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Lichen Metabolites: An Overview of Some Secondary Metabolites and Their Biological Potential

  • Michal GogaEmail author
  • Ján Elečko
  • Margaréta Marcinčinová
  • Dajana Ručová
  • Miriam Bačkorová
  • Martin Bačkor
Living reference work entry
Part of the Reference Series in Phytochemistry book series (RSP)

Abstract

Lichens present a symbiotic association between two or more organisms. These unique organisms produce many chemical compounds, known as secondary metabolites or lichen acids. Most of them are localized in the cortex and form specific crystals on the surface of the fungal hyphae. Approximately 1000 secondary metabolites were discovered so far and most of them are specific for lichens. Lichen secondary metabolites showed many pharmaceutical activities, including antimicrobial, antiproliferative, antioxidant, antiviral, anti-inflammatory and further allelopathic, antiherbivore, photoprotective activities. Lichens are important source of bioactive compounds, and despite a lot of studies dealing with activity of lichen secondary metabolites, their production in lichens and their role is still very enigmatic. In this present chapter, we demonstrated all three main pathways of how secondary compounds originate and chose most characteristic acids with their proposed biological and ecological activities. This chapter gives a basic overview of lichens, secondary metabolites, and their properties.

Keywords

Symbiosis Lichens Biosynthetic pathways Secondary metabolites Pharmaceutical activities 

Notes

Acknowledgments

We thank to Irene Lichtscheidl for providing the imaging equipment at Core Facility Cell Imaging and Ultrastructure Research and Marianna Gazdíková for critical reading and reviewing this manuscript. This work was supported by Aktion Österreich – Slowakei, grant from Slovak Grant Agency VEGA 1/0792/16, grant KEGA- 012UPJŠ-4/2016, and grant VVGS-PF-2018-765.

References

  1. 1.
    Taylor TN, Taylor EL (1993) The biology and evolution of fossil plants. Prentice Hall, Englewood CliffsGoogle Scholar
  2. 2.
    Atsatt PR (1991) Fungi and the origin of land plants. In: Margulis L, Fester R (eds) Symbiosis as a source of evolutionary innovation. The MIT Press, Cambridge, MA/LondonGoogle Scholar
  3. 3.
    Newsham KK, Fitter AH, Watkinson AR (1995) Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J Ecol 83:991–1000CrossRefGoogle Scholar
  4. 4.
    Selosse MA, Le Tacon F (1998) The land flora: a phototroph-fungus partnership? Trees 13:5–20Google Scholar
  5. 5.
    Hawksworth DL, Kirk PM, Sutton BC, Pegler DN (1995) Ainsworth and Bisby’s dictionary of the fungi, 8th edn. CAB International, WallingfordGoogle Scholar
  6. 6.
    Kosanić M, Ranković B (2015) Lichen secondary metabolites as potential antibiotic agents. In: Ranković B (ed) Lichen secondary metabolites bioactive properties and pharmaceutical potential. Springer International Publishing, Springer Cham Heidelberg New York Dordrecht London, pp. 81–104Google Scholar
  7. 7.
    Larson DW (1987) The absorption and release of water by lichens. Bibl Lichenologica 25:351–360Google Scholar
  8. 8.
    Nash TH (2008) Lichen biology, 2nd edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  9. 9.
    Spribille T, Tuovinen V, Resl P, Vanderpool D, Wolinski H, Aime MC, Schneider K, Stabentheiner E, Toome-Heller M, Thor G, Mayrhofer H, Johannesson H, McCutcheon JP (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353:488–492PubMedCentralCrossRefPubMedGoogle Scholar
  10. 10.
    Yuan X, Xiao S, Taylor TN (2005) Lichen-like symbiosis 600 million years ago. Science 308:1017–1020CrossRefGoogle Scholar
  11. 11.
    Gargas A, DePriest PT, Grube M, Tehler A (1995) Multiple origins of lichen symbiosis in fungi suggested by SSU rDNA phylogeny. Science 268:1492–1495CrossRefGoogle Scholar
  12. 12.
    Lutzoni F, Pagel M, Reeb V (2001) Major fungal lineages are derived from lichen symbiotic ancestors. Nature 411:937–940CrossRefGoogle Scholar
  13. 13.
    Palice Z, Halda JP (2005) Neviditelný svět mikrolišejníků. Živa 2:57–59Google Scholar
  14. 14.
    Aschenbrenner IA, Cernava T, Berg G, Grube M (2016) Understanding microbial multi-species symbioses. Front Microbiol 7:180PubMedCentralCrossRefPubMedGoogle Scholar
  15. 15.
    Honegger R (1991) Functional aspects of the lichens symbiosis. Annu Rev Plant Physiol 42:553–578CrossRefGoogle Scholar
  16. 16.
    Gilbert OL (2000) Lichens. Harper Collins Publishers, LondonGoogle Scholar
  17. 17.
    Purvis OW, Pawlik-Skowrońska B (2008) Lichens and metals. Br Mycol Symp 27:175–200CrossRefGoogle Scholar
  18. 18.
    Tschermak-Woess E (1988) The algal partner. In: Galun M (ed) CRC handbook of lichenology. CRC Press, Boca RatonGoogle Scholar
  19. 19.
    Büdel B (1992) Taxonomy of lichenized procaryotic blue-green algae. In: Reisser W (ed) Algae and symbioses. Biopress Limited, BristolGoogle Scholar
  20. 20.
    Bold H, Wynne MJ (1958) Introduction to the algae and reproduction. Englewood Cliffs, Prentice HallGoogle Scholar
  21. 21.
    Van de Hoek C, Mann DG, Jahns HM (1993) Algen. Einfühtung in die Phykologie. Thieme, StuttgartGoogle Scholar
  22. 22.
    Hawksworth DL (1988) The variety of fungal-algal symbioses, their evolutionary significance, and the nature of lichens. Bot J Linn Soc 96:3–20CrossRefGoogle Scholar
  23. 23.
    Margulis L, Fester R (1991) Symbiosis as a source of evolutionary innovation: speciasion and morphogenesis. MIT Press, CambridgeGoogle Scholar
  24. 24.
    Jahns HM (1988) The lichen thallus. In: Galun M (ed) CRC handbook of lichenology. CRC Press, Boca RatonGoogle Scholar
  25. 25.
    Büdel B, Scheidegger C (2008) Thallus morphology and anatomy. In: Nash TH (ed) Lichen biology, 2nd edn. Cambridge University Press, CambridgeGoogle Scholar
  26. 26.
    Bačkor M (2011) Lichens and heavy metals: toxicity and tolerance. Pavol Jozef Šafárik University in Košice, KošiceGoogle Scholar
  27. 27.
    Mitrović T, Stamenković S, Cvetković V, Tošić S, Stanković M, Radojević I, Stefanović O, Comić L, Dačić D, Curčić M, Marković S (2011) Antioxidant, antimicrobial and antiproliferative activities of five lichen species. Int J Mol Sci 12:5428–5448PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    Lawrey JD (1986) Biological role of lichen substances. Bryologist 89:111–122CrossRefGoogle Scholar
  29. 29.
    Huneck S, Yoshimura I (1996) Identification of lichen substances. Springer, BerlinCrossRefGoogle Scholar
  30. 30.
    Fahselt D (1994) Carbon metabolism in lichens. Symbiosis 17:127–182Google Scholar
  31. 31.
    Hale ME (1983) The biology of lichens, 3rd edn. Edward Arnold, LondonGoogle Scholar
  32. 32.
    Culberson WL (1970) Chemosystematics and ecology of lichen-forming fungi. Annu Rev Ecol Syst 1:153–170CrossRefGoogle Scholar
  33. 33.
    Galun M, Shomer-Ilan A (1988) Secondary metabolic products. In: Galun M (ed) CRC handbook of lichenology. CRC Press, Boca RatonGoogle Scholar
  34. 34.
    Stocker-Wörgötter E (2008) Metabolic diversity of lichen-forming ascomycetous fungi: culturing polyketide and shikimate metabolite production and PKS genes. Nat Prod Rep 25:188–200CrossRefGoogle Scholar
  35. 35.
    Solhaug KA, Lind M, Nybakken L, Gauslaa Y (2009) Possible functional roles of cortical depsides and medullary depsidones in the foliose lichen Hypogymnia physodes. Flora 204:40–48CrossRefGoogle Scholar
  36. 36.
    Rundel PW (1978) The ecological role of secondary lichen substances. Biochem Syst Ecol 6:157–170CrossRefGoogle Scholar
  37. 37.
    Culberson CF, Elix JA (1989) Lichen substances. In: Dey PM, Harborne JB (eds) Methods in plant biochemistry: plant Phenolics. Academic, LondonGoogle Scholar
  38. 38.
    Molnar K, Farkas E (2010) Current results on biological activities of lichen secondary metabolites: a review. Z Naturforsch C 65:157–173CrossRefGoogle Scholar
  39. 39.
    Kosanić M, Monojlović N, Janković S, Stanojković T, Ranković B (2013) Evernia prunastri and Pseudoevernia furfuraceae lichens and their major metabolites as antioxidant, antimicrobial and anticancer agents. Food Chem Toxicol 53:112–118CrossRefGoogle Scholar
  40. 40.
    Kizil HE, Ağar G, Mustafa A (2014) Cytotoxic and antiproliferative effects of evernic acid on HeLa cell lines: a candidate anticancer drug. J Biotechnol 185:S29CrossRefGoogle Scholar
  41. 41.
    Endo T, Takahagi T, Kinoshida Y, Yamamoto Y, Sato F (1998) Inhibition of photosystem II on spinach by lichen-derived depsides. Biosci Biotechnol Biochem 62:2023–2027CrossRefGoogle Scholar
  42. 42.
    Bogo D, Matos MFC, Honda NK, Pontes EC, Oguma PM, da Santos EC, de Carvalho JE, Nomizo A (2010) In vitro antitumor activity of orsellinates. Z Naturforsch C 65:43–48CrossRefGoogle Scholar
  43. 43.
    Thadhani VM, Choudhary MI, Ali S, Omar I, Siddique H, Karunaratne V (2011) Antioxidant activity of some lichen metabolites. Nat Prod Res 25:1827–1837CrossRefGoogle Scholar
  44. 44.
    Ranković B, Mišić M (2008) The antimicrobial activity of the lichen substances of the lichens Cladonia furcata, Ochrolechia androgyna, Parmelia caperata and Parmelia conspersa. Biotechnol Equip 22:1013–1016CrossRefGoogle Scholar
  45. 45.
    Ranković B, Mišić M, Sukdolak S (2008) The antimicrobial activity of substances derived from the lichens Physcia aipolia, Umbilicaria polyphylla, Parmelia caperata and Hypogymnia physodes. World J Michrobiol Biotechnol 24:1239–1242CrossRefGoogle Scholar
  46. 46.
    Gomes AT, Honda NK, Roese FM, Muzzi RM, Marques MR (2002) Bioactive derivates obtained from lecanoric acid, a constituent of the lichen Parmotrema tinctorum (Nyl.) Hale (Parmeliaceae). Rev Bras Farm 12:74–75CrossRefGoogle Scholar
  47. 47.
    Buçukoglu TZ, Albayrak S, Halici MG, Tay T (2012) Antimicrobial and antioxidant activities of extracts and lichen acids obtained from some Umbilicaria species from Central Anatolia, Turkey. J Food Process Preserv 37:1103–1110CrossRefGoogle Scholar
  48. 48.
    Candan M, Yilmaz M, Tay T, Kivanç M, Türk H (2006) Antimicrobial activity of extracts of the lichen Xanthoparmelia pokornyi and its gyrophoric and stenosporic acid constituents. Z Naturforsch C 61:319–323CrossRefGoogle Scholar
  49. 49.
    Bačkorová M, Bačkor M, Mikeš J, Jendželovský R, Fedoročko P (2011) Variable responses of different human cancer cells to the lichen compounds parietin, atranorin, usnic acid and gyrophoric acid. Toxicol In Vitro 25:37–44CrossRefGoogle Scholar
  50. 50.
    Kosanić M, Ranković B, Stanojković T, Rančić A, Manojlović N (2014) Cladonia lichens and their major metabolites as possible natural antioxidant, antimicrobial and anticancer agents. Food Sci Technol 59:518–525Google Scholar
  51. 51.
    Bačkorová M, Jendželovský R, Kello M, Bačkor M, Mikeš J, Fedoročko P (2012) Lichen secondary metabolites are responsible for induction of apoptosis in HT-29 and A2780 human cancer cell lines. Toxicol In Vitro 26:462–468CrossRefGoogle Scholar
  52. 52.
    Correché ER, Enriz RD, Piovano M, Garbarino J, Gómez-Lechón MJ (2004) Cytotoxic and apoptotic effects on hepatocytes of secondary metabolites obtained from lichens. Altern Lab Anim 32:605–615Google Scholar
  53. 53.
    Cankılıç MY, Sarıözlü NY, Candan MC, Tay F (2017) Screening of antibacterial, antituberculosis and antifungal effects of lichen Usnea florida and its thamnolic acid constituent. Biomed Res 28:3108–3113Google Scholar
  54. 54.
    Nishanth KS, Sreerag RS, Deepa I, Mohandas C, Nambisan B (2015) Protocetraric acid: an excellent broad spectrum compound from the lichen Usnea albopuncta against medically important microbes. Nat Prod Res 29:574–577CrossRefGoogle Scholar
  55. 55.
    Honda NK, Pavan FR, Coelho RG, de Andrade Leite SR, Micheletti AC, Lopes TI, Misutsu MY, Beatriz A, Brum RL, Leite CQ (2010) Antimycobacterial activity of lichen substances. Phytomedicine 17:328–332CrossRefGoogle Scholar
  56. 56.
    de Barros Alves GM, de Sousa Maia MB, de Souza FE et al (2014) Expectorant and antioxidant activities of purified fumarprotocetraric acid from Cladonia verticillaris lichen in mice. Pulm Pharmacol Ther 27:139–143CrossRefGoogle Scholar
  57. 57.
    Yilmaz M, Türk AO, Tay T, Kivanç M (2004) The antimicrobial activity of extracts of the lichen Cladonia foliacea and its (−)-usnic acid, atranorin, and fumarprotocetraric acid constituents. Z Naturforsch C 59:249–254CrossRefGoogle Scholar
  58. 58.
    Cardile V, Graziano ACE, Avola R, Piovano M, Russo A (2017) Potential anticancer activity of lichen secondary metabolite physodic acid. Chem Biol Interact 263:36–45CrossRefGoogle Scholar
  59. 59.
    Türk H, Yilmaz M, Tay T, Türk AO, Kivanç M (2006) Antimicrobial activity of extracts of chemical races of the lichen Pseudevernia furfuracea and their physodic acid, chloroatranorin, atranorin, and olivetoric acid constituens. Z Naturforsch C 61:499–507CrossRefGoogle Scholar
  60. 60.
    Amo de Paz G, Gomez-Serranillos MP, Palomino OM, González-Burgos E, Carretero ME, Crespo A (2010) HPLC isolation of antioxidant constituents from Xanthoparmelia spp. J Pharm Biomed 53:165–171CrossRefGoogle Scholar
  61. 61.
    Papadopoulou P, Tzakou O, Vagias C, Kefalas P, Roussis V (2007) Beta-orcinol metabolites from the lichen Hypotrachyna revolute. Molecules 12:997–1005PubMedCentralCrossRefPubMedGoogle Scholar
  62. 62.
    Pejin B, Iodice C, Bogdanović G, Kojić V, Tešević V (2017) Stictic acid inhibits cell growth of human colon adenocarcinoma HT-29 cells. Arab J Chem 10:1240–1242CrossRefGoogle Scholar
  63. 63.
    Ranković B (2015) Lichen secondary metabolites. Springer, LondonCrossRefGoogle Scholar
  64. 64.
    Goga M, Pöykkö H, Adlassnig W, Bačkor M (2016) Response of the lichen-eating moth Cleorodes lichenaria larvae to varying amounts of usnic acid in the lichens. Arthropod Plant Interact 10:71–77CrossRefGoogle Scholar
  65. 65.
    Waring B (2008) Light exposure affects secondary compound diversity in lichen communities in Monteverde, Costa Rica. Penn Sci J 6:11–13Google Scholar
  66. 66.
    Mayer M, O’Neill MA, Murray KE, antos-Magalhaes NS, Carneiro-Leao AM, Thompson AM, Appleyard VC (2005) Usnic acid: a non-genotoxic compound with anticancer properties. Anti-Cancer Drugs 16:805–809CrossRefGoogle Scholar
  67. 67.
    Han D, Matsumaru K, Rettori D, Kaplowitz N (2004) Usnic acid-induced necrosis of cultured mouse hepatocytes: inhibition of mitochondrial function and oxidative stress. Biochem Pharmacol 67:439–451CrossRefGoogle Scholar
  68. 68.
    Goga M, Antreich SJ, Bačkor M, Weckwerth W, Lang I (2017) Lichen secondary metabolites affect growth of Physcomitrella patens by allelopathy. Protoplasma 254:1307–1315CrossRefGoogle Scholar
  69. 69.
    Goga M, Ručová D, Kolarčik V, Sabovljević M, Bačkor M, Lang I (2018) Usnic acid, as a biotic factor, changes the ploidy level in mosses. Ecol Evol 8:2781–2787PubMedCentralCrossRefPubMedGoogle Scholar
  70. 70.
    Gollapudi SR, Telikepalli H, Jampani HB, Mirhom YW, Drake SD, Bhattiprolu KR, Vander Velde D, Mitscher LA (1994) Alectosarmentin, a new antimicrobial dibenzofuranoid lactol from the lichen, Alectoria sarmentosa. J Nat Prod 57:934–938CrossRefGoogle Scholar
  71. 71.
    Læssøe T, Srikitikulchai P, Fournier J, Köpcke B, Stadler M (2010) Lepraric acid derivates as chemotaxic markers in Hypoxylon aeruginosum, Chlorostroma subcubisporum and C. cyaninum, sp. nov. Fungal Biol 114:481–489CrossRefGoogle Scholar
  72. 72.
    Abdel-Lateff A, Fisch K, Wright AD (2003) Two new xanthone derivates from the algicolous marine fungus Wardomyces anomalus. J Nat Prod 66:706–708CrossRefGoogle Scholar
  73. 73.
    Ebada SS, Schultz B, Wray V, Totzke F, Kubbutat MH, Müller WE, Hamacher A, Kassack MU, Lin W, Proksch P (2011) Arthrinins A-D: novel diterpenoids and further constituents from the sponge derived fungus Arthrinium sp. Bioorg Med Chem 19:4644–4651CrossRefGoogle Scholar
  74. 74.
    Huneck S, Schreiber K (1972) Wachstumsregulatorische eigenschaften von flechten-und moos-inhaltsstoffen. Phytochemistry 11:2429–2434CrossRefGoogle Scholar
  75. 75.
    Dayan FE, Romagni JG (2001) Lichens as a potential source of pesticides. Pestic Outlook 12:229–232CrossRefGoogle Scholar
  76. 76.
    Manojlovic NT, Solujic S, Sukdolak S, Krstic LJ (2000) Isolation and antimicrobial activity of anthraquinones from some species of the lichen genus Xanthoria. J Serb Chem Soc 65:555–560CrossRefGoogle Scholar
  77. 77.
    Lin L, Chou C, Kuo Y (2001) Cytotoxic principles from Ventilago leiocarpa. J Nat Prod 64(5):674–676CrossRefGoogle Scholar
  78. 78.
    Muzychkina RA (1998) Natural anthraquinones, biological and physicochemical properties. House Phasis, MoscowGoogle Scholar
  79. 79.
    Manojlovic NT, Solujic S, Sukdolak S (2002) Antimicrobial activity of an extract and anthraquinones from Caloplaca schaereri. Lichenologist 34:83–85CrossRefGoogle Scholar
  80. 80.
    Schinazi RF, Chu CK, Babu JR, Oswald BJ, Saalmann V, Cannon DL, Eriksson BFH, Nasr M (1990) Anthraquinones as a new class of antiviral agents against human immunodeficiency virus. Antivir Res 13:265–272CrossRefGoogle Scholar
  81. 81.
    Cohen PA, Hudson JB, Towers GHN (1996) Antiviral activities of anthraquinones, bianthrones and hypericin derivatives from lichens. Experientia 52:180–183CrossRefGoogle Scholar
  82. 82.
    Koyama M, Takahashi K, Chou TC, Darzynkiewicz Z, Kapuscinski J, Kelly TR, Watanabe KA (1989) Intercalating agents with covalent bond forming capability. A novel type of potential anticancer agents. 2. Derivatives of chrysophanol and emodin. J Med Chem 32:1594–1599CrossRefGoogle Scholar
  83. 83.
    Hill DJ, Woolhouse HW (1966) Aspects of the antecology of Xanthoria parietina agg. Lichenologist 3:207–214CrossRefGoogle Scholar
  84. 84.
    Fahselt D (1994) Secondary biochemistry of lichens. Symbiosis 16:117–165Google Scholar
  85. 85.
    Solhaug KA, Gauslaa Y (2004) Photosynthates stimulate the UV-B induced fungal anthraquinone synthesis in the foliose lichen Xanthoria parietina. Plant Cell Environ 27:167–176CrossRefGoogle Scholar
  86. 86.
    Gauslaa Y, Ustvedt EM (2003) Is parietin a UV-B or a bluelight screening pigment in the lichen Xanthoria parietina? Photochem Photobiol Sci 2:424–432CrossRefGoogle Scholar
  87. 87.
    Silberstein L, Siegel BZ, Siegel SM, Mukhtar A, Galun M (1996) Comparative studies on Xanthoria parietina, a pollution-resistant lichen, and Ramalina duriaei, a sensitive species. I. Effects of air pollution on physiological processes. Lichenologist 28:355–365CrossRefGoogle Scholar
  88. 88.
    Kahriman N, Yazici K, Arslan T, Aslan A, Karaoglu SA, Yayli N (2011) Chemical composition and antimicrobial activity of the essential oils from Evernia prunastri (L.) ach. and Evernia divaricata (L.) ach. Asian J Chem 23:1937–1939Google Scholar
  89. 89.
    Rajab MS, Cantrell CL, Franzblau SG, Fischer NH (1998) Antimycobacterial activity of (E)-phytol and derivates: a preliminary structure-activity study. Planta Med 64:2–4CrossRefGoogle Scholar
  90. 90.
    Shukla V, Joshi G, Rawat M (2010) Lichens as a potential natural source of bioactive compounds: a review. Phytochem Rev 9:303–314CrossRefGoogle Scholar
  91. 91.
    Kosanić M, Ranković B, Sukdolak S (2010) Antimicrobial activity of the lichen Lecanora frustulosa and Parmeliopsis hyperopta and their divaricatic acid and zeorin constituents. Afr J Microbiol Res 4:885–890Google Scholar
  92. 92.
    Gonzalez AG, Rodrigues Perez EM, Hernandez PCE, Barrera JB (1992) Chemical constituents of the lichen Stereocaulon azorerum. Z Naturforsch C 47:503–507CrossRefGoogle Scholar
  93. 93.
    Dahlman L, Näsholm T, Palmqwist K (2001) Growth, nitrogen uptake and resource allocation in the two tripartire lichens Nephroma arctucim and Peltigera aphthosa during nitrogen stress. New Phytol 153:307–315CrossRefGoogle Scholar
  94. 94.
    Safe S, Safe LM, Maass WSG (1975) Sterols of three lichen species: Lobaria pulmonaria, Lobaria scrobiculata and Usnea longissima. Phytochemistry 14:1821–1823CrossRefGoogle Scholar
  95. 95.
    Shukla V, Negi S, Rawat MSM, Pant G, Nagatsu A (2004) Chemical study of Ramalina africana (Ramaliniaceae) from Garhwal Himalayas. Biochem Syst Ecol 32:449–453CrossRefGoogle Scholar
  96. 96.
    Goodwin TW (1980) Algae. In: Goodwin TW (ed) The biochemistry of the carotenoids, vol 1, 2nd edn. Chapmann and Hall, London/New YorkCrossRefGoogle Scholar
  97. 97.
    Goodwin TW, Britton G (1988) Distribution and analysis of carotenoids. In: Goodwin TW (ed) Plant pigments. Academic, London/San DiegoGoogle Scholar
  98. 98.
    Czeczuga B (1980) Investigation on carotenoids in Embryophyta. I Bryophyta Bryologist 83:21–28CrossRefGoogle Scholar
  99. 99.
    Edwards HGM, Rull Perez F (1999) Lichen biodeteriorarion of the Convento de la Peregrina, Sahagun, Spain. Biospectroscopy 5:47–52CrossRefGoogle Scholar
  100. 100.
    Czeczuga B (1987) The effect of light on the content of photosynthetically active pigments in plants. VII. Chromatic adaptation in the lichens Peltigera polydactyla and Peltigera rufescens. Phyton 26:201–208Google Scholar
  101. 101.
    Taiz L, Zeiger E (2010) Plant physiology, 5th edn. Sinauer Associates Inc, SunderlandGoogle Scholar
  102. 102.
    Knecht W, Henseling J, Löffler M (2000) Kinetics of inhibition of human and rat dihydroorotate dehydrogenase by atovaquone, lawsone derivates, brequinar sodium and polyporic acid. Chem Biol Interact 124:61–76CrossRefGoogle Scholar
  103. 103.
    Kraft J, Bauer S, Keilhoff G, Miersch J, Wend D, Riemann D, Hirschelmann R, Holzhausen HJ, Langner J (1998) Biological effects of the dihydroorotate dehydrogenase inhibitor polyporic acid, a toxic constituent of the mushroom Hapalopilus rutilans, in rats and humans. Arch Toxicol 72:711–721CrossRefGoogle Scholar
  104. 104.
    Burton JF, Cain BF (1959) Antileukaemic activity of polyporic acid. Nature 184:1326–1327CrossRefGoogle Scholar
  105. 105.
    Kwak JY, Rhee IK, Lee KB, Hwang JS, Yoo ID, Song KS (1999) Thelephoric acid and kynapcin-9 in mushroom Polyozellus multiflex inhibit prolyl endopeptidase in vitro. J Microbiol Biotechnol 9:798–803Google Scholar
  106. 106.
    Chung SK, Jeon SY, Kim SK, Kim SI, Kim GS, Kwon SH (2004) Antioxidative effects of polyozellin and thelephoric acid isolated from Polyzellus multiplex. J Korean Soc Appl Biol Chem 47:283–286Google Scholar
  107. 107.
    Rao PS, Sarma KG, Seshadri TR (1965) Chemical components of the Lobaria lichens from the Western Himalayas. Curr Sci India 34:9–11Google Scholar
  108. 108.
    Abo-Khatwa AN, al-Robai AA, al-Jawhari DA (1996) Lichen acids as uncouplers of oxidative phosphorylation of mouse-liver mitochondria. Nat Toxins 4:96–102CrossRefGoogle Scholar
  109. 109.
    Legouin B, Le Dévéhat FL, Ferron S, Rouaud I, Le Pogam P, Cornevin L, Bertrand M, Boustie J (2017) Specialized metabolites of the lichen Vulpicida pinastri act as photoprotective agents. Molecules 22:1162PubMedCentralCrossRefPubMedGoogle Scholar
  110. 110.
    Varol M, Turk A, Candan M, Tay T, Koparal AT (2016) Photoprotective activity of vulpinic and gyrophoric acids toward ultraviolet B-induced damage in human keratinocytes. Phytother Res 30:9–15CrossRefGoogle Scholar
  111. 111.
    Bačkor M, Hudá J, Repčák M, Ziegler W, Bačkorová M (1992) The influence of pH and lichen metabolites (Vulpinic acid and (+) usnic acid) on the growth of the lichen photobiont Trebouxia irregularis. Lichenologist 30:577–582Google Scholar
  112. 112.
    Emmerich R, Giez I, Lange OL, Proksch P (1993) Toxicity and antifeedant activity of lichen compounds against the polyphagous herbivorous insect Spodoptera littoralis. Phytochemistry 33:1389–1394CrossRefGoogle Scholar
  113. 113.
    Koparal AT (2015) Anti-angiogenic and antiproliferative properties of the lichen substances (−)-usnic acid and vulpinic acid. Z Naturforsch C 70:159–164CrossRefGoogle Scholar
  114. 114.
    Nadal B, Thetiot-Laurent S, Pin S, Renault JP, Cressier D, Rima G, Le Roux A, Meunier S, Wagner A, Lion C, Le Gall T (2010) Synthesis and antioxidant properties of pulvinic acids analogoues. Bioorg Med Chem 18:7931–7939CrossRefGoogle Scholar
  115. 115.
    Huang YT, Onose J, Abe N, Yoshikawa K (2009) In vitro inhibitory effects of pulvinic acid derivates isolated from Chinese edible mushrooms, Boletus calopus and Suillus bovinus, on cytochrome P450 activity. Biosci Biotechnol Biochem 23:855–860CrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Michal Goga
    • 1
    • 2
    Email author
  • Ján Elečko
    • 3
  • Margaréta Marcinčinová
    • 1
  • Dajana Ručová
    • 1
  • Miriam Bačkorová
    • 4
  • Martin Bačkor
    • 1
  1. 1.Department of BotanyInstitute of Biology and Ecology, University of Pavol Jozef ŠafárikKošiceSlovakia
  2. 2.Core Facility Cell Imaging and Ultrastructure ResearchUniversity of ViennaViennaAustria
  3. 3.Department of Organic ChemistryInstitute of Chemistry, University of Pavol Jozef ŠafárikKošiceSlovakia
  4. 4.Department of Pharmacognosy and BotanyUniversity of Veterinary Medicine and PharmacyKošiceSlovakia

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