Deep insight into the Ganoderma lucidum by comprehensive analysis of its transcriptome

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Yu, Guo Jun ^a   Wang, Man ^a   Huang, Jie ^a   Yin, Ya Lin ^a   Chen, Yi Jie ^a   Jiang, Shuai ^a   Jin, Yan Xia ^a   Lan, Xian Qing ^a   Wong, Barry Hon Cheung ^a   Liang, Yi ^a,b   Sun, Hui ^a,c  

^a WUHAN UNIVERSITY   (China)

^b GUANGDONG MEDICAL UNIVERSITY   (China)

^c HUBEI UNIVERSITY OF TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE ACTIVE ENZYME; FUNGAL ENZYME; FUNGAL OXIDATIVE LIGNIN ENZYME; LIGNOCELLULOSE; TERPENOID; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; ENZYMATIC DEGRADATION; FRUITING BODY; FUNGAL GENE; FUNGAL GENOME; GANODERMA LUCIDUM; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC ANALYSIS; GENETIC DATABASE; HIGH THROUGHPUT SEQUENCING; ILLUMINA SEQUENCING TECHNOLOGY; MYCELIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; QUANTITATIVE REAL TIME POLYMERASE CHAIN REACTION; REAL TIME POLYMERASE CHAIN REACTION; TRANSCRIPTOMICS; UNIGENE; UPREGULATION;

DATABASES, GENETIC; FRUITING BODIES, FUNGAL; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; METABOLIC NETWORKS AND PATHWAYS; MOLECULAR SEQUENCE ANNOTATION; PROTEIN STRUCTURE, TERTIARY; REISHI; SEQUENCE ANALYSIS, DNA; TRANSCRIPTOME; TRITERPENES; WOOD;

EID: 84865421038     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044031     Document Type: Article

References (83)

1. Paterson RR, (2006) Ganoderma- a therapeutic fungal biofactory. Phytochemistry 67: 1985-2001.
2. Sanodiya BS, Thakur GS, Baghel RK, Prasad GB, Bisen PS, (2009) Ganoderma lucidum: a potent pharmacological macrofungus. Curr Pharm Biotechnol 10: 717-742.
3. Gao Y, Zhou S, Wen J, Huang M, Xu A, (2002) Mechanism of the antiulcerogenic effect of Ganoderma lucidum polysaccharides on indomethacin-induced lesions in the rat. Life Sci 72: 731-745.
4. Wasser SP, Weis AL, (1999) Therapeutic effects of substances occurring in higher Basidiomycetes mushrooms: a modern perspective. Crit Rev Immunol 19: 65-96.
5. Ko HH, Hung CF, Wang JP, Lin CN, (2008) Antiinflammatory triterpenoids and steroids from Ganoderma lucidum and G. tsugae. Phytochemistry 69: 234-239.
6. Ko EM, Leem YE, Choi HT, (2001) Purification and characterization of laccase isozymes from the white-rot basidiomycete Ganoderma lucidum. Appl Microbiol Biotechnol 57: 98-102.
7. Wang HX, Ng TB, (2006) A laccase from the medicinal mushroom Ganoderma lucidum. Appl Microbiol Biotechnol 72: 508-513.
8. Levasseur A, Piumi F, Coutinho PM, Rancurel C, Asther M, et al. (2008) FOLy: an integrated database for the classification and functional annotation of fungal oxidoreductases potentially involved in the degradation of lignin and related aromatic compounds. Fungal Genet Biol 45: 638-645.
9. Zhou X, Lin J, Yin Y, Zhao J, Sun X, et al. (2007) Ganodermataceae: natural products and their related pharmacological functions. Am J Chin Med 35: 559-574.
10. Bao X, Liu C, Fang J, Li X, (2001) Structural and immunological studies of a major polysaccharide from spores of Ganoderma lucidum (Fr.) Karst. Carbohydr Res 332: 67-74.
11. Zhang CR, Yang SP, Yue JM, (2008) Sterols and triterpenoids from the spores of Ganoderma lucidum. Nat Prod Res 22: 1137-1142.
12. Kino K, Yamashita A, Yamaoka K, Watanabe J, Tanaka S, et al. (1989) Isolation and characterization of a new immunomodulatory protein, ling zhi-8 (LZ-8), from Ganoderma lucidium. J Biol Chem 264: 472-478.
13. Bao XF, Wang XS, Dong Q, Fang JN, Li XY, (2002) Structural features of immunologically active polysaccharides from Ganoderma lucidum. Phytochemistry 59: 175-181.
14. Bao XF, Dong Q, Fang JN, (2000) Structure and Conformation Behavior of a Glucan from Spores of Ganoderma lucidum (Fr.) Karst. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai) 32: 557-561.
15. Chan WK, Cheung CC, Law HK, Lau YL, Chan GC, (2008) Ganoderma lucidum polysaccharides can induce human monocytic leukemia cells into dendritic cells with immuno-stimulatory function. J Hematol Oncol 1: 9.
16. Cheng KC, Huang HC, Chen JH, Hsu JW, Cheng HC, et al. (2007) Ganoderma lucidum polysaccharides in human monocytic leukemia cells: from gene expression to network construction. BMC Genomics 8: 411.
17. Gao Y, Gao H, Chan E, Tang W, Xu A, et al. (2005) Antitumor activity and underlying mechanisms of ganopoly, the refined polysaccharides extracted from Ganoderma lucidum, in mice. Immunol Invest 34: 171-198.
18. Guo L, Xie J, Ruan Y, Zhou L, Zhu H, et al. (2009) Characterization and immunostimulatory activity of a polysaccharide from the spores of Ganoderma lucidum. Int Immunopharmacol 9: 1175-1182.
19. Dudhgaonkar S, Thyagarajan A, Sliva D, (2009) Suppression of the inflammatory response by triterpenes isolated from the mushroom Ganoderma lucidum. Int Immunopharmacol 9: 1272-1280.
20. Kimura Y, Taniguchi M, Baba K, (2002) Antitumor and antimetastatic effects on liver of triterpenoid fractions of Ganoderma lucidum: mechanism of action and isolation of an active substance. Anticancer Res 22: 3309-3318.
21. Huie CW, (2002) A review of modern sample-preparation techniques for the extraction and analysis of medicinal plants. Anal Bioanal Chem 373: 23-30.
22. Luo J, Lin ZB, (2002) [Advances of pharmacological effects of triterpenes from Ganoderma lucidum]. Yao Xue Xue Bao 37: 574-578.
23. Xu JW, Zhao W, Zhong JJ, (2010) Biotechnological production and application of ganoderic acids. Appl Microbiol Biotechnol 87: 457-466.
24. Kino K, Sone T, Watanabe J, Yamashita A, Tsuboi H, et al. (1991) Immunomodulator, LZ-8, prevents antibody production in mice. Int J Immunopharmacol 13: 1109-1115.
25. Tanaka S, Ko K, Kino K, Tsuchiya K, Yamashita A, et al. (1989) Complete amino acid sequence of an immunomodulatory protein, ling zhi-8 (LZ-8). An immunomodulator from a fungus, Ganoderma lucidium, having similarity to immunoglobulin variable regions. J Biol Chem 264: 16372-16377.
26. Huang L, Sun F, Liang C, He YX, Bao R, et al. (2009) Crystal structure of LZ-8 from the medicinal fungus Ganoderma lucidium. Proteins 75: 524-527.
27. Kino K, Mizumoto K, Sone T, Yamaji T, Watanabe J, et al. (1990) An immunomodulating protein, Ling Zhi-8 (LZ-8) prevents insulitis in non-obese diabetic mice. Diabetologia 33: 713-718.
28. Liang C, Li H, Zhou H, Zhang S, Liu Z, et al. (2011) Recombinant Lz-8 from Ganoderma lucidum induces endoplasmic reticulum cancer cells. Oncol Rep.
29. Lyashenko AV, Belova O, Gabdulkhakov AG, Lashkov AA, Lisov AV, et al. (2011) Purification, crystallization and preliminary X-ray structure analysis of the laccase from Ganoderma lucidum. Acta Crystallogr Sect F Struct Biol Cryst Commun 67: 926-929.
30. MacLean D, Jones JD, Studholme DJ, (2009) Application of 'next-generation' sequencing technologies to microbial genetics. Nat Rev Microbiol 7: 287-296.
31. Pop M, Salzberg SL, (2008) Bioinformatics challenges of new sequencing technology. Trends Genet 24: 142-149.
32. Trombetti GA, Bonnal RJ, Rizzi E, De Bellis G, Milanesi L, (2007) Data handling strategies for high throughput pyrosequencers. BMC Bioinformatics 8Suppl 1: S22.
33. Gibbons JG, Janson EM, Hittinger CT, Johnston M, Abbot P, et al. (2009) Benchmarking next-generation transcriptome sequencing for functional and evolutionary genomics. Mol Biol Evol 26: 2731-2744.
34. Human genome: Genomes by the thousand. Nature 467: 1026-1027.
35. Ekker SC, Stemple DL, Clark M, Chien CB, Rasooly RS, et al. (2007) Zebrafish genome project: bringing new biology to the vertebrate genome field. Zebrafish 4: 239-251.
36. Hayashizaki Y, (2003) Mouse Genome Encyclopedia Project. Cold Spring Harb Symp Quant Biol 68: 195-204.
37. Walbot V, (2000) Arabidopsis thaliana genome. A green chapter in the book of life. Nature 408: 794-795.
38. Goff SA, Ricke D, Lan TH, Presting G, Wang R, et al. (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296: 92-100.
39. Martinez D, Larrondo LF, Putnam N, Gelpke MD, Huang K, et al. (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22: 695-700.
40. Vanden Wymelenberg A, Minges P, Sabat G, Martinez D, Aerts A, et al. (2006) Computational analysis of the Phanerochaete chrysosporium v2.0 genome database and mass spectrometry identification of peptides in ligninolytic cultures reveal complex mixtures of secreted proteins. Fungal Genet Biol 43: 343-356.
41. Sato S, Feltus FA, Iyer P, Tien M, (2009) The first genome-level transcriptome of the wood-degrading fungus Phanerochaete chrysosporium grown on red oak. Curr Genet 55: 273-286.
42. Jeffries TW, Grigoriev IV, Grimwood J, Laplaza JM, Aerts A, et al. (2007) Genome sequence of the lignocellulose-bioconverting and xylose-fermenting yeast Pichia stipitis. Nat Biotechnol 25: 319-326.
43. Martinez D, Berka RM, Henrissat B, Saloheimo M, Arvas M, et al. (2008) Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nat Biotechnol 26: 553-560.
44. Martin F, Aerts A, Ahren D, Brun A, Danchin EG, et al. (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452: 88-92.
45. Larsen PE, Trivedi G, Sreedasyam A, Lu V, Podila GK, et al. (2010) Using deep RNA sequencing for the structural annotation of the Laccaria bicolor mycorrhizal transcriptome. PLoS One 5: e9780.
46. Li S, Zhang X, Yin T, (2010) Characteristics of microsatellites in the transcript sequences of the Laccaria bicolor genome. J Microbiol Biotechnol 20: 474-479.
47. Vanden Wymelenberg A, Gaskell J, Mozuch M, Sabat G, Ralph J, et al. (2010) Comparative transcriptome and secretome analysis of wood decay fungi Postia placenta and Phanerochaete chrysosporium. Appl Environ Microbiol 76: 3599-3610.
48. Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, et al. (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci U S A 106: 1954-1959.
49. Stajich JE, Wilke SK, Ahren D, Au CH, Birren BW, et al. (2010) Insights into evolution of multicellular fungi from the assembled chromosomes of the mushroom Coprinopsis cinerea (Coprinus cinereus). Proc Natl Acad Sci U S A 107: 11889-11894.
50. Ohm RA, de Jong JF, Lugones LG, Aerts A, Kothe E, et al. (2010) Genome sequence of the model mushroom Schizophyllum commune. Nat Biotechnol 28: 957-963.
51. Bai X, Mamidala P, Rajarapu SP, Jones SC, Mittapalli O, (2011) Transcriptomics of the bed bug (Cimex lectularius). PLoS One 6: e16336.
52. Xue J, Bao YY, Li BL, Cheng YB, Peng ZY, et al. (2010) Transcriptome analysis of the brown planthopper Nilaparvata lugens. PLoS One 5: e14233.
53. Wang XW, Luan JB, Li JM, Bao YY, Zhang CX, et al. (2010) De novo characterization of a whitefly transcriptome and analysis of its gene expression during development. BMC Genomics 11: 400.
54. Rismani-Yazdi H, Haznedaroglu BZ, Bibby K, Peccia J, (2011) Transcriptome sequencing and annotation of the microalgae Dunaliella tertiolecta: pathway description and gene discovery for production of next-generation biofuels. BMC Genomics 12: 148.
55. Shi CY, Yang H, Wei CL, Yu O, Zhang ZZ, et al. (2011) Deep sequencing of the Camellia sinensis transcriptome revealed candidate genes for major metabolic pathways of tea-specific compounds. BMC Genomics 12: 131.
56. Shen GM, Dou W, Niu JZ, Jiang HB, Yang WJ, et al. (2011) Transcriptome analysis of the oriental fruit fly (Bactrocera dorsalis). PLoS One 6: e29127.
57. Luo H, Sun C, Song J, Lan J, Li Y, et al. (2010) Generation and analysis of expressed sequence tags from a cDNA library of the fruiting body of Ganoderma lucidum. Chin Med 5: 9.
58. Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, et al. (2012) The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 40: D26-32.
59. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.
60. Ding N, Yang Q, Huang SS, Fan LY, Zhang W, et al. (2010) Separation and determination of four ganoderic acids from dried fermentation mycelia powder of Ganoderma lucidum by capillary zone electrophoresis. J Pharm Biomed Anal 53: 1224-1230.
61. Jiang J, Grieb B, Thyagarajan A, Sliva D, (2008) Ganoderic acids suppress growth and invasive behavior of breast cancer cells by modulating AP-1 and NF-kappaB signaling. Int J Mol Med 21: 577-584.
62. Liu J, Shiono J, Shimizu K, Kondo R, (2010) Ganoderic acids from Ganoderma lucidum: inhibitory activity of osteoclastic differentiation and structural criteria. Planta Med 76: 137-139.
63. Wanke M, Skorupinska-Tudek K, Swiezewska E, (2001) Isoprenoid biosynthesis via 1-deoxy-D-xylulose 5-phosphate/2-C-methyl-D-erythritol 4-phosphate (DOXP/MEP) pathway. Acta Biochim Pol 48: 663-672.
64. Rodriguez-Concepcion M, (2004) The MEP pathway: a new target for the development of herbicides, antibiotics and antimalarial drugs. Curr Pharm Des 10: 2391-2400.
65. Shang CH, Zhu F, Li N, Ou-Yang X, Shi L, et al. (2008) Cloning and characterization of a gene encoding HMG-CoA reductase from Ganoderma lucidum and its functional identification in yeast. Biosci Biotechnol Biochem 72: 1333-1339.
66. Ding YX, Ou-Yang X, Shang CH, Ren A, Shi L, et al. (2008) Molecular cloning, characterization, and differential expression of a farnesyl-diphosphate synthase gene from the basidiomycetous fungus Ganoderma lucidum. Biosci Biotechnol Biochem 72: 1571-1579.
67. Zhao MW, Liang WQ, Zhang DB, Wang N, Wang CG, et al. (2007) Cloning and characterization of squalene synthase (SQS) gene from Ganoderma lucidum. J Microbiol Biotechnol 17: 1106-1112.
68. Shang CH, Shi L, Ren A, Qin L, Zhao MW, (2010) Molecular cloning, characterization, and differential expression of a lanosterol synthase gene from Ganoderma lucidum. Biosci Biotechnol Biochem 74: 974-978.
69. Tang YJ, Zhong JJ, (2003) Role of oxygen supply in submerged fermentation of Ganoderma lucidum for production of Ganoderma polysaccharide and ganoderic acid. Enzyme and Microbial Technology 32: 478-484.
70. Zhang W, Tang YJ, (2008) A novel three-stage light irradiation strategy in the submerged fermentation of medicinal mushroom Ganoderma lucidum for the efficient production of ganoderic acid and Ganoderma polysaccharides. Biotechnol Prog 24: 1249-1261.
71. Tang YJ, Zhang W, Zhong JJ, (2009) Performance analyses of a pH-shift and DOT-shift integrated fed-batch fermentation process for the production of ganoderic acid and Ganoderma polysaccharides by medicinal mushroom Ganoderma lucidum. Bioresour Technol 100: 1852-1859.
72. Tang YJ, Zhu LW, (2010) Improvement of ganoderic acid and Ganoderma polysaccharide biosynthesis by Ganoderma lucidum fermentation under the inducement of Cu2+. Biotechnol Prog 26: 417-423.
73. 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.
74. Sakamoto Y, Irie T, Sato T, (2005) Isolation and characterization of a fruiting body-specific exo-beta-1,3-glucanase-encoding gene, exg1, from Lentinula edodes. Curr Genet 47: 244-252.
75. Leonowicz A, Matuszewska A, Luterek J, Ziegenhagen D, Wojtas-Wasilewska M, et al. (1999) Biodegradation of lignin by white rot fungi. Fungal Genet Biol 27: 175-185.
76. Garcia S, Latge JP, Prevost MC, Leisola M, (1987) Wood degradation by white rot fungi: cytochemical studies using lignin peroxidase-immunoglobulin-gold complexes. Appl Environ Microbiol 53: 2384-2387.
77. Joo SS, Ryu IW, Park JK, Yoo YM, Lee DH, et al. (2008) Molecular cloning and expression of a laccase from Ganoderma lucidum, and its antioxidative properties. Mol Cells 25: 112-118.
78. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233-238.
79. Park BH, Karpinets TV, Syed MH, Leuze MR, Uberbacher EC, (2010) CAZymes Analysis Toolkit (CAT): web service for searching and analyzing carbohydrate-active enzymes in a newly sequenced organism using CAZy database. Glycobiology 20: 1574-1584.
80. Li R, Zhu H, Ruan J, Qian W, Fang X, et al. (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20: 265-272.
81. Audic S, Claverie JM, (1997) The significance of digital gene expression profiles. Genome Res 7: 986-995.
82. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I, (2001) Controlling the false discovery rate in behavior genetics research. Behav Brain Res 125: 279-284.
83. Fei X, Zhao MW, Li YX, (2006) Cloning and sequence analysis of a glyceraldehyde-3-phosphate dehydrogenase gene from Ganoderma lucidum. J Microbiol 44: 515-522.