as anti-inflammatory and anti-platelet aggregation agents. Org Biomol Chem 9:70–73CrossRefPubMedGoogle Scholar
  41. Lee K-H et al (2012) Recent progress of research on medicinal mushrooms, foods, and other herbal products used in traditional Chinese medicine. J Tradit Complement Med 2:1–12CrossRefPubMedPubMedCentralGoogle Scholar
  42. Li H et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079CrossRefPubMedPubMedCentralGoogle Scholar
  43. Li R et al (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272CrossRefPubMedPubMedCentralGoogle Scholar
  44. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964CrossRefPubMedPubMedCentralGoogle Scholar
  45. Lu M-YJ et al (2014) Genomic and transcriptomic analyses of the medicinal fungus Antrodia cinnamomea for its metabolite biosynthesis and sexual development. Proc Natl Acad Sci 111:4743–4752. CrossRefGoogle Scholar
  46. Martinez D et al (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci 106:1954–1959. CrossRefPubMedGoogle Scholar
  47. Meldrum BS (2000) Glutamate as a neurotransmitter in the brain: review of physiology and pathology. J Nutr 130:1007S–1015SCrossRefPubMedGoogle Scholar
  48. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35:W182–W185CrossRefPubMedPubMedCentralGoogle Scholar
  49. Ortiz-Santana B, Lindner DL, Miettinen O, Justo A, Hibbett DS (2013) A phylogenetic overview of the antrodia clade (Basidiomycota, Polyporales). Mycologia 105:1391–1411CrossRefPubMedGoogle Scholar
  50. Parra G, Bradnam K, Korf I (2007) CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 23:1061–1067CrossRefPubMedGoogle Scholar
  51. Powell S et al (2012) eggNOG v3. 0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic Acids Res 40:D284–D289CrossRefPubMedGoogle Scholar
  52. Rosenheim O, Webster TA (1928) The specificity of ergosterol as parent substance of vitamin D. Biochem J 22:762CrossRefPubMedPubMedCentralGoogle Scholar
  53. Sanodiya BS, Thakur GS, Baghel RK, Prasad G, Bisen P (2009) Ganoderma lucidum: a potent pharmacological macrofungus. Curr Pharm Biotechnol 10:717–742CrossRefPubMedGoogle Scholar
  54. Stanke M, Morgenstern B (2005) AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res 33:W465–W467CrossRefPubMedPubMedCentralGoogle Scholar
  55. Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 34:W609–W612CrossRefPubMedPubMedCentralGoogle Scholar
  56. Tatusov RL et al (2003) The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4:1CrossRefGoogle Scholar
  57. Tempel S (2012) Using and understanding RepeatMasker. Mobile Genetic Elements. 859:29–51.
  58. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25:1105–1111CrossRefPubMedPubMedCentralGoogle Scholar
  59. Trapnell C et al (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515. CrossRefPubMedPubMedCentralGoogle Scholar
  60. Tsai T-C et al (2015) Anti-inflammatory effects of Antrodia camphorata, a herbal medicine, in a mouse skin ischemia model. J Ethnopharmacol 159:113–121CrossRefPubMedGoogle Scholar
  61. Wu S-H et al (2004) Taiwanofungus, a polypore new genus. Fungal Sci 19:109–116Google Scholar
  62. Yang Z (2007) PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24:1586–1591CrossRefPubMedGoogle Scholar
  63. Yeh C-T et al (2009) Cytotoxic triterpenes from Antrodia camphorata and their mode of action in HT-29 human colon cancer cells. Cancer Lett 285:73–79CrossRefPubMedGoogle Scholar
  64. Yu Z-H, Wu S-H, Wang D-M, Chen C-T (2010) Phylogenetic relationships of Antrodia species and related taxa based on analyses of nuclear large subunit ribosomal DNA sequences. Bot Stud 51:1586–1591Google Scholar

Copyright information

© German Mycological Society and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Lingyu Yang
    • 1
  • Rongliang Guan
    • 2
  • Yixiang Shi
    • 3
  • Jinmei Ding
    • 1
  • Ronghua Dai
    • 1
  • Weixing Ye
    • 3
  • Ke Xu
    • 1
  • Yu Chen
    • 2
  • Li Shen
    • 3
  • Yanyan Liu
    • 3
  • Fangmei Ding
    • 3
  • Chuan He
    • 1
  • He Meng
    • 1
  1. 1.School of Agriculture and BiologyShanghai Jiao Tong University, Shanghai Key Laboratory of Veterinary BiotechnologyShanghaiPeople’s Republic of China
  2. 2.Shanghai Qinshengyuan Biotechnology Limited CompanyShanghaiPeople’s Republic of China
  3. 3.Shanghai Personal Biotechnology Limited CompanyShanghaiPeople’s Republic of China

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