Mycobiology

The Korean Society of Mycology (한국균학회)
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Three New Non-reducing Polyketide Synthase Genes from the Lichen-Forming Fungus Usnea longissima

  • Wang, Yi (Laboratory of Forest Plant Cultivation and Utilization, Yunnan Academy of Forestry) ;
  • Wang, Juan (Laboratory of Forest Plant Cultivation and Utilization, Yunnan Academy of Forestry) ;
  • Cheong, Yong Hwa (Korean Lichen Research Institute, Sunchon National University) ;
  • Hur, Jae-Seoun (Korean Lichen Research Institute, Sunchon National University)
  • Received : 2013.09.06
  • Accepted : 2013.10.30
  • Published : 2014.03.31
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Abstract

Usnea longissima has a long history of use as a traditional medicine. Several bioactive compounds, primarily belonging to the polyketide family, have been isolated from U. longissima. However, the genes for the biosynthesis of these compounds are yet to be identified. In the present study, three different types of non-reducing polyketide synthases (UlPKS2, UlPKS4, and UlPKS6) were identified from a cultured lichen-forming fungus of U. longissima. Phylogenetic analysis of product template domains showed that UlPKS2 and UlPKS4 belong to group IV, which includes the non-reducing polyketide synthases with an methyltransferase (MeT) domain that are involved in methylorcinol-based compound synthesis; UlPKS6 was found to belong to group I, which includes the non-reducing polyketide synthases that synthesize single aromatic ring polyketides, such as orsellinic acid. Reverse transcriptase-PCR analysis demonstrated that UlPKS2 and UlPKS4 were upregulated by sucrose; UlPKS6 was downregulated by asparagine, glycine, and alanine.

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References

  1. Honegger R. Cytological aspects of the mycobiont-phycobiont relationship in lichens. Lichenologist 1984;16:111-27. https://doi.org/10.1017/S0024282984000293
  2. Boustie J, Grube M. Lichens: a promising source of bioactive secondary metabolites. Plant Genet Resour 2005;3:273-87. https://doi.org/10.1079/PGR200572
  3. Boustie J, Tomasi S, Grube M. Bioactive lichen metabolites: alpine habitats as an untapped source. Phytochem Rev 2011; 10:287-307. https://doi.org/10.1007/s11101-010-9201-1
  4. Stocker-Wörgötter E. Metabolic diversity of lichen-forming ascomycetous fungi: culturing polyketide and shikimate metabolite production, and PKS genes. Nat Prod Rep 2008; 25:188-200. https://doi.org/10.1039/b606983p
  5. Shrestha G, Clair LL. Lichens: a promising source of antibiotic and anticancer drugs. Phytochem Rev 2013;12:229-44. https://doi.org/10.1007/s11101-013-9283-7
  6. Huneck S. The significance of lichens and their metabolites. Naturwissenschaften 1999;86:559-70. https://doi.org/10.1007/s001140050676
  7. Shukla V, Joshi GP, Rawat MS. Lichens as a potential natural source of bioactive compounds: a review. Phytochem Rev 2010;9:303-14. https://doi.org/10.1007/s11101-010-9189-6
  8. Stojanovic G, Stojanovic I, Smelcerovic A. Lichen depsidones as potential novel pharmacologically active compounds. Mini Rev Org Chem 2012;9:178-84. https://doi.org/10.2174/157019312800604689
  9. Zambare VP, Christopher LP. Biopharmaceutical potential of lichens. Pharm Biol 2012;50:778-98. https://doi.org/10.3109/13880209.2011.633089
  10. Cox RJ. Polyketides, proteins and genes in fungi: programmed nano-machines begin to reveal their secrets. Org Biomol Chem 2007;5:2010-26. https://doi.org/10.1039/b704420h
  11. Kroken S, Glass NL, Taylor JW, Yoder OC, Turgeon BG. Phylogenomic analysis of type I polyketide synthase genes in pathogenic and saprobic ascomycetes. Proc Natl Acad Sci U S A 2003;100:15670-5. https://doi.org/10.1073/pnas.2532165100
  12. Li Y, Xu W, Tang Y. Classification, prediction, and verification of the regioselectivity of fungal polyketide synthase product template domains. J Biol Chem 2010;285:22764-73. https://doi.org/10.1074/jbc.M110.128504
  13. Elix JA, Stocker-Worgotter E. Biochemistry and secondary metabolites. In: Nash TH 3rd, editor. Lichen biology. 2nd ed. Cambridge: Cambridge University Press; 2008. p. 104-33.
  14. Armaleo D, Sun X, Culberson C. Insights from the first putative biosynthetic gene cluster for a lichen depside and depsidone. Mycologia 2011;103:741-54. https://doi.org/10.3852/10-335
  15. Chooi YH, Stalker DM, Davis MA, Fujii I, Elix JA, Louwhoff SH, Lawrie AC. Cloning and sequence characterization of a non-reducing polyketide synthase gene from the lichen Xanthoparmelia semiviridis. Mycol Res 2008;112(Pt 2):147-61. https://doi.org/10.1016/j.mycres.2007.08.022
  16. Brunauer G, Muggia L, Stocker-Wörgötter E, Grube M. A transcribed polyketide synthase gene from Xanthoria elegans. Mycol Res 2009;113(Pt 1):82-92. https://doi.org/10.1016/j.mycres.2008.08.007
  17. Gagunashvili AN, Davídsson SP, Jónsson ZO, Andrésson OS. Cloning and heterologous transcription of a polyketide synthase gene from the lichen Solorina crocea. Mycol Res 2009;113(Pt 3):354-63. https://doi.org/10.1016/j.mycres.2008.11.011
  18. Valarmathi R, Hariharan GN, Venkataraman G, Parida A. Characterization of a non-reducing polyketide synthase gene from lichen Dirinaria applanata. Phytochemistry 2009;70: 721-9. https://doi.org/10.1016/j.phytochem.2009.04.007
  19. Yu NY, Kim JA, Jeong MH, Cheong YH, Jung JS, Hur JS. Characterization of two novel non-reducing polyketide synthase genes from the lichen-forming fungus Hypogymnia physodes. Mycol Prog 2013;12:519-24. https://doi.org/10.1007/s11557-012-0858-2
  20. Wang Y, Kim JA, Cheong YH, Joshi Y, Koh YJ, Hur JS. Isolation and characterization of a reducing polyketide synthase gene from the lichen-forming fungus Usnea longissima. J Microbiol 2011;49:473-80. https://doi.org/10.1007/s12275-011-0362-4
  21. Wang Y, Kim JA, Cheong YH, Koh YJ, Hur JS. Isolation and characterization of a non-reducing polyketide synthase gene from the lichen-forming fungus Usnea longissima. Mycol Prog 2012;11:75-83. https://doi.org/10.1007/s11557-010-0730-1
  22. Van den Berg MA, Albang R, Albermann K, Badger JH, Daran JM, Driessen AJ, Garcia-Estrada C, Fedorova ND, Harris DM, Heijne WH, et al. Genome sequencing and analysis of the filamentous fungus Penicillium chrysogenum. Nat Biotechnol 2008;26:1161-8. https://doi.org/10.1038/nbt.1498
  23. Lans C, Turner N, Khan T, Brauer G, Boepple W. Ethnoveterinary medicines used for ruminants in British Columbia, Canada. J Ethnobiol Ethnomed 2007;3:11. https://doi.org/10.1186/1746-4269-3-11
  24. Nishitoba Y, Nishimura I, Nishiyama T, Mizutani J. Lichen acids, plant growth inhibitors from Usnea longissima. Phytochemistry 1987;26:3181-5. https://doi.org/10.1016/S0031-9422(00)82466-8
  25. Feng J, Yang X. New dibenzofuran and anthraquinone from Usnea longissima. Zhongguo Zhong Yao Za Zhi 2009;34:852-3.
  26. Honegger R. Simon Schwendener (1829-1919) and the dual hypothesis of lichens. Bryologist 2000;103:307-13. https://doi.org/10.1639/0007-2745(2000)103[0307:SSATDH]2.0.CO;2
  27. Li WC, Zhou J, Guo SY, Guo LD. Endophytic fungi associated with lichens in Baihua Mountain of Beijing, China. Fungal Divers 2007;25:69-80.
  28. Yamamoto Y, Mizuguchi R, Yamada Y. Tissue cultures of Usnea rubescens and Ramalina yasudae and production of usnic acid in their cultures. Agric Biol Chem 1985;49:3347-8. https://doi.org/10.1271/bbb1961.49.3347
  29. Regueira TB, Kildegaard KR, Hansen BG, Mortensen UH, Hertweck C, Nielsen J. Molecular basis for mycophenolic acid biosynthesis in Penicillium brevicompactum. Appl Environ Microbiol 2011;77:3035-43. https://doi.org/10.1128/AEM.03015-10
  30. Bailey AM, Cox RJ, Harley K, Lazarus CM, Simpson TJ, Skellam E. Characterisation of 3-methylorcinaldehyde synthase (MOS) in Acremonium strictum: first observation of a reductive release mechanism during polyketide biosynthesis. Chem Commun (Camb) 2007;(39):4053-5.
  31. Schroeckh V, Scherlach K, Nützmann HW, Shelest E, Schmidt-Heck W, Schuemann J, Martin K, Hertweck C, Brakhage AA. Intimate bacterial-fungal interaction triggers biosynthesis of archetypal polyketides in Aspergillus nidulans. Proc Natl Acad Sci U S A 2009;106:14558-63. https://doi.org/10.1073/pnas.0901870106
  32. Zhou H, Qiao K, Gao Z, Meehan MJ, Li JW, Zhao X, Dorrestein PC, Vederas JC, Tang Y. Enzymatic synthesis of resorcylic acid lactones by cooperation of fungal iterative polyketide synthases involved in hypothemycin biosynthesis. J Am Chem Soc 2010;132:4530-1. https://doi.org/10.1021/ja100060k
  33. Wang S, Xu Y, Maine EA, Wijeratne EM, Espinosa-Artiles P, Gunatilaka AA, Molnár I. Functional characterization of the biosynthesis of radicicol, an Hsp90 inhibitor resorcylic acid lactone from Chaetomium chiversii. Chem Biol 2008;15:1328-38. https://doi.org/10.1016/j.chembiol.2008.10.006
  34. Hamada N. Effects of osmotic culture conditions on isolated lichen mycobionts. Bryologist 1993;96:569-72. https://doi.org/10.2307/3243987
  35. Kinoshita Y, Yamamoto Y, Kurokawa T, Yoshimura I. Influences of nitrogen sources on usnic acid production in a cultured mycobiont of the lichen Usnea hirta (L.) Wigg. Biosci Biotechnol Biochem 2001;65:1900-2. https://doi.org/10.1271/bbb.65.1900