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Axenic culture and biosynthesis of secondary compounds in lichen symbiotic fungi, the Parmeliaceae

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Abstract

Lichens produce unique secondary metabolites with a rich potential as bioactive compounds. In many cases, the use of these molecules is limited by the low concentration of these compounds in thalli, low growth rate in culture, and changes in chemical patterns between thalli and aposymbiotic culture. In addition, the massive collection of some species of industrial interest can cause damage to lichen diversity and the associated environment. Six lichenized fungi (Arctoparmelia centrifuga, Parmelia saxatilis, Parmelina tiliacea, Platismatia glauca, Xanthoparmelia tinctina, and Usnea ghattensis) with biotechnological interest and belonging to Parmeliaceae have been cultured in order to test culture conditions and obtain enough biomass for further studies. In addition, we analyzed the compounds synthetized in axenic conditions and they were compared with chemosyndromes identified in complete thalli. Arctoparmelia centrifuga, P. saxatilis, P. tiliacea and X. tinctina were successfully cultivated while for P. glauca and U. ghattensis we only obtained sporulation and germination of the spores. The chemical pattern of the compounds secreted into the culture media varied significantly from the chemosyndrome of the whole thallus. Phenolic compounds of pharmacological and industrial interest (usnic acid, aspicilin, α-alectoronic acid, physodic acid, lobaric acid and nordivaricatic acid) and a wide variety of potentially bioactive compounds were obtained during the culture process.

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References

  • Abdel-Hameed M, Bertrand RL, Piercey-Normore MD, Sorensen JL (2016) Putative identification of the usnic acid biosynthetic gene cluster by de novo whole-genome sequencing of a lichen-forming fungus. Fungal Biol 120:306–316

    CAS  PubMed  Google Scholar 

  • Ahmadjian V (1993) The lichen symbiosis. Wiley, Chichester

    Google Scholar 

  • Ahmadjian V, Reynolds JT (1961) Production of biologically active compounds by isolated lichenized fungi. Science 133:700–701

    CAS  PubMed  Google Scholar 

  • Alors D, Cendón Y, Divakar PK, Crespo A, Benítez NG, Molina MC (2019) Differences in sexual aposymbiotic phase of the reproductive cycle of Parmelina carporrhizans and Parmelina quercina. Possible implications in its reproductive biology. Lichenologist 51:175–186

    Google Scholar 

  • Alors D, Grande F, Cubas P, Crespo A, Schmitt I, Molina MC, Divakar PK (2017) Panmixia and dispersal from the Mediterranean Basin to Macaronesian Islands of a macrolichen species. Sci Rep 7:40879. https://doi.org/10.1038/srep40879

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anstett DN, Salcedo A, Larsen EW (2014) Growing foliose lichens on cover slips: a method for asexual propagation and observing development. Bryologist 117:179–187

    Google Scholar 

  • Aptroot A, Perez-Ortega S (2018) Xanthoparmelia beccae. The IUCN red list of threatened species 2018: e.T71639618A71640065

  • Aschenbrenner IA, Cernava T, Berg G, Grube M (2016) Understanding microbial multi-species symbioses. Front Microbiol 7:180

    PubMed  PubMed Central  Google Scholar 

  • Bate PNN, Orock AE, Nyongbela KD, Babiaka SB, Kukwah A, Ngemenya MN (2018) In vitro activity against multi-drug resistant bacteria and cytotoxicity of lichens collected from Mount Cameroon. J King Saud Univ Sci 32:614–619

    Google Scholar 

  • Behera BC, Makhija U (2001) Effect of various culture conditions on growth and production of salazinic acid in Bulbothrix setschwanensis (lichenized ascomycetes) in vitro. Curr Sci 80:1424–1427

    CAS  Google Scholar 

  • Behera BC, Verma N, Sonone A, Makhija U (2005) Antioxidant and antibacterial activities of lichen Usnea ghattensis in vitro. Biotechnol Lett 27:991–995

    CAS  PubMed  Google Scholar 

  • Behera BC, Verma N, Sonone A, Makhija U (2009) Optimization of culture conditions for lichen Usnea ghattensis G. Awasthi to increase biomass and antioxidant metabolite production. Food Technol Biotechnol 47:7–12

    CAS  Google Scholar 

  • Bertrand RL, Sorensen JL (2018) A comprehensive catalogue of polyketide synthase gene clusters in lichenizing fungi. J Ind Microbiol Biotechnol 45:1067–1081

    CAS  PubMed  Google Scholar 

  • Bertrand RL, Sorensen JL (2019) Lost in translation: challenges with heterologous expression of lichen polyketide synthases. ChemistrySelect 4:6473–6483

    CAS  Google Scholar 

  • Brodo IM, Sharnoff SD, Sharnoff S (2001) Lichens of North America. Yale University Press, New Haven and London

    Google Scholar 

  • Brunauer G, Hager A, Grube M, Türk R, Stocker-Wörgötter E (2007) Alterations in secondary metabolism of aposymbiotically grown mycobionts of Xanthoria elegans and cultured resynthesis stages. Plant Physiol Biochem 45:146–151

    CAS  PubMed  Google Scholar 

  • Bu'lock JD (1961) Intermediary metabolism and antibiotic synthesis. Adv Appl Microbiol 3:293–342

    CAS  PubMed  Google Scholar 

  • Calchera A, Dal Grande F, Bode HB, Schmitt I (2019) Biosynthetic gene content of the ‘perfume lichens’ Evernia prunastri and Pseudevernia furfuracea. Molecules 24:203

    PubMed Central  Google Scholar 

  • Castle H, Kubsch F (1949) The production of usnic, didymic, and rhodocladonic acids by the fungal component of the lichen Cladonia cristatella. Arch Biochem 23:158–160

    CAS  PubMed  Google Scholar 

  • Chooi Y, Stalker DM, Davis MA, Fujii I, Elix JA, Louwhoff SH, Lawrie AC (2008) Cloning and sequence characterization of a non-reducing polyketide synthase gene from the lichen Xanthoparmelia semiviridis. Mycol Res 112:147–161

    CAS  PubMed  Google Scholar 

  • Cocchietto M, Skert N, Nimis PL, Sava G (2002) A review on usnic acid, an interesting natural compound. Naturwissenschaften 89:137–146

    CAS  PubMed  Google Scholar 

  • Crittenden PD, Porter N (1991) Lichen-forming fungi: potential sources of novel metabolites. Trends Biotechnol 9:409–414

    CAS  PubMed  Google Scholar 

  • Culberson CF (1969) Chemical and botanical guide to lichen products. University of North Carolina Press, Chapel Hill

    Google Scholar 

  • de Paz GA, Raggio J, Gómez-Serranillos MP, Palomino OM, González-Burgos E, Carretero ME, Crespo A (2010) HPLC isolation of antioxidant constituents from Xanthoparmelia spp. J Pharm Biomed Anal 53:165–171

    PubMed  Google Scholar 

  • Deason DR, Bold HC (1960) Phycological studies. I. Exploratory studies of Texas soil algae. University of Texas Publication no. 6022. University of Texas, Austin, Texas, USA

  • Deduke C, Piercey-Normore MD (2015) Substratum preference of two species of Xanthoparmelia. Fungal Biol 119:812–822

    PubMed  Google Scholar 

  • Deduke C, Timsina B, Piercey-Normore MD (2012) Effect of environmental change on secondary metabolite production in lichen-forming Fungi. In: Young SS, Silvern SE (eds) International perspectives on global environmental change. InTech, pp 198–230

  • Devkota S, Chaudhary RP, Wert S, Scheidegger C (2017) Indigenous knowledge and use of lichens by the lichenophilic communities of the Nepal Himalaya. J Ethnobiol Ethnomed 13:15

    PubMed  PubMed Central  Google Scholar 

  • Devkota S, Weerakoon G (2017) Everniastrum nepalense. The IUCN red list of threatened species 2017: e.T109425875A109425892

  • Ebrahim HY, Akl MR, Elsayed HE, Hill RA, El Sayed KA (2017) Usnic acid Benzylidene analogues as potent mechanistic target of rapamycin inhibitors for the control of breast malignancies. J Nat Prod 80:932–952

    CAS  PubMed  Google Scholar 

  • Evans GC (1972) The quantitative analysis of plant growth (Vol. 1). University of California Press

  • Farkhutdinov RG, Saitova ZR, Shpirnava IA, Zaitsev DY, Sharipova GV (2018) Hormonal and antioxidant status of Physcia stellaris (L.) Nyl. Population growing in different natural zones of the republic of Bashkortostan. Vestnik Tomskogo Gosudarstvennogo Universiteta, Biologiya. Тom Roc Yh-ta Биология 42:176–191

    Google Scholar 

  • Fernández-Moriano C, Gómez-Serranillos MP, Crespo A (2016) Antioxidant potential of lichen species and their secondary metabolites. A systematic review. Pharm Biol 54:1–17

    PubMed  Google Scholar 

  • Fontaniella B, Millanes AM, Vicente C, Legaz ME (2004) Concanavalin a binds to a mannose-containing ligand in the cell wall of some lichen phycobionts. Plant Physiol Biochem 42:773–779

    CAS  PubMed  Google Scholar 

  • Gadea A, Le Lamer AC, Le Gall S, Jonard C, Ferron S, Catheline D, Ertz D, Le Pogam P, Boustie J, Maryvonne C, Lohezic - Le Devehat F (2018) Metabolite profiles of the lichen Argopsis friesiana may explain sectorial land snail damage. J Chem Ecol 44:471–472

    CAS  PubMed  Google Scholar 

  • Gaio-Oliveira G, Dahlman L, Máguas C, Palmqvist K (2004) Growth in relation to microclimatic conditions and physiological characteristics of four Lobaria pulmonaria populations in two contrasting habitats. Ecography 27:13–28

    Google Scholar 

  • Gómez-Serranillos MP, Fernández-Moriano C, González-Burgos E, Divakar PK, Crespo A (2014) Parmeliaceae family: phytochemistry, pharmacological potential and phylogenetic features. R Soc Chem Adv 4:59017–59047

    Google Scholar 

  • Gulluce M, Aslan A, Sokmen M, Sahin FIKRETTIN, Adiguzel A, Agar G, Sokmen A (2006) Screening the antioxidant and antimicrobial properties of the lichens Parmelia saxatilis, Platismatia glauca, Ramalina pollinaria, Ramalina polymorpha and Umbilicaria nylanderiana. Phytomedicine 13:515–521

    CAS  PubMed  Google Scholar 

  • Hong JM, Suh SS, Kim TK, Kim JE, Han SJ, Youn UJ, Jim JHK, II-C (2018) Anti-cancer activity of lobaric acid and lobarstin extracted from the antarctic lichen Stereocaulon alpnum. Molecules 23:658

    PubMed Central  Google Scholar 

  • Horák J, Materna J, Halda JP, Mladenović S, Bogusch P, Pech P (2019) Biodiversity in remnants of natural mountain forests under conservation-oriented management. Sci Rep 9:1–10

    Google Scholar 

  • Ingolfsdottir K (2002) Usnic acid. Phytochemistry 61:729–736

    CAS  PubMed  Google Scholar 

  • Ismed F, Lohézic-Le Dévéhat F, Delalande O, Sinbandhit S, Bakhtiar A, Boustie J (2012) Lobarin from the Sumatran lichen, Stereocaulon halei. Fitoterapia 83:1693–1698

    CAS  PubMed  Google Scholar 

  • Joulain D, Tabacchi R (2009) Lichen extracts as raw materials in perfumery. Part 1: oakmoss. Flavour Fragr J 24:49–61

    CAS  Google Scholar 

  • Karagoz A, Aslan A (2005) Antiviral and cytotoxic activity of some lichen extracts. Biologia-Bratislava 60:281

    Google Scholar 

  • Kosanić M, Ranković B, Stanojković TP (2012) Antioxidant, antimicrobial and anticancer activities of three Parmelia species. J Sci Food Agric 92:1909–1916

    PubMed  Google Scholar 

  • Lallemant R (1985) Le de!veloppement en cultures pures in vitro des mycosymbiotes des lichens. Can J Bot 63:681–703

    Google Scholar 

  • Latkowska E, Białczyk J, Węgrzyn M, Erychleb U (2019) Host species affects the phenolic compounds content in Hypogymnia physodes (L) Nyl thalli. Allelopathy J:47(2)

  • Leavitt SD, Lumbsch HT (2016) Ecological biogeography of lichen-forming Fungi. In: Druzhinina IS, Kubicek CP (eds) environmental and microbial relationships, 3rd edn. The Mycota IV. Springer international publishing, Switzerland, pp 15-37

  • Legaz ME, Armas R, Vicente V (2011) Bioproduction of depsidones for pharmaceutical purposes. In: Rundfeldt C (ed) Drug development – a case study based insight into modern strategies. In Tech, Rijeka, pp 492–493

    Google Scholar 

  • Legaz ME, Molina MC, Vicente C (2003) Lichen lectins: glycoproteins for cell recognition. Curr Top Plant Biol 4:63–78

    CAS  Google Scholar 

  • Lendemer J, Allen J, McMullin T (2020) Cladonia appalachiensis. The IUCN red list of threatened species 2020: e.T80702853A80702858

  • Lilly VG, Barnett HL (1951) Physiology of the Fungi. McGraw-Hill, New York

    Google Scholar 

  • Machado NM, Ribeiro AB, Nicolella HD, Ozelin SD, Silva LHDD, Guissone APP, Rinaldi-Neto F, Limonti IL, Furtado RRA, Cunha WR, Rezende AAAD, Spanó MA, Tavares DC (2019) Usnic acid attenuates genomic instability in Chinese hamster ovary (CHO) cells as well as chemical-induced preneoplastic lesions in rat colon. J Toxic Environ Health A 82:401–410

    CAS  Google Scholar 

  • Manojlović N, Ranković B, Kosanić M, Vasiljević P, Stanojković T (2012) Chemical composition of three Parmelia lichens and antioxidant, antimicrobial and cytotoxic activities of some their major metabolites. Phytomedicine 19:1166–1172

    PubMed  Google Scholar 

  • McDonald T, Gaya E, Lutzoni F (2013) Twenty-five cultures of lichenizing fungi available for experimental studies on symbiotic systems. Symbiosis 59:165–171

    Google Scholar 

  • Meessen J, Ott S (2013) Recognition mechanisms during the pre-contact state of lichens: I. Mycobiont-photobiont interactions of the mycobiont of Fulgensia bracteata. Symbiosis 59:131–143

    CAS  Google Scholar 

  • Miao V, Coëffet-LeGal MF, Brown D, Sinnemann S, Donaldson G, Davies J (2001) Genetic approaches to harvesting lichen products. Trends Biotechnol 19:349–355

    CAS  PubMed  Google Scholar 

  • Millot M, Girardot M, Dutreix L, Mambu L, Imbert C (2017) Antifungal and anti-biofilm activities of acetone lichen extracts against Candida albicans. Molecules 22:651

    PubMed Central  Google Scholar 

  • Millot M, Tomasi S, Articus K, Rouaud I, Bernard A, Boustie J (2007) Metabolites from the lichen Ochrolechia parella growing under two different heliotropic conditions. J Nat Prod 70:316–318

    CAS  PubMed  Google Scholar 

  • Millot M, Tomasi S, Sinbandhit S, Boustie J (2008) Phytochemical investigation of Tephromela atra: NMR studies of collatolic acid derivatives. Phytochem Lett 1:139–143

    CAS  Google Scholar 

  • Molina MC, Crespo A (2000) Comparison of development of axenic cultures of five species of lichen-forming fungi. Mycol Res 104:595–602

    Google Scholar 

  • Molina MC, Crespo A, Vicente C, Elix JA (2003) Differences in the composition of phenolics and fatty acids of cultured mycobiont and thallus of Physconia distorta. Plant Physiol Biochem 41:175–180

    CAS  Google Scholar 

  • Molina MC, Divakar PK, González N (2015) Success in the isolation and axenic culture of Anaptychia ciliaris (Physciaceae, Lecanoromycetes) mycobiont. Mycoscience 56:351–358

    CAS  Google Scholar 

  • Molina MC, Divakar PK, Zhang N, González N, Struwe L (2013) Non-developing ascospores found in apothecia of asexually reproducing lichen-forming fungi. Int Microbiol 16:145–155

    CAS  PubMed  Google Scholar 

  • Molina MC, Stocker-Wörgötter E, Türk R, Vicente C (1997) Axenic culture of the mycobiont of Xanthoria parietina in different nutritive media, effect of carbon source in spores germination. Endocytobiosis Cell Res 12:103–109

  • Muggia L, Kopun T, Grube M (2017) Effects of growth media on the diversity of culturable fungi from lichens. Molecules 22:824

    PubMed Central  Google Scholar 

  • Munsell AH (1912) A pigment color system and notation. Am J Psychol 23:236–244

    Google Scholar 

  • Myers OD, Sumner SJ, Li S, Barnes S, Du X (2017) One step forward for reducing false positive and false negative compound identifications from mass spectrometry metabolomics data: new algorithms for constructing extracted ion chromatograms and detecting chromatographic peaks. Anal Chem 89:8696–8703. https://doi.org/10.1021/acs.analchem.7b00947

    Article  CAS  PubMed  Google Scholar 

  • Oliver E, Crittenden PD, Beckett A, Brown DH (1989) Growth of lichen-forming fungi on membrane filters. Lichenologist 21:387–392

    Google Scholar 

  • Paukov A, Teptina A, Morozova M, Kruglova E, Favero-Longo SE, Bishop C, Rajakaruna N (2019) The effects of edaphic and climatic factors on secondary lichen chemistry: a case study using saxicolous lichens. Diversity 11:94

    CAS  Google Scholar 

  • Paukov AG, Teptina AY, Pushkarev EV (2015) Heavy metal uptake by chemically distinct lichens from Aspicilia spp. growing on ultramafic rocks. Aust J Bot 63:111–118

    CAS  Google Scholar 

  • Pykälä J (2019) Habitat loss and deterioration explain the disappearance of populations of threatened vascular plants, bryophytes and lichens in a hemiboreal landscape. Glob Ecol Conserv 18:e00610

    Google Scholar 

  • R Development Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Ranković B (2015) Lichen secondary metabolites bioactive properties and pharmaceutical potential. Springer International Publishing, Cham

  • Rafat A, Ridgway HJ, Cruickshank RH, Buckley HL, Rafat A, Ridgway HJ, Cruickshank RH, Buckley HL (2015) Isolation and co-culturing of symbionts in the genus Usnea. Symbiosis 66:123–132

    CAS  Google Scholar 

  • Rehman S, Andleeb S, Niazi AR, Ali S (2018) Estimation of trace elements and in vitro biological activities of lichens extracts. Pak J Pharm Sci 31:1407–1416

    CAS  PubMed  Google Scholar 

  • Rikkinen J (2013) Molecular studies on cyanobacterial diversity in lichen symbioses. MycoKeys 6:3–32

    Google Scholar 

  • Sahin E, Dabagoglu Psav S, Avan I, Candan M, Sahinturk V, Koparal AT (2019) Vulpinic acid, a lichen metabolite, emerges as a potential drug candidate in the therapy of oxidative stress–related diseases, such as atherosclerosis. Hum Exp Toxicol 38:675–684

    CAS  PubMed  Google Scholar 

  • Saidhareddy P, Ajay S, Shaw AK (2014) ‘Chiron’ approach to the total synthesis of macrolide (+)-aspicilin. RSC Adv 4:4253–4259

    CAS  Google Scholar 

  • Salgado F, Albornoz L, Cortéz C, Stashenko E, Urrea-Vallejo K, Nagles E, Galicia-Virviescas C, Cornejo A, Ardiles A, Simirgiotis M, García-Beltrán O, Areche C (2018) Secondary metabolite profiling of species of the genus Usnea by UHPLC-ESI-OT-MS-MS. Molecules 23:54

    CAS  Google Scholar 

  • Schaubach S, Michigami K, Fürstner A (2017) Hydroxyl-assisted trans-reduction of 1, 3-Enynes: application to the formal synthesis of (+)-Aspicilin. Synthesis 49:202–208

    CAS  Google Scholar 

  • Schmidt R, Ostermeier M, Schobert R (2017) Wittig cyclization of ω-hydroxy hemiacetals: synthesis of (+)-aspicilin. J Org Chem 82:9126–9132

    CAS  PubMed  Google Scholar 

  • Shaheen S, Iqbal Z, Hussain M (2019) First report of dye yielding potential and compounds of lichens; a cultural heritage of Himalayan communities, Pakistan. Pak J Bot 51:341–360

    CAS  Google Scholar 

  • Shanmugam K, Srinivasan M, Hariharan GN (2016) Developmental stages and secondary compound biosynthesis of mycobiont and whole thallus cultures of Buellia subsororioides. Mycol Prog 15:41

    Google Scholar 

  • Shukla P, Upreti DK (2015) Lichen dyes: current scenario and future prospects. In: Upreti DK, Divakar PK, Shukla V, Bajpai R (eds) Recent advances in lichenology. Springer, New Delhi, pp 209–229

    Google Scholar 

  • Shukla V, Joshi GP, Rawat MSM (2010) Lichens as a potential natural source of bioactive compounds: a review. Phytochem Rev 9:303–314

    CAS  Google Scholar 

  • Sieteiglesias V, González-Burgos E, Bermejo-Bescós P, Divakar PK, Gómez-Serranillos MP (2019) Lichens of parmelioid clade as promising multi-target neuroprotective agents. Chem Res Toxicol 32:1162–1177

    Google Scholar 

  • Solárová Z, Liskova A, Samec M, Kubatka P, Büsselberg D, Solár P (2020) Anticancer potential of lichens’ secondary metabolites. Biomolecules 10:87

    PubMed Central  Google Scholar 

  • 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 353:488–492

    CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava P, Upreti DK, Dhole TN, Srivastava AK, Nayak MT (2013) Antimicrobial property of extracts of Indian lichen against human pathogenic Bacteria. Interdiscip Perspect Infect Dis 2013:709348

    PubMed  PubMed Central  Google Scholar 

  • Stanojković T (2015) Investigations of lichen secondary metabolites with potential anticancer activity. In: Ranković B (ed) Lichen secondary metabolites: bioactive properties and pharmaceutical potential. Springer International Publishing, Cham, pp 127–146

  • Stocker-Wörgötter E (2008) Metabolic diversity of lichen-forming ascomycetous fungi: culturing, polyketide and shikimate metabolite production, and PKS genes. Nat Prod Rep 25:188–200

    PubMed  Google Scholar 

  • Stocker-Wörgötter E, Cordeiro LMC, Iacomini M (2013) Accumulation of potential pharmaceutically relevant lichen metabolites in lichens and cultured lichen symbionts Studies in Natural Products Chemistry 39:337–380

  • Studzińska-Sroka E, Piotrowska H, Kucińska M, Murias M, Bylka W (2016) Cytotoxic activity of physodic acid and acetone extract from Hypogymnia physodes against breast cancer cell lines. Pharm Biol 54:2480–2485

    PubMed  Google Scholar 

  • Thadhani VM, Karunaratne V (2017) Potential of lichen compounds as Antidiabetic agents with Antioxidative properties: a review. Oxidative Med Cell Longev 2017:1–10. https://doi.org/10.1155/2017/2079697

    Article  CAS  Google Scholar 

  • Thell A, Crespo A, Divakar PK, Kärnefelt I, Leavitt SD, Lumbsch HT, Seaward MR (2012) A review of the lichen family Parmeliaceae–history, phylogeny and current taxonomy. Nord J Bot 30:641–664

    Google Scholar 

  • Timsina BA, Sorensen JL, Weihrauch D, Piercey-Normore MD (2013) Effect of aposymbiotic conditions on colony growth and secondary metabolite production in the lichen-forming fungus Ramalina dilacerata. Fungal Biol 117:731–743

    CAS  PubMed  Google Scholar 

  • Upreti DK, Divakar PK, Nayaka S (2005) Commercial and ethnic use of lichens in India. Econ Bot 59:269–273

    Google Scholar 

  • Upreti DK, Joshi S, Nayaka S (2010) Chemistry of common dye yielding lichens of India. ENVIS Forestry Bulletin 10:122–133

    Google Scholar 

  • Valarmathi R, Hariharan GN, Venkataraman G, Parida A (2009) Characterization of a non-reducing polyketide synthase gene from lichen Dirinaria applanata. Phytochemistry 70:721–729

    CAS  PubMed  Google Scholar 

  • Williams DE, Loganzo F, Whitney L, Togias J, Harrison R, Singh MP, McDonald LA, Kathirgamanathar S, Karunaratne V, Andersen RJ, Andersen RJ (2011) Depsides isolated from the Sri Lankan lichen Parmotrema sp. exhibit selective Plk1 inhibitory activity. Pharm Biol 49:296–301

    CAS  PubMed  Google Scholar 

  • Xu M, Heidmarsson S, Olafsdottir ES, Buonfiglio R, Kogej T, Omarsdottir S (2016) Secondary metabolites from cetrarioid lichens: chemotaxonomy, biological activities and pharmaceutical potential. Phytomedicine 15:441–459

    Google Scholar 

  • Yahr R (Lichen Specialist Group) (2003) Cladonia perforata. The IUCN Red List of Threatened Species 2003: e.T43994A10838980

  • Yamamoto Y, Hara K, Kawakami H, Komine M (2015) Lichen substances and their biological activities. In: Upreti DK, Divakar PK, Rajesh VS, Bajpai R (eds.) Recent advances in lichenology. Modern methods and approaches in lichen systematics and culture techniques, Volume 2. Springer, New Delhi, pp 181–199

  • Yamamoto Y, Miura Y, Kinoshita Y, Higuchi M, Yamada Y, Murakami A, Ohigashi H, Koshimizu K (1995) Screening of tissue cultures and thalli of lichens and some of their active constituents for inhibition of tumor promoter-induced Epstein-Barr virus activation. Chem Pharm Bull 43:1388–1390

    CAS  Google Scholar 

  • Zambare VP, Christopher LP (2012) Biopharmaceutical potential of lichens. Pharm Biol 50:778–798

    PubMed  Google Scholar 

  • Zheng Z, Zhang S, Lu X, Ma Y, Fan Y, Shi Y, Dong A, Duan B (2012) Trivaric acid, a potent depside human leukocyte elastase inhibitor. Biol Pharm Bull:b12–b00642

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Acknowledgements

This publication is dedicated to our friend, colleague and mentor, Dr. Eva Barreno. We want to thank to Prof. M. Wedin for joining P. Divakar in field collection and Prof. D. González for statistical assistance. This study was supported by the Spanish Ministerio de Ciencia e Innovacion (CGL2013–42498-P, PID2019-105312GB-I00) and the Santander-Universidad Complutense de Madrid (PR75/18–21,605, PR 87/19–22,637 and G/6400100/3000).

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Authors and Affiliations

  1. Department of Biology, Geology, Physical and Inorganic Chemistry, Rey Juan Carlos University, 28933, Madrid, Spain

    E. M. Díaz, N. González-Benítez & M. C. Molina

  2. Department Pharmacology, Pharmacognosy and Botany, Complutense University of Madrid, 28040, Madrid, Spain

    J. C. Zamora, C. Ruibal, P. K. Divakar & A. Crespo

  3. University Rennes, CNRS, ISCR (Institut des Sciences Chimiques de Rennes) - UMR 6226, F-35000, Rennes, France

    F. Le Devehat, M. Chollet, S. Ferron, A. Sauvager & J. Boustie

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  1. E. M. Díaz
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  2. J. C. Zamora
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  3. C. Ruibal
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  4. P. K. Divakar
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  12. M. C. Molina
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Correspondence to M. C. Molina.

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Díaz, E.M., Zamora, J.C., Ruibal, C. et al. Axenic culture and biosynthesis of secondary compounds in lichen symbiotic fungi, the Parmeliaceae. Symbiosis 82, 79–93 (2020). https://doi.org/10.1007/s13199-020-00719-3

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