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Oxygenated lanostane-type triterpenes profiling in laccate Ganoderma chemotaxonomy

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Abstract

Oxygenated lanostane-type triterpenes (OLTT), including ganoderic acids and lucidenic acids produced by fungi of the genus Ganoderma (Polyporales), are abundantly documented for their potential pharmacological value. In order to test the correlation between species identity and OLTT composition, methanolic extracts of seven laccate Ganoderma species were analyzed by liquid chromatography coupled to mass spectrometry. OLTT profiles of each species were compared to a phylogenetic reconstruction of Ganoderma based on ITS rDNA sequences. The results suggest a high specificity in OLTT composition in one of the phylogenetic lineages of Ganoderma that encompasses tropical species, when no OLTT compound was detected in other lineages (including the European G. lucidum and the Asian G. sinense). Within the OLTT-positive lineage, G. sichuanense, G. martinicense, and G. tuberculosum (Asian-tropicum clade) were characterized by a specific composition in ganoderic acids and G. curtisii by a variety of lucidenic acids. An unidentified OLTT was found in G. resinaceum, also equivocally positioned in phylogenetic analyses. These results confirm OLTT as a suitable taxonomic marker in a lineage of pharmacologically and economically valuable species. Correlations with phylogeny, and development of OLTT composition as a fingerprint tool for quality control, could be an issue to address next, based on a more complete species sampling.

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Abbreviations

GA:

ganoderic acid

HPLC:

high performance liquid chromatography

HRMS:

high resolution mass spectrometry

LC–ESI–MS:

liquid chromatography–electrospray–ionization–mass spectrometry

LC–ESI–MS/MS:

liquid chromatography–electrospray ionization–mass tandem spectrometry

PCR:

polymerase chain reaction

RDB:

ring double bond

TIC:

total ion current

References

  • Arisawa M, Fujita A, Saga M, Fukumura H, Hayashi T, Shimizu M, Morita N (1986) Three new lanostanoids from Ganoderma lucidum. J Nat Prod 49:621–625

    Article  CAS  PubMed  Google Scholar 

  • Binder M, Bresinsky A (2002) Retiboletus, a new genus for a species–complex in the Boletaceae producing retipolides. Feddes Report 113:30–40

    Article  Google Scholar 

  • Bouxin G (2005) Ginkgo, a multivariate analysis package. J Veg Sci 16:353–359

    Article  Google Scholar 

  • Cao Y, Dai YC, Wu SH (2012) Species clarification for the world-famous medicinal Ganoderma fungus ‘Lingzhi’ distributed in East Asia. Fungal Divers 56:49–62

    Article  Google Scholar 

  • Chen Y, Yan Y, Xie MY, Nie SP, Liu W, Gong XF, Wang YX (2008) Development of a chromatographic fingerprint for the chloroform extracts of Ganoderma lucidum by HPLC and LC–MS. J Pharm Biomed Anal 47:469–477

    Article  CAS  PubMed  Google Scholar 

  • Cheng CR, Yang M, Wu ZY, Wang Y, Zeng F, Wu WY, Guan SH, Guo DA (2011) Fragmentation pathways of oxygenated tetracyclic triterpenoids and their application in the qualitative analysis of Ganoderma lucidum by multistage tandem mass spectrometry. Rapid Commun Mass Spectrom 25:1323–1335

    Article  CAS  PubMed  Google Scholar 

  • Chinese Pharmacopoeia Commission (2000) Pharmacopoeia of the people’s republic of China. Chemical Industry Press, Beijing

    Google Scholar 

  • Da J, Wu WY, Hou JJ, Long HL, Yao S, Yang Z, Cai LY, Yang M, Jiang BH, Liu XL, Cheng CR, Li YF, Guo DA (2012) Comparison of two officinal Chinese pharmacopoeia species of Ganoderma based on chemical research with multiple technologies and chemometrics analysis. J Chromatogr 1222:59–70

    Article  CAS  Google Scholar 

  • Dai YC, Yang ZL, Cui BK, Yu CJ, Zhou LW (2009) Species diversity and utilization of medicinal mushrooms and fungi in China (Review). Int J Med Mushr 11:287–302

    Article  Google Scholar 

  • Dai YC, Bau T, Cui BK, Qin GF (2012) Illustrations of medicinal fungi in China. Northeast Forestry University Press, Harbin

    Google Scholar 

  • Davoli P, Weber RWS (2002) Simple method for reversed-phase high-performance liquid chromatographic analysis of fungal pigments in fruit bodies of Boletales (Fungi). J Chromatogr A 964:f29–135

    Article  Google Scholar 

  • Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85:407–415

    Article  Google Scholar 

  • Du XH, Zhao Q, Yang ZL, Hansen K, Taskin H, Büyükalaca S, Dewsbury D, Moncalvo JM, Douhan GW, Robert VA, Crous PW, Rehner SA, Rooney AP, Sink S, O’Donnell K (2012) How well do ITS rDNA sequences differentiate species of true morels (Morchella)? Mycologia 104:1351–1368

    Article  PubMed  Google Scholar 

  • Frisvad JC, Andersen B, Thrane U (2008) The use of secondary metabolite profiling in chemotaxonomy of filamentous fungi. Mycol Res 112:231–240

    Article  CAS  PubMed  Google Scholar 

  • Frøslev TG, Matheny PB, Hibbett DS (2005) Lower level relationships in the mushroom genus Cortinarius (Basidiomycota, Agaricales): a comparison of RPB1, RPB2, and ITS phylogenies. Mol Phylogenet Evol 37:602–618

    Article  PubMed  Google Scholar 

  • Fu CM, Lu GH, Schmitz OJ, Li ZW, Leung KSY (2008) Improved chromatographic fingerprints for facile differentiation of two Ganoderma spp. Biomed Chromatogr 23:280–288

    Article  Google Scholar 

  • Gao JM (2006) New biologically active metabolites from Chinese higher fungi. Curr Org Chem 10:849–871

    Article  CAS  Google Scholar 

  • Gao JJ, Min BS, Ahn EM, Norio N, Lee HK, Hattori M (2002) New triterpene aldehydes, lucialdehydes A–C, from Ganoderma lucidum and their cytoxicity against murine and human tumors cell. Chem Pharm Bull 5:837–840

    Article  Google Scholar 

  • Gao J, Sato N, Hattori M, Ma CM (2013) The simultaneous quantification of Ganoderma acids and alcohols using ultra high-performance liquid chromatography–mass spectrometry in dynamic selected reaction monitoring mode. J Pharm Biomed Anal 74:246–249

    Article  CAS  PubMed  Google Scholar 

  • Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes–application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    Article  CAS  PubMed  Google Scholar 

  • Gill M, Steglich W (1987) Pigments of fungi (Macromycetes). In: Herz W, Grisebach H, Kirby GW, Tamm C (eds) Progress in the chemistry of organic natural products, vol 51. Springer Verlag, Berlin, pp 1–317

    Google Scholar 

  • Higgins D, Thompson J, Gibson T, Thompson JD, Higgins G, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed Central  PubMed  Google Scholar 

  • Hirotani M, Furuya T, Shiro M (1984) A ganoderic acid derivative, a highly oxygenated lanostane-type triterpenoid from Ganoderma lucidum. Phytochemistry 24:2055–2061

    Article  Google Scholar 

  • Kang D, Kim J, Choi JN, Liu K–H, Lee CH (2011) Chemotaxonomy of Trichoderma spp. Using mass spectrometry-based metabolite profiling. J Microbiol Biotechnol 21:5–13

    Article  CAS  PubMed  Google Scholar 

  • Kikuchi T, Matsuda S, Kadota S, Murai Y, Ogita Z (1985) Ganoderic acid D, E, F, and H and lucidenic acid D, E, and F, new triterpenoids from Ganoderma lucidum. Chem Pharm Bull 33:2624–2627

    Article  CAS  Google Scholar 

  • Lee S, Park S, Oh JJ, Yang C (1998) Natural inhibitors for protein prenyltransferase. Plant Med 64:303–308

    Article  CAS  Google Scholar 

  • Liu J, Shimizu K, Konishi F, Kumamoto S, Kondo R (2007) The antiandrogen effect of Ganoderol B isolated from the fruiting body of Ganoderma lucidum. Bioorg Med Chem 15:4966–4972

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Liu Y, Qiu F, Di X (2011) Sensitive and selective chromatography–tandem mass spectrometry method for the determination of five ganoderic acids in Ganoderma lucidum and its related species. J Pharm Biomed Anal 54:717–721

    Article  CAS  PubMed  Google Scholar 

  • Lomascolo A, Cayol JL, Roche M, Guo L, Robert JL, Record E, Lesage–Meessen L, Ollivier B, Sigoillot JC, Asther M (2002) Molecular clustering of Pycnoporus strains from various geographic origins and isolation of monokaryotic strains for laccase hyperproduction. Mycol Res 106:1193–1203

    Article  CAS  Google Scholar 

  • Milne I, Wright F, Rowe G, Marshal DF, Husmeier D, McGuire G (2004) TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments. Bioinformatics 20:1806–1807

    Article  CAS  PubMed  Google Scholar 

  • Min BS, Gao JJ, Nakamura N, Hattori M (2000) Triterpenes from the spores of Ganoderma lucidum and their cytotoxicity against Meth–A and LLC tumor cells. Chem Pharm Bull 48:1026–1033

    Article  CAS  PubMed  Google Scholar 

  • Moncalvo JM (2000) Chapter 2) Systematics of Ganoderma. International Journal of Food, P.D. Bridge, M. Holderness (Eds.), Ganoderma diseases of perennial crops. CABI Publ 23–46

  • Moncalvo JM, Ryvarden L (1997) Nomenclatural study of the Ganodermataceae Donk. Synopsis Fungorum.1

  • Moncalvo JM, Wang HF, Hseu RSH (1995) Gene phylogeny of the Ganoderma lucidum complex based on ribosomal DNA sequences. Comparaison with traditional taxonomic characters. Mycol Res 99:1489–1499

    Article  Google Scholar 

  • Nishitoba T, Sato H, Shirasu S, Sakamura S (1986) Evidence on the strain-specific terpenoid pattern of Ganoderma lucidum. Agric Biol Chem 50:2151–2154

    Article  CAS  Google Scholar 

  • Paterson RRM (2006) Ganoderma—a therapeutic fungal biofactory. Phytochemistry 67:1985–2001

    Article  CAS  PubMed  Google Scholar 

  • Pegler DN, Yao YJ (1996) Oriental species of Ganoderma, section Ganoderma. In: Wasser SP (ed) Botany and mycology for the next Millenium: collection of scientific articles devoted to the 70th anniversary of academician sytnik KM. N. G. Kholodny institute of botany, National Academy of Sciences of Ukraine, Kyiv, pp 336–347

    Google Scholar 

  • Qi Y, Zhao L, Sun HH (2012) Development of a rapid and confirmatory method to identify ganoderic acids in Ganoderma mushrooms. Front Pharm 3:1–7

    Article  Google Scholar 

  • Richter C, Wittstein K, Kirk PM, Stadler M (2015) An assessment of the taxonomy and chemotaxonomy of Ganoderma. Fungal Divers 71:1–15

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) Mr Bayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Ryvarden L (2004) Neotropical polypores. Part. 1) Introduction, Ganodermataceae and Hymenochaetaceae. Syn Fung 19

  • Schoch CL, Seifert KA, Huhndorf S et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A 109:6241–6246. doi:10.1073/pnas.1117018109

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Stadler M, Læssøe T, Fournier J, Decock C, Schmieschek B, Tichy HV, Peršoh D (2014) A polyphasic taxonomy of Daldinia (Xylariaceae). Stud Mycol 77:1–143

    Article  PubMed Central  PubMed  Google Scholar 

  • Su CH, Yang YZ, Ho HO, Hu CH, Sheu MT (2001) High-performance liquid chromatographic analysis for the characterization of triterpenoids from Ganoderma. J Chromatogr Sci 39:93–100

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Toth JO, Luu B, Ourisson G (1983) Les acides ganodériques T à Z: triterpenes cytotoxiques de Ganoderma lucidum. Tetrahedron Lett 24:1081–1084

    Article  CAS  Google Scholar 

  • Tyler VE (1971) Chemotaxonomy in the basidiomycetes. In: Petersen RH (ed) Evolution in the higher Basidiomycetes—an international symposium. The university of Tennessee press, Knoxville, pp 29–62

    Google Scholar 

  • Wang XM, Yang M, Guan SH, Liu RX, Xia JM, Bi KS, Gou DA (2006) Quantitative determination of six major triterpenoids in Ganoderma lucidum and related species by high performance liquid chromatography. J Pharm Biomed Anal 41:838–844

    Article  CAS  PubMed  Google Scholar 

  • Wang DM, Wu SH, Su CH, Peng JT, Shih YH, Chen LC (2009) Ganoderma multipileum, the correct name for ‘G. lucidum’ in tropical Asia. Bot Stud 50:451–458

    Google Scholar 

  • Wang XC, Xi RJ, Li Y, Wang DM, Yao YJ (2012) The species identity of the widely cultivated Ganoderma, ‘G. lucidum’ (Ling Zhi), in China. PLoS One 7:e40857

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wasser SP (2005) Reishi or Ling Zhi (Ganoderma lucidum). Encyclopedia of Dietary Supplements. M. Dekker 603–621

  • Welti S, Courtecuisse R (2010) The Ganodermataceae in the French West Indies (Guadeloupe and Martinique). Fungal Divers 43:103–126

    Article  Google Scholar 

  • Welti S, Moreau PA, Azaroual N, Lemoine A, Duhal N, Kouach M, Millet R, Courtecuisse R (2009) Antiproliferative activities of methanolic extracts from a Neotropical Ganoderma species: identification and characterization of a novel ganoderic acid. Int J Med Mushrooms 12:17–31

    Article  Google Scholar 

  • Weng CJ, Chau CF, Chen KD, Chen DH, Yen GC (2007) The anti–invasive effect of lucidenic acids isolated from a new Ganoderma lucidum strain. Mol Nutr Food Res 51:1472–1477

    Article  CAS  PubMed  Google Scholar 

  • Weng CJ, Chau CF, Hsieh YS, Yang SF, Yen GC (2008) Lucidenic acid inhibits PMA-induced invasion of human hepatoma cells through inactivating MAPK/ERK signal transduction pathway and reducing binding activities of NF–κB and AP–1. Carcinogenesis 29:147–156

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA et al (eds) PCR Protocols: a guide to methods and applications. Academic, San Diego, pp 315–322

    Google Scholar 

  • Winner M, Gimenez A, Schmidt H, Sontag B, Steffan B, Steglich W (2004) Unusual pulvinic acid dimers from the common fungi Scleroderma citrinum (Common Earthball) and Chalciporus piperatus (Peppery Bolete). Angew Chem Int Ed 43:1883–1886

    Article  CAS  Google Scholar 

  • Wu TS, Shi LS, Kuo SC (2001) Cytotoxicity of Ganoderma lucidum triterpenes. J Nat Prod 64:1121–1122

    Article  CAS  PubMed  Google Scholar 

  • Xia Q, Zhang H, Sun X, Zhao H, Wu L, Zhu D, Yang G, Shao Y, Zhang X, Mao X, Zhang L, She GA (2014) Comprehensive review of the structure elucidation and biological activity of triterpenoids from Ganoderma spp. Molecules 19:17478–17535

    Article  PubMed  Google Scholar 

  • Xu JW, Zhao W, Zhong JJ (2010) Biotechnological production and application of ganoderic acids. Appl Micro Biotechnol 87:457–466

    Article  CAS  Google Scholar 

  • Yang M, Wang X, Guan S, Xia J, Sun J, Guo H, Guo DA (2007) Analysis of triterpenoids in Ganoderma lucidum using liquid chromatography coupled with electrospray ionization mass spectrometry. J Am Mass Spectrom 18:927–939

    Article  CAS  Google Scholar 

  • Yao YJ, Wang XC, Wang B (2013) Epitypification of Ganoderma sichuanense J.D. Zhao & X.Q. Zhang (Ganodermataceae). Taxon 62:1025–1031

    Article  Google Scholar 

  • Ying J, Mao X, Ma Q, Zong Y, Wen H (1987) Icons of medicinal fungi from China. Science Press, Beijing

    Google Scholar 

  • Zamora JC, Calonge FD, Martín MP (2015) Integrative taxonomy reveals an unexpected diversity in Geastrum section Geastrum (Geastrales, Basidiomycota). Persoonia 34:130–165

    Article  Google Scholar 

  • Zhao JD (1989) The Ganodermataceae in China. Gebruder Bibliotheca Mycologica Ser Borntraeger Verlagsbuchhandlung, Science Publishers 132pp 1–176

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Acknowledgments

We thank Jean-Paul Bonte, Jean-François Goossens, Mostafa Kouach and Brigitte Callens (CUMA), Ines Devred and Christophe Lécuru (Laboratoire des Sciences Végétales et Fongiques), Jean-François Goossens, Catherine Foulon, Nadège Schifano and Valérie Verones (Laboratoire de Chimie Analytique) for their technical assistance, Jean-Michel Bellanger (CEFE-CNRS, Montpellier) for his attempts to get DNA sequences from vouchers and Béatrice Boury (DSI, Université Lille 2) for computer assistance. We also thank David Navarro and “Le Centre Internationational de Ressources Microbiennes (CIRM)”, INRA, Aix-Marseille Université, UMR1163 BBF, ESIL Polytech. Jean-Pierre Fiard (Fort-de-France, Martinique) and Félix Lurel (Petit-Bourg, Guadeloupe) are warmly acknowledged for logistics and accommodation during field work in the French West Indies, as is Christian Lechat (Virollet, France) for field assistance. Material from Guadeloupe and Martinique was collected in the research program “Lesser Antilles Fungi; diversity, ecology and conservation”—(R. Courtecuisse) and financially supported by DIREN Guadeloupe (Regional Environment Administration—Luc Legendre), DIREN Martinique (Vincent Arenales del Campo), ONF Martinique (National Forestry Office, regional direction—Philippe Richard and Jean-Baptiste Schneider). The Parc National de Guadeloupe administration is thanked for yearly collecting authorizations in the protected areas of Guadeloupe. Cony Decock gratefully acknowledges the financial support received from the FNRS / FRFC (convention FRFC 2.4544.10) and from the Belgian State—Belgian Federal Science Policy through the BCCM™ research program. Finally, we are grateful to Pr. Terry Henkel and Dr. Michael Howsam for English revision and helpful comments.

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Welti, S., Moreau, P., Decock, C. et al. Oxygenated lanostane-type triterpenes profiling in laccate Ganoderma chemotaxonomy. Mycol Progress 14, 45 (2015). https://doi.org/10.1007/s11557-015-1066-7

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  • DOI: https://doi.org/10.1007/s11557-015-1066-7

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