Differential Gene Expression Network in Terpenoid Synthesis of Antrodia cinnamomea in Mycelia and Fruiting Bodies

Journal of Agricultural and Food Chemistry

Volumn 65, Issue 9, 2017, Pages 1874-1886

  Lin, Yan Liang ^a   Ma, Li Ting ^a   Lee, Yi Ru ^a   Shaw, Jei Fu ^b   Wang, Sheng Yang ^c,d   Chu, Fang Hua ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b I SHOU UNIVERSITY   (Taiwan)

^c NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^d AGRICULTURAL BIOTECHNOLOGY RESEARCH CENTER   (Taiwan)

Author keywords

Antrodia cinnamomea; genetic network; next generation sequencing; terpenoid synthase; transcriptome

Indexed keywords

GENE EXPRESSION; POLYMERASE CHAIN REACTION; SCAFFOLDS; TERPENES;

ANTRODIA CINNAMOMEA; GENETIC NETWORKS; NEXT-GENERATION SEQUENCING; SYNTHASES; TRANSCRIPTOMES;

LIPIDS;

FUNGAL PROTEIN; TERPENE; TRANSCRIPTOME;

ANTRODIA; FRUITING BODY; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MYCELIUM;

ANTRODIA; FRUITING BODIES, FUNGAL; FUNGAL PROTEINS; GENE REGULATORY NETWORKS; MYCELIUM; TERPENES; TRANSCRIPTOME;

EID: 85014715274     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.6b05386     Document Type: Article

References (53)

1. Chang, T. T.; Chou, W. N. Antrodia cinnamomea reconsidered and A. salmonea sp. nov. on Cunninghamia konishii in Taiwan Bot. Bull. Acad. Sin. 2004, 45 ( 4 ) 347-352
2. Wu, S. H.; Ryvarden, L.; Chang, T. T. Antrodia camphorata (“niu-chang-chih”), new combination of a medicinal fungus in Taiwan Bot. Bull. Acad. Sin. 1997, 38 ( 4 ) 273-275
3. Chen, C. H.; Yang, S. W.; Shen, Y. C. New steroid acids from Antrodia cinnamomea, a fungal parasite of Cinnamomum micranthum J. Nat. Prod. 1995, 58 ( 11 ) 1655-1661 10.1021/np50125a002
4. Hsu, Y. L.; Kuo, Y. C.; Kuo, P. L.; Ng, L. T.; Kuo, Y. H.; Lin, C. C. Apoptotic effects of extract from Antrodia camphorata fruiting bodies in human hepatocellular carcinoma cell lines Cancer Lett. 2005, 221 ( 1 ) 77-89 10.1016/j.canlet.2004.08.012
5. Shen, Y. C.; Chou, C. J.; Wang, Y. H.; Chen, C. F.; Chou, Y. C.; Lu, M. K. Anti-inflammatory activity of the extracts from mycelia of Antrodia camphorata cultured with water-soluble fractions from five different Cinnamomum species FEMS Microbiol. Lett. 2004, 231 ( 1 ) 137-143 10.1016/S0378-1097(03)00953-4
6. Liu, D. Z.; Liang, H. J.; Chen, C. H.; Su, C. H.; Lee, T. H.; Huang, C. T.; Hou, W. C.; Lin, S. Y.; Zhong, W. B.; Lin, P. J.; Hung, L. F.; Liang, Y. C. Comparative anti-inflammatory characterization of wild fruiting body, liquid-state fermentation, and solid-state culture of Taiwanofungus camphoratus in microglia and the mechanism of its action J. Ethnopharmacol. 2007, 113 ( 1 ) 45-53 10.1016/j.jep.2007.03.037
7. Song, T. Y.; Yen, G. C. Antioxidant properties of Antrodia camphorata in submerged culture J. Agric. Food Chem. 2002, 50 ( 11 ) 3322-3327 10.1021/jf011671z
8. Hsiao, G.; Shen, M. Y.; Lin, K. H.; Lan, M. H.; Wu, L. Y.; Chou, D. S.; Lin, C. H.; Su, C. H.; Sheu, J. R. Antioxidative and hepatoprotective effects of Antrodia camphorata extract J. Agric. Food Chem. 2003, 51 ( 11 ) 3302-3308 10.1021/jf021159t
9. Nakamura, N.; Hirakawa, A.; Gao, J. J.; Kakuda, H.; Shiro, M.; Komatsu, Y.; Sheu, C.; Hattori, M. Five new maleic and succinic acid derivatives from the mycelium of Antrodia camphorata and their cytotoxic effects on LLC tumor cell line J. Nat. Prod. 2004, 67 ( 1 ) 46-48 10.1021/np030293k
10. Lee, I. H.; Huang, R. L.; Chen, C. T.; Chen, H. C.; Hsu, W. C.; Lu, M. K. Antrodia camphorata polysaccharides exhibit anti-hepatitis B virus effects FEMS Microbiol. Lett. 2002, 209 ( 1 ) 63-67 10.1111/j.1574-6968.2002.tb11110.x
11. Ao, Z. H.; Xu, Z. H.; Lu, Z. M.; Xu, H. Y.; Zhang, X. M.; Dou, W. F. Niuchangchih (Antrodia camphorata) and its potential in treating liver diseases J. Ethnopharmacol. 2009, 121 ( 2 ) 194-212 10.1016/j.jep.2008.10.039
12. 4-induced hepatic toxicity in rats J. Agric. Food Chem. 2003, 51 ( 6 ) 1571-1577 10.1021/jf0209701
13. 2+-NO-cGMP pathway Life Sci. 2003, 73 ( 21 ) 2769-2783 10.1016/S0024-3205(03)00669-6
14. Lin, Y. L.; Wen, T. N.; Chang, S. T.; Chu, F. H. Proteomic analysis of differently cultured endemic medicinal mushroom Antrodia cinnamomea T.T. Chang et W.N. Chou from Taiwan Int. J. Med. Mushrooms 2011, 13 ( 5 ) 473-481 10.1615/IntJMedMushr.v13.i5.70
15. Shen, Y. C.; Wang, Y. H.; Chou, Y. C.; Chen, C. F.; Lin, L. C.; Chang, T. T.; Tien, J. H.; Chou, C. J. Evaluation of the anti-inflammatory activity of zhankuic acids isolated from the fruiting bodies of Antrodia camphorata Planta Med. 2004, 70 ( 4 ) 310-314 10.1055/s-2004-818941
16. Lu, M. C.; El-Shazly, M.; Wu, T. Y.; Du, Y. C.; Chang, T. T.; Chen, C. F.; Hsu, Y. M.; Lai, K. H.; Chiu, C. P.; Chang, F. R.; Wu, Y. C. Recent research and development of Antrodia cinnamomea Pharmacol. Ther. 2013, 139 ( 2 ) 124-156 10.1016/j.pharmthera.2013.04.001
17. Erkel, G.; Anke, T. Products from Basidiomycetes. In Biotechnology; Wiley-VCH Verlag GmbH: 1997; pp 489-533.
18. Schüffler, A.; Anke, T. Secondary metabolites of Basidiomycetes. In physiology and genetics, 1st ed.; The Mycota; Springer Berlin Heidelberg: 2009; Vol. 15, pp 209-231.
19. Buckingham, J. Dictionary of natural products on DVD; Chapman and Hall/CRC: 1993.
20. Wawrzyn, G. T.; Quin, M. B.; Choudhary, S.; López-Gallego, F.; Schmidt-Dannert, C. Draft genome of Omphalotus olearius provides a predictive framework for sesquiterpenoid natural product biosynthesis in Basidiomycota Chem. Biol. 2012, 19 ( 6 ) 772-783 10.1016/j.chembiol.2012.05.012
21. Gonzalez Del Val, A.; Platas, G.; Arenal, F.; Orihuela, J. C.; Garcia, M.; Hernandez, P.; Royo, I.; De Pedro, N.; Silver, L. L.; Young, K.; Vicente, M. F.; Pelaez, F. Novel illudins from Coprinopsis episcopalis (syn. Coprinus episcopalis), and the distribution of illudin-like compounds among filamentous fungi Mycol. Res. 2003, 107 ( 10 ) 1201-1209 10.1017/S0953756203008487
22. Bräse, S.; Encinas, A.; Keck, J.; Nising, C. F. Chemistry and biology of mycotoxins and related fungal metabolites Chem. Rev. 2009, 109 ( 9 ) 3903-3990 10.1021/cr050001f
23. Chen, C. Y.; Chien, S. C.; Tsao, N. W.; Lai, C. S.; Wang, Y. Y.; Hsiao, W. W.; Chu, F. H.; Kuo, Y. H.; Wang, S. Y. Metabolite profiling and comparison of bioactivity in Antrodia cinnamomea and Antrodia salmonea fruiting bodies Planta Med. 2016, 82 ( 3 ) 244-249 10.1055/s-0035-1558141
24. Lin, Y. L.; Lee, Y. R.; Tsao, N. W.; Wang, S. Y.; Shaw, J. F.; Chu, F. H. Characterization of the 2,3-oxidosqualene cyclase gene from Antrodia cinnamomea and enhancement of cytotoxic triterpenoid compound production J. Nat. Prod. 2015, 78, 1556-1562 10.1021/acs.jnatprod.5b00020
25. de Santana, M. F.; Guimarães, A. G.; Chaves, D. O.; Silva, J. C.; Bonjardim, L. R.; Lucca Júnior, W. d.; Ferro, J. N. d. S.; Barreto, E. d. O.; Santos, F. E. D.; Soares, M. B. P.; Villarreal, C. F.; Quintans, J. d. S. S.; Quintans-Júnior, L. J. The anti-hyperalgesic and anti-inflammatory profiles of p-cymene: Evidence for the involvement of opioid system and cytokines Pharm. Biol. 2015, 53 ( 11 ) 1583-1590 10.3109/13880209.2014.993040
26. 6-p-cymene) complexes of nonsteroidal anti-inflammatory drug derivatives Organometallics 2014, 33 ( 19 ) 5546-5553 10.1021/om500825h
27. Ninomiya, K.; Hayama, K.; Ishijima, S. A.; Maruyama, N.; Irie, H.; Kurihara, J.; Abe, S. Suppression of inflammatory reactions by terpinen-4-ol, a main constituent of tea tree oil, in a murine model of oral candidiasis and its suppressive activity to cytokine production of macrophages in vitro Biol. Pharm. Bull. 2013, 36 ( 5 ) 838-844 10.1248/bpb.b13-00033
28. Mondello, F.; De Bernardis, F.; Girolamo, A.; Cassone, A.; Salvatore, G. In vivo activity of terpinen-4-ol, the main bioactive component of Melaleuca alternifolia Cheel (tea tree) oil against azole-susceptible and-resistant human pathogenic Candida species BMC Infect. Dis. 2006, 6, 158 10.1186/1471-2334-6-158
29. Rangasamy, K.; Namasivayam, E. In vitro antioxidant and free radical scavenging activity of isolongifolene Asian J. Biol. Sci. 2014, 7 ( 1 ) 13-23 10.3923/ajbs.2014.13.23
30. MacLean, D.; Jones, J. D. G.; Studholme, D. J. Application of “next-generation” sequencing technologies to microbial genetics Nat. Rev. Microbiol. 2009, 7 ( 4 ) 287-296
31. Lin, Y. L.; Ma, L. T.; Lee, Y. R.; Lin, S. S.; Wang, S. Y.; Chang, T. T.; Shaw, J. F.; Li, W. H.; Chu, F. H. MicroRNA-like small RNAs pediction in the development of Antrodia cinnamomea PLoS One 2015, 10, e0123245 10.1371/journal.pone.0123245
32. Tamura, K.; Peterson, D.; Peterson, N.; Stecher, G.; Nei, M.; Kumar, S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods Mol. Biol. Evol. 2011, 28 ( 10 ) 2731-2739 10.1093/molbev/msr121
33. Lin, Y. L.; Lee, Y. R.; Huang, W. K.; Chang, S. T.; Chu, F. H. Characterization of S-(+)-linalool synthase from several provenances of Cinnamomum osmophloeum Tree Genet. Genomes 2014, 10 ( 1 ) 75-86 10.1007/s11295-013-0665-1
34. Wen, C. H.; Lin, S. S.; Chu, F. H. Transcriptome analysis of a subtropical deciduous tree: Autumn leaf senescence gene expression profile of Formosan gum Plant Cell Physiol. 2015, 56 ( 1 ) 163-174 10.1093/pcp/pcu160
35. Liu, L. Y. D.; Tseng, H. I.; Lin, C. P.; Lin, Y. Y.; Huang, Y. H.; Huang, C. K.; Chang, T. H.; Lin, S. S. High-throughput transcriptome analysis of the leafy flower transition of Catharanthus roseus induced by peanut witches’-broom phytoplasma Infection Plant Cell Physiol. 2014, 55 ( 5 ) 942-957 10.1093/pcp/pcu029
36. Bastian, M.; Heymann, S. Gephi: An open source software for exploring and manipulating networks Int. AAAI Conf. Weblogs Soc. Media 2009, 361-362
37. Starks, C. M.; Back, K.; Chappell, J.; Noel, J. P. Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase Science 1997, 277 ( 5333 ) 1815-1820 10.1126/science.277.5333.1815
38. Whittington, D. A.; Wise, M. L.; Urbansky, M.; Coates, R. M.; Croteau, R. B.; Christianson, D. W. Bornyl diphosphate synthase: structure and strategy for carbocation manipulation by a terpenoid cyclase Proc. Natl. Acad. Sci. U. S. A. 2002, 99 ( 24 ) 15375-15380 10.1073/pnas.232591099
39. Kwon, M.; Cochrane, S. A.; Vederas, J. C.; Ro, D. K. Molecular cloning and characterization of drimenol synthase from valerian plant (Valeriana officinalis) FEBS Lett. 2014, 588 ( 24 ) 4597-4603 10.1016/j.febslet.2014.10.031
40. Adams, R. P. Identification of essential oil components by gas chromatography/mass spectrometry, 4th ed.; Allured Publising Corporation: Carol Sream, IL, 2007.
41. Scott, J. Social network analysis; SAGE: 2012.
42. Yahyaa, M.; Matsuba, Y.; Brandt, W.; Doron-Faigenboim, A.; Bar, E.; McClain, A.; Davidovich-Rikanati, R.; Lewinsohn, E.; Pichersky, E.; Ibdah, M. Identification, functional characterization, and evolution of terpene synthases from a basal dicot Plant Physiol. 2015, 169 ( November ) 1683-1697 10.1104/pp.15.00930
43. López-Gallego, F.; Wawrzyn, G. T.; Schmidt-Dannert, C. Selectivity of fungal sesquiterpene synthases: role of the active site’s H-1 alpha loop in catalysis Appl. Environ. Microbiol. 2010, 76 ( 23 ) 7723-7733 10.1128/AEM.01811-10
44. Chooi, Y. H.; Hong, Y. J.; Cacho, R. A.; Tantillo, D. J.; Tang, Y. A cytochrome p450 serves as an unexpected terpene cyclase during fungal meroterpenoid biosynthesis J. Am. Chem. Soc. 2013, 135 ( 45 ) 16805-16808 10.1021/ja408966t
45. Itoh, T.; Tokunaga, K.; Matsuda, Y.; Fujii, I.; Abe, I.; Ebizuka, Y.; Kushiro, T. Reconstitution of a fungal meroterpenoid biosynthesis reveals the involvement of a novel family of terpene cyclases Nat. Chem. 2010, 2 ( 10 ) 858-864 10.1038/nchem.764
46. Bromann, K.; Toivari, M.; Viljanen, K.; Vuoristo, A.; Ruohonen, L.; Nakari-Setälä, T. Identification and characterization of a novel diterpene gene cluster in Aspergillus nidulans PLoS One 2012, 7 ( 4 ) e35450 10.1371/journal.pone.0035450
47. Ram, M.; Khan, M. A.; Jha, P.; Khan, S.; Kiran, U.; Ahmad, M. M.; Javed, S.; Abdin, M. Z. HMG-CoA reductase limits artemisinin biosynthesis and accumulation in Artemisia annua L. plants Acta Physiol. Plant. 2010, 32, 859-866 10.1007/s11738-010-0470-5
48. Caracuel, Z.; Roncero, M. I. G.; Espeso, E. A.; González-Verdejo, C. I.; García-Maceira, F. I.; Di Pietro, A. The pH signalling transcription factor PacC controls virulence in the plant pathogen Fusarium oxysporum Mol. Microbiol. 2003, 48, 765-779 10.1046/j.1365-2958.2003.03465.x
49. Brakhage, A. A. Regulation of fungal secondary metabolism Nat. Rev. Microbiol. 2013, 11 ( 1 ) 21-32 10.1038/nrmicro2916
50. Bok, J. W.; Wiemann, P.; Garvey, G. S.; Lim, F. Y.; Haas, B.; Wortman, J.; Keller, N. P. Illumina identification of RsrA, a conserved C2H2 transcription factor coordinating the NapA mediated oxidative stress signaling pathway in Aspergillus BMC Genomics 2014, 15 ( 1 ) 1011 10.1186/1471-2164-15-1011
51. 2 transcription factor MtfA is a novel regulator of secondary metabolism and morphogenesis in Aspergillus nidulans PLoS One 2013, 8 ( 9 ) e74122 10.1371/journal.pone.0074122
52. Kurahashi, A.; Shimoda, T.; Sato, M.; Fujimori, F.; Hirama, J.; Nishibori, K. A putative transcription factor Gf.BMR1 in Grifola frondosa, the homolog of BMR1 in Bipolaris oryzae, was strongly induced by near-ultraviolet light and blue light Mycoscience 2015, 56 ( 2 ) 177-182 10.1016/j.myc.2014.05.005
53. Kihara, J.; Moriwaki, A.; Tanaka, N.; Tanaka, C.; Ueno, M.; Arase, S. Characterization of the BMR1 gene encoding a transcription factor for melanin biosynthesis genes in the phytopathogenic fungus Bipolaris oryzae FEMS Microbiol. Lett. 2008, 281, 221-227 10.1111/j.1574-6968.2008.01101.x