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Biological activities and chemical composition of Xanthoria lichens from Turkey

Year 2021, Volume 8, Issue 4, 376 - 388, 26.12.2021
https://doi.org/10.21448/ijsm.994427

Abstract

This study presents the biopharmaceutical potential and bioactive composition of Xanthoria lichens (X. candelaria, X. elegans, X. parietina) that wildly grown and traditionally utilized as medicine in North Eastern Anatolia, Turkey, which has specific microclimatic and ecological zones. Chromatographic findings revealed significant levels of parietin compound (35 to 49 mg/g extract), low levels of various fatty acids and a volatile compound; α-terpinene in the extracts. The extracts exhibited pronounced antioxidant potential through reducing and scavenging mechanisms; FCR: 33-38 mg gallic acid equivalent, FRAP: 511-815 µ mol Fe2+, ORAC: 1032-1355 µ mol Trolox equivalent per gram extract, respectively and DPPH: IC50: 1.1-2.7, ABTS: IC50: 2-2.3, CUPRAC: IC50: 0.7-1.2, phosphomolybdenum: IC50: 2-2.9, metal chelation: IC50: 1.3-2.3 mg extract/ml, respectively. Concerning enzyme inhibitory activities, the extracts effectively suppressed the activity of acetylcholinesterase (IC50: 0.5-0.75 mg/ml), butyrylcholinesterase (IC50: 0.7-1.1 mg/ml), tyrosinase (IC50: 0.6-0.7 mg/ml), amylase (IC50: 1.7-2 mg/ml), glucosidase (IC50: 0.6-3 mg/ml) and lipase (IC50: 55-79 µg/ml) enzymes. These findings showed that Xanthoria lichens are dominated by parietin as the major key compound and high-tolerated lichen taxa towards to different ecological and climatic conditions. These lichens might be promising sources of novel antioxidant and enzyme inhibitory activities such as Xanthoria candelaria as antioxidant and antilipase, Xanthoria elegans as anticholinesterase, and Xanthoria parietina as antiamylase and antiglucosidase.

References

  • Ainsworth, E.A., & Gillespie, K.M. (2007). Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nature Protocols, 2(4), 875-877.
  • Ali, S., & Hameed, H.N. (2019). Antibacterial and antioxidant activity of a chemically induced mutant of Xanthoria parietina. The Journal of Animal and Plant Sciences, 29(3), 881-888.
  • Atalay, F., Halici, M.B., Mavi, A., Çakır, A., Odabasioglu, F., Kazaz, C., Aslan, A., & Kufrevioglu, Ö.İ. (2011). Antioxidant phenolics from Lobaria pulmonaria L. Hoffm. and Usnea longissima Ach. lichen species. Turkish Journal Chemistry, 35, 647-661.
  • Basile, A., Rigano, D., Loppi, S., Santi, A.D., Nebbioso, A., Sorbo, S., Conte, B., Paoli, L., Ruberto, F.D., Molinari, A.M., Altucci, L., & Bontempo, P. (2015). Antiproliferative, antibacterial and antifungal activity of the lichen Xanthoria parietina and its secondary metabolite parietin. International Journal of Molecular Sciences, 16, 7861-7875.
  • Benzie, I.F.F., & Strain, J.J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay. Analytical Biochemistry, 239, 70-76.
  • Boustie, J., & Grube, M. (2005). Lichens—a promising source of bioactive secondary metabolites. Plant Genetic Resources, 3(2), 273–287.
  • Bown, D. (2001). Encyclopedia of Herbs and Their Uses, second ed. Dorling Kindersley.
  • Calcott, M.J., Ackerley, D.F., Knight, A., Keyzers, R.A., & Owen, J.G. (2018). Secondary metabolism in the lichen symbiosis. Chemical Society Reviews, 47(5), 1730-1760.
  • Chevallier, A. (1996). The Encyclopaedia of Medicinal Plants, first ed. Dorling Kindersley, London.
  • Copeland, R. A. (2000). Enzymes: A practical Introductions to Structure, Mechanism and Data Analysis, 2nd ed. Wiley.
  • Cornejo, A., Salgado, F., Caballero, J., Vargas, R., Simirgiotis, M., & Areche, C. (2016). Secondary metabolites in Ramalina terebrata detected by UHPLC/ESI/MS/MS and identification of parietin as tau protein inhibitor. International Journal of Molecular Sciences, 17(8), 1303.
  • Dalar, A., & Konczak, I. (2013). Phenolic contents, antioxidant capacities and inhibitory activities against key metabolic syndrome relevant enzymes of herbal teas from Eastern Anatolia. Industrial Crops and Products, 44, 383-390.
  • Fernandez-Moriano C., Gomez-Serranillos M.P., & Crespo, A. (2016). Antioxidant potential of lichen species and their secondary metabolites. A systematic review. Pharmaceutical Biology, 54(1), 1-17.
  • Gonçalves, S., & Romano, A. (2017). Inhibitory properties of phenolic compounds against enzymes linked with human diseases in: Soto-Hernandez, M., Palma-Tenango, M., Garcia-Mateos, M.R. (Eds.), Phenolic Compounds - Biological Activity. IntechOpen, Ltd., London, pp. 99-118.
  • Gundogdu, G., Gundogdu, K., Nalci, K.A., Demirkaya, A.K., Tascı, S.Y., Miloglu, F.D., Senol, O., & Hacimuftuoglu, A. (2019). The effect of parietin isolated from Rheum ribes L. on in vitro wound model using human dermal fibroblast cells. The International Journal of Lower Extremity Wounds, 18(1), 56-64.
  • Hawksworth, D.L. (2003). Hallucinogenic and toxic lichens. International Lichenological Newsletter, 36, 33–35.
  • Ingólfsdóttir, K. (2002). Usnic acid. Phytochemistry, 61, 729–736.
  • Karthikaidevi, G., Thirumaran, G., Manivannan, K., Anantharaman, P., Kathiresan, K., & Balasubaramanian, T. (2011). Antimicrobial activities of the lichen Roccella belangeriana (Awasthi) from mangroves of Gulf of Mannar. Indian Journal of Geo-Marine Sciences, 40(3), 449-453.
  • Kekuda, T. P., Lavanya, D., & Pooja, R. (2019). Lichens as promising resources of enzyme inhibitors: A review. Journal of Drug Delivery and Therapeutics, 9(2), 665-676.
  • Kumar, J., Dhar, P., Tayade, A.B., Gupta, D., Chaurasia, O.P., Upreti, D.K., Arora, R., & Srivastava, R.B. (2014). Antioxidant capacities, phenolic profile and cytotoxic effects of Saxicolous lichens from Trans-Himalayan cold desert of Ladakh. Plos One, 9(6), e98696.
  • Lina, A., Ghassan, K., Mohammed, W., & Ahmed, E. (2015). Efficacy of extracts of some lichens for potential antibacterial activity. Research Journal of Pharmaceutical, Biological and Chemical Sciences, 6(1), 318-331.
  • Lopez-Tobar, E., Verebova, V., Blascakova, L., Jancura, D., Fabriciova, G., Sanchez-& Cortes, S. (2016). Detection and aggregation of the antitumoral drug parietin in ethanol/water mixture and on plasmonic metal nanoparticles studied by surface-enhanced optical spectroscopy: Effect of pH and ethanol concentration. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, 159, 134-140.
  • Manojlovic, N.T., Vasiljevic, P.J., Maskovic, P.Z., Juskovic, M., & Bogdanovic-Dusanovic, G. (2012). Chemical composition, antioxidant, and antimicrobial activities of lichen Umbilicaria cylindrica (L.) Delise (Umbilicariaceae). Evidence-Based Complementary and Alternative Medicine, 452431.
  • Moldovan, L., Moldovan, N.I., 2004. Oxygen free radicals and redox biology of organelles. Histochemistry and Cell Biology, 122, 395–412.
  • Nybakken, L., Solhaug, K.A., Bilger, W., & Gauslaa, Y. (2004). The lichens Xantoria elegans and Cetraria islandica maintain a high protection against UV-B radiation in arctic habitats. Oecologia, 140, 211–216.
  • Piervittori, R., Alessio, F., & Maffei, M. (1994). Fatty acid variations in the lichen, Xanthoria parietina. Phytochemistry, 36(4), 853-856.
  • Pirie, A., Parsons, D., Renggli, J., Narkowicz, C., Jacobson, G.A., & Shabala, S. (2013). Modulation of flavonoid and tannin production of Carpobrotus rossi by environmental conditions. Environmental and Experimental Botany, 87, 19-31.
  • Prior, R.L. (2015). Oxygen radical absorbance capacity (ORAC): New horizons in relating dietary antioxidants/bioactives and health benefits. Journal of Functional Foods, 18, 797-810.
  • Raj, P.S., Prathapan, A., Sebastian, J., Antony, A.K., Riya, M.P., Rani, M.R.P., Biju, H., Priya, S., & Raghu, K.G. (2014). Parmotrema tinctorum exhibits antioxidant, antiglycation and inhibitory activities against aldose reductase and carbohydrate digestive enzymes: an in vitro study. Natural Product Research, 28(18), 1480–1484.
  • Reddy, V.M., O’Sullivan, J.F., & Gangadharam, PR. (1999). Antimycobacterial activities of riminophenazines. Journal of Antimicrobial Chemotherapy, 43, 615–623.
  • Torres, A., Dor, I., Rotem, J., Srebnik, M., & Dembitsky, V.M. (2003). Characterization of surface n‐alkanes and fatty acids of the epiphytic lichen Xanthoria parietina, its photobiont a green alga Trebouxia sp., and its mycobiont, from the Jerusalem hills. European Journal of Biochemistry, 270(10), 2120-2125.
  • Shivanna, R., Hengameh, P., & Rajkumar, H.G. (2015). Screening of lichen extracts for in-vitro antidiabetic activity using alpha-amylase inhibitory assay. International Journal of Biological & Pharmaceutical Research, 6(5), 364–367.
  • Uysal, S., Zengin, G., Locatelli, M., Bahadori, M.B., Mocan, A., Bellagamba, G., & Aktumsek, A. (2017). Cytotoxic and enzyme inhibitory potential of two Potentilla species (P. speciosa L. and P. reptans Willd.) and their chemical composition. Frontiers in Pharmacology, 23(8), 290.
  • Uzun, Y., Dalar, A., & Konczak, I. (2017). Sempervivum davisii: phytochemical composition, antioxidant and lipase-inhibitory activities. Pharmaceutical Biology, 55, 532-540.
  • Valadbeigi, T., & Shaddel, M. (2016). Amylase inhibitory activity of some macro lichens in Mazandaran province, Iran. Physiology and Pharmacology, 20, 215–219.
  • Zambare, V.P., & Christopher, L.P. (2012). Biopharmaceutical potential of lichens. Pharmaceutical Biology, 50(6), 778-798.
  • Zengin, G. (2016). A study on in vitro enzyme inhibitory properties of Asphodeline anatolica: new sources of natural inhibitors for public health problems. Industrial Crops and Products, 83, 39-43.

Biological activities and chemical composition of Xanthoria lichens from Turkey

Year 2021, Volume 8, Issue 4, 376 - 388, 26.12.2021
https://doi.org/10.21448/ijsm.994427

Abstract

This study presents the biopharmaceutical potential and bioactive composition of Xanthoria lichens (X. candelaria, X. elegans, X. parietina) that wildly grown and traditionally utilized as medicine in North Eastern Anatolia, Turkey, which has specific microclimatic and ecological zones. Chromatographic findings revealed significant levels of parietin compound (35 to 49 mg/g extract), low levels of various fatty acids and a volatile compound; α-terpinene in the extracts. The extracts exhibited pronounced antioxidant potential through reducing and scavenging mechanisms; FCR: 33-38 mg gallic acid equivalent, FRAP: 511-815 µ mol Fe2+, ORAC: 1032-1355 µ mol Trolox equivalent per gram extract, respectively and DPPH: IC50: 1.1-2.7, ABTS: IC50: 2-2.3, CUPRAC: IC50: 0.7-1.2, phosphomolybdenum: IC50: 2-2.9, metal chelation: IC50: 1.3-2.3 mg extract/ml, respectively. Concerning enzyme inhibitory activities, the extracts effectively suppressed the activity of acetylcholinesterase (IC50: 0.5-0.75 mg/ml), butyrylcholinesterase (IC50: 0.7-1.1 mg/ml), tyrosinase (IC50: 0.6-0.7 mg/ml), amylase (IC50: 1.7-2 mg/ml), glucosidase (IC50: 0.6-3 mg/ml) and lipase (IC50: 55-79 µg/ml) enzymes. These findings showed that Xanthoria lichens are dominated by parietin as the major key compound and high-tolerated lichen taxa towards to different ecological and climatic conditions. These lichens might be promising sources of novel antioxidant and enzyme inhibitory activities such as Xanthoria candelaria as antioxidant and antilipase, Xanthoria elegans as anticholinesterase, and Xanthoria parietina as antiamylase and antiglucosidase.

References

  • Ainsworth, E.A., & Gillespie, K.M. (2007). Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nature Protocols, 2(4), 875-877.
  • Ali, S., & Hameed, H.N. (2019). Antibacterial and antioxidant activity of a chemically induced mutant of Xanthoria parietina. The Journal of Animal and Plant Sciences, 29(3), 881-888.
  • Atalay, F., Halici, M.B., Mavi, A., Çakır, A., Odabasioglu, F., Kazaz, C., Aslan, A., & Kufrevioglu, Ö.İ. (2011). Antioxidant phenolics from Lobaria pulmonaria L. Hoffm. and Usnea longissima Ach. lichen species. Turkish Journal Chemistry, 35, 647-661.
  • Basile, A., Rigano, D., Loppi, S., Santi, A.D., Nebbioso, A., Sorbo, S., Conte, B., Paoli, L., Ruberto, F.D., Molinari, A.M., Altucci, L., & Bontempo, P. (2015). Antiproliferative, antibacterial and antifungal activity of the lichen Xanthoria parietina and its secondary metabolite parietin. International Journal of Molecular Sciences, 16, 7861-7875.
  • Benzie, I.F.F., & Strain, J.J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of "antioxidant power": the FRAP assay. Analytical Biochemistry, 239, 70-76.
  • Boustie, J., & Grube, M. (2005). Lichens—a promising source of bioactive secondary metabolites. Plant Genetic Resources, 3(2), 273–287.
  • Bown, D. (2001). Encyclopedia of Herbs and Their Uses, second ed. Dorling Kindersley.
  • Calcott, M.J., Ackerley, D.F., Knight, A., Keyzers, R.A., & Owen, J.G. (2018). Secondary metabolism in the lichen symbiosis. Chemical Society Reviews, 47(5), 1730-1760.
  • Chevallier, A. (1996). The Encyclopaedia of Medicinal Plants, first ed. Dorling Kindersley, London.
  • Copeland, R. A. (2000). Enzymes: A practical Introductions to Structure, Mechanism and Data Analysis, 2nd ed. Wiley.
  • Cornejo, A., Salgado, F., Caballero, J., Vargas, R., Simirgiotis, M., & Areche, C. (2016). Secondary metabolites in Ramalina terebrata detected by UHPLC/ESI/MS/MS and identification of parietin as tau protein inhibitor. International Journal of Molecular Sciences, 17(8), 1303.
  • Dalar, A., & Konczak, I. (2013). Phenolic contents, antioxidant capacities and inhibitory activities against key metabolic syndrome relevant enzymes of herbal teas from Eastern Anatolia. Industrial Crops and Products, 44, 383-390.
  • Fernandez-Moriano C., Gomez-Serranillos M.P., & Crespo, A. (2016). Antioxidant potential of lichen species and their secondary metabolites. A systematic review. Pharmaceutical Biology, 54(1), 1-17.
  • Gonçalves, S., & Romano, A. (2017). Inhibitory properties of phenolic compounds against enzymes linked with human diseases in: Soto-Hernandez, M., Palma-Tenango, M., Garcia-Mateos, M.R. (Eds.), Phenolic Compounds - Biological Activity. IntechOpen, Ltd., London, pp. 99-118.
  • Gundogdu, G., Gundogdu, K., Nalci, K.A., Demirkaya, A.K., Tascı, S.Y., Miloglu, F.D., Senol, O., & Hacimuftuoglu, A. (2019). The effect of parietin isolated from Rheum ribes L. on in vitro wound model using human dermal fibroblast cells. The International Journal of Lower Extremity Wounds, 18(1), 56-64.
  • Hawksworth, D.L. (2003). Hallucinogenic and toxic lichens. International Lichenological Newsletter, 36, 33–35.
  • Ingólfsdóttir, K. (2002). Usnic acid. Phytochemistry, 61, 729–736.
  • Karthikaidevi, G., Thirumaran, G., Manivannan, K., Anantharaman, P., Kathiresan, K., & Balasubaramanian, T. (2011). Antimicrobial activities of the lichen Roccella belangeriana (Awasthi) from mangroves of Gulf of Mannar. Indian Journal of Geo-Marine Sciences, 40(3), 449-453.
  • Kekuda, T. P., Lavanya, D., & Pooja, R. (2019). Lichens as promising resources of enzyme inhibitors: A review. Journal of Drug Delivery and Therapeutics, 9(2), 665-676.
  • Kumar, J., Dhar, P., Tayade, A.B., Gupta, D., Chaurasia, O.P., Upreti, D.K., Arora, R., & Srivastava, R.B. (2014). Antioxidant capacities, phenolic profile and cytotoxic effects of Saxicolous lichens from Trans-Himalayan cold desert of Ladakh. Plos One, 9(6), e98696.
  • Lina, A., Ghassan, K., Mohammed, W., & Ahmed, E. (2015). Efficacy of extracts of some lichens for potential antibacterial activity. Research Journal of Pharmaceutical, Biological and Chemical Sciences, 6(1), 318-331.
  • Lopez-Tobar, E., Verebova, V., Blascakova, L., Jancura, D., Fabriciova, G., Sanchez-& Cortes, S. (2016). Detection and aggregation of the antitumoral drug parietin in ethanol/water mixture and on plasmonic metal nanoparticles studied by surface-enhanced optical spectroscopy: Effect of pH and ethanol concentration. Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, 159, 134-140.
  • Manojlovic, N.T., Vasiljevic, P.J., Maskovic, P.Z., Juskovic, M., & Bogdanovic-Dusanovic, G. (2012). Chemical composition, antioxidant, and antimicrobial activities of lichen Umbilicaria cylindrica (L.) Delise (Umbilicariaceae). Evidence-Based Complementary and Alternative Medicine, 452431.
  • Moldovan, L., Moldovan, N.I., 2004. Oxygen free radicals and redox biology of organelles. Histochemistry and Cell Biology, 122, 395–412.
  • Nybakken, L., Solhaug, K.A., Bilger, W., & Gauslaa, Y. (2004). The lichens Xantoria elegans and Cetraria islandica maintain a high protection against UV-B radiation in arctic habitats. Oecologia, 140, 211–216.
  • Piervittori, R., Alessio, F., & Maffei, M. (1994). Fatty acid variations in the lichen, Xanthoria parietina. Phytochemistry, 36(4), 853-856.
  • Pirie, A., Parsons, D., Renggli, J., Narkowicz, C., Jacobson, G.A., & Shabala, S. (2013). Modulation of flavonoid and tannin production of Carpobrotus rossi by environmental conditions. Environmental and Experimental Botany, 87, 19-31.
  • Prior, R.L. (2015). Oxygen radical absorbance capacity (ORAC): New horizons in relating dietary antioxidants/bioactives and health benefits. Journal of Functional Foods, 18, 797-810.
  • Raj, P.S., Prathapan, A., Sebastian, J., Antony, A.K., Riya, M.P., Rani, M.R.P., Biju, H., Priya, S., & Raghu, K.G. (2014). Parmotrema tinctorum exhibits antioxidant, antiglycation and inhibitory activities against aldose reductase and carbohydrate digestive enzymes: an in vitro study. Natural Product Research, 28(18), 1480–1484.
  • Reddy, V.M., O’Sullivan, J.F., & Gangadharam, PR. (1999). Antimycobacterial activities of riminophenazines. Journal of Antimicrobial Chemotherapy, 43, 615–623.
  • Torres, A., Dor, I., Rotem, J., Srebnik, M., & Dembitsky, V.M. (2003). Characterization of surface n‐alkanes and fatty acids of the epiphytic lichen Xanthoria parietina, its photobiont a green alga Trebouxia sp., and its mycobiont, from the Jerusalem hills. European Journal of Biochemistry, 270(10), 2120-2125.
  • Shivanna, R., Hengameh, P., & Rajkumar, H.G. (2015). Screening of lichen extracts for in-vitro antidiabetic activity using alpha-amylase inhibitory assay. International Journal of Biological & Pharmaceutical Research, 6(5), 364–367.
  • Uysal, S., Zengin, G., Locatelli, M., Bahadori, M.B., Mocan, A., Bellagamba, G., & Aktumsek, A. (2017). Cytotoxic and enzyme inhibitory potential of two Potentilla species (P. speciosa L. and P. reptans Willd.) and their chemical composition. Frontiers in Pharmacology, 23(8), 290.
  • Uzun, Y., Dalar, A., & Konczak, I. (2017). Sempervivum davisii: phytochemical composition, antioxidant and lipase-inhibitory activities. Pharmaceutical Biology, 55, 532-540.
  • Valadbeigi, T., & Shaddel, M. (2016). Amylase inhibitory activity of some macro lichens in Mazandaran province, Iran. Physiology and Pharmacology, 20, 215–219.
  • Zambare, V.P., & Christopher, L.P. (2012). Biopharmaceutical potential of lichens. Pharmaceutical Biology, 50(6), 778-798.
  • Zengin, G. (2016). A study on in vitro enzyme inhibitory properties of Asphodeline anatolica: new sources of natural inhibitors for public health problems. Industrial Crops and Products, 83, 39-43.

Details

Primary Language English
Subjects Pharmacology and Pharmacy
Published Date December
Journal Section Articles
Authors

Muzaffer MÜKEMRE
HAKKARI UNIVERSITY, YÜKSEKOVA VOCATIONAL SCHOOL
0000-0001-6154-6603
Türkiye


Gokhan ZENGİN
SELCUK UNIVERSITY, FACULTY OF SCIENCE
0000-0002-8901-6484
Türkiye


Rabia Sena TÜRKER
VAN YUZUNCU YIL UNIVERSITY, FACULTY OF PHARMACY, PHARMACY PR.
0000-0002-2017-7159
Türkiye


Ali ASLAN
VAN YUZUNCU YIL UNIVERSITY, FACULTY OF PHARMACY, PHARMACY PR.
0000-0002-5122-6646
Türkiye


Abdullah DALAR (Primary Author)
VAN YUZUNCU YIL UNIVERSITY, FACULTY OF PHARMACY
0000-0002-0080-2519
Türkiye

Publication Date December 26, 2021
Published in Issue Year 2021, Volume 8, Issue 4

Cite

APA Mükemre, M. , Zengin, G. , Türker, R. S. , Aslan, A. & Dalar, A. (2021). Biological activities and chemical composition of Xanthoria lichens from Turkey . International Journal of Secondary Metabolite , 8 (4) , 376-388 . DOI: 10.21448/ijsm.994427

International Journal of Secondary Metabolite (IJSM)

ISSN-e: 2148-6905