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Comparison of the Phytotoxic Effects of Usnic Acid on Cultures of Free-Living Alga Scenedesmus quadricauda and Aposymbiotically Grown Lichen Photobiont Trebouxia erici

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Abstract

The phytotoxic effects of the lichen secondary metabolite—usnic acid on cultures of free living alga—Scenedesmus quadricauda (UTEX 76) and aposymbiotically grown lichen photobiont Trebouxia erici (UTEX 911) were assessed. We found a relatively strong inhibition effect of usnic acid on the growth of alga Scenedesmus, accompanied by an increase of cell size, an alteration of assimilation pigment composition, followed by strong degradation of chlorophyll a, a decrease of chlorophyll a fluorescence, and an increase of reactive oxygen species in the cells. The content of soluble proteins remained a stable parameter. Phytotoxicity of usnic acid on cultures of Trebouxia photobiont was significantly lower. Usnic acid in lichens may act as an allochemical that controls the division of photobiont cells, thereby regulating the balance between the photobiont and mycobiont forming thallus. Higher tolerance to usnic acid in Trebouxia cultures may be an adaptation resulting from the long term co-evolution of these algae with fungi that produce secondary metabolites.

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References

  • Ahmadjian, V. 1993. The Lichen Symbiosis. Wiley, New York.

    Google Scholar 

  • Al-Bekairi, A. M., Qureshi, S., Chaudhry, M. A., Krishna, D. R., and Shah, A. H. 1991. Mitodepressive, clastogenic and biochemical effects of (+)-usnic acid in mice. J. Ethnopharmacol. 33:217–220.

    Article  CAS  PubMed  Google Scholar 

  • Bačkor, M. and Fahselt, D. 2008. Lichen photobionts and metal toxicity. Symbiosis 46:1–10.

    Google Scholar 

  • Bačkor, M. and Loppi, S. 2009. Interactions of lichens with heavy metals. Biol. Plantarum 53:214–222.

    Article  Google Scholar 

  • Bačkor, M., Hudák, J., Repčák, M., Ziegler, W., and Bačkorová, M. 1998. The influence of pH and lichen metabolites (vulpinic acid and (+) usnic acid) on the growth of lichen photobiont Trebouxia irregularis. Lichenologist 30:577–582.

    Google Scholar 

  • Bačkor, M., Fahselt, D., Davidson, R., and Wu, C. T. 2003. Effects of copper on wild and tolerant strains of the lichen photobiont Trebouxia erici (Chlorophyta) and possible tolerance mechanisms. Arch. Environ. Con. Tox. 45:159–167.

    Article  Google Scholar 

  • Bačkor, M., Fahselt, D., and Wu, C. T. 2004. Free proline content is positively correlated with copper tolerance of the lichen photobiont Trebouxia erici (Chlorophyta). Plant Sci. 167:151–157.

    Article  Google Scholar 

  • Bačkor, M., Váczi, P., Barták, M., Buďová, J., and Dzubaj, A. 2007. Uptake, photosynthetic characteristics and membrane lipid peroxidation levels in the lichen photobiont Trebouxia erici exposed to copper and cadmium. Bryologist 110: 100–107.

    Article  Google Scholar 

  • Barnes, J. D., Balaguer, L., Manrique, E., Elvira, S., and Davison, A. W. 1992. A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environ. Exp. Bot. 32:85–100.

    Article  CAS  Google Scholar 

  • Bradford, M. M. 1976. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248–254.

    Article  CAS  PubMed  Google Scholar 

  • Buďová, J., Bačkor, M., Bačkorová, M., and Židzik, J. 2006. Usnic acid and copper toxicity in aposymbiotically grown lichen photobiont Trebouxia erici. Symbiosis 42:169–174.

    Google Scholar 

  • Cardarelli, M., Serino, G., Campanella, L., Ercole, P., de Cicco Nardone, F., Alesiani, O., and Rossiello, F. 1997. Antimitotic effects of usnic acid on different biological systems. CMLS 53:667–672.

    Article  CAS  PubMed  Google Scholar 

  • Caviglia, A. M., Nicora, P., Giordani, P., Brunialti, G., and Modenesi, P. 2001. Oxidative stress and usnic acid content in Parmelia caperata and Parmelia soredians (Lichenes). Farmaco 56:379–382.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Elstner, E. F. and Heupel, A. 1976. Inhibition of nitrite formation from hydroxylammonium chloride: A simple assay for superoxide dismutase. Anal. Biochem. 70:616–620.

    Article  CAS  PubMed  Google Scholar 

  • Endo, T., Takahagi, T., Kinoshita, Y., Yamamoto, Y., and Sato, F. 1998. Inhibition of photosystem II of spinach by lichen-derived depsides. Biosci. Biotechnol. Biochem. 62:2023–2027.

    Article  CAS  Google Scholar 

  • Fahselt, D. 1994. Secondary biochemistry of lichens. Symbiosis 16:117–165.

    CAS  Google Scholar 

  • Fahselt, D. 2008. Individuals and populations of lichens, pp. 252–273, in T. H. Nash (ed.). Lichen Biology, 2nd edition, Cambridge University Press, Cambridge.

    Google Scholar 

  • Han, D., Matsumaru, K., Rettori, D., and Kaplowitz, N. 2004. Usnic acid-induced necrosis of cultured mouse hepatocytes: inhibition of mitochondrial function and oxidative stress. Biochem. Pharmacol. 67: 439–451.

    Article  CAS  PubMed  Google Scholar 

  • Hauck, M., Willenbruch, K., and Leuschner, C. 2009. Lichen substances prevent lichens from nutrient deficiency. J. Chem. Ecol. 35:71–73.

    Article  CAS  PubMed  Google Scholar 

  • Hendry, G.A.F., Houghton, J.D., and Brown, S.B. 1987. The degradation of chlorophyll—a biological enigma. Tansley Review No. 11. New Phytol. 107: 255–302.

    Article  CAS  Google Scholar 

  • Kováčik, J. and Bačkor, M. 2007. Changes of phenolic metabolism and oxidative status in nitrogen-deficient Matricaria chamomilla plants. Plant Soil 297:255–265.

    Article  Google Scholar 

  • Latkowska, E., Lechowski, Z., Bialczyk, J., and Pilarski, J. 2006. Photosynthesis and water relations in tomato plants cultivated long-term in media containing (+)-usnic acid. J. Chem. Ecol. 32:2053–2066.

    Article  CAS  PubMed  Google Scholar 

  • Lawrey, J. D. 1986. Biological role of lichen substances. Bryologist 89:111–122.

    Article  CAS  Google Scholar 

  • Lechowski, Z., Mej, E., and Bialczyk, J. 2006. Accumulation of biomass and some macroelements in tomato plants grown in media with (+)-usnic acid. Environ. Exp. Bot. 56:239–244.

    Article  CAS  Google Scholar 

  • Pöykkö, H., Hyvärinen, M., and Bačkor, M. 2005. Removal of lichen secondary metabolites affects food choice and survival of lichenivorous moth larvae. Ecology 86:2623–2632.

    Article  Google Scholar 

  • Ronen, R. and Galun, M. 1984. Pigment extraction from lichens with dimethyl sulfoxide (DMSO) and estimation of chlorophyll degradation. Environ. Exp. Bot. 24:239–245.

    Article  CAS  Google Scholar 

  • Sarret, G., Manceau, A., Cuny, D., van Haluwyn, C., Déruelle, S., Hazemann, J. L., Soldo, Y., Eybert-Bérard, L., and Menthonnex, J. J. 1998. Mechanisms of lichen resistance to metallic pollution. Environ. Sci. Technol. 32: 3325–3330.

    Article  CAS  Google Scholar 

  • Solhaug, K. A., Lind, M., Nybakken, L., and Gauslaa, Y. 2009. Possible functional roles of cortical depsides and medullary depsidones in the foliose lichen Hypogymnia physodes. Flora 204:40–48.

    Google Scholar 

  • Takahagi, T., Endo, T., Yamamoto, Y., and Sato, F. 2008. Lichen photobionts show tolerance against lichen acids produced by lichen mycobionts. Biosci. Biotech. Bioch. 72:3122–3127.

    Article  CAS  Google Scholar 

  • Wellburn, A. R. 1994. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolutions. J. Plant Physiol. 144:307–313.

    CAS  Google Scholar 

  • Yuan, X., Xiao, S. and Taylor, T. N. 2005. Lichen-like symbiosis 600 million years ago. Science 308:1017–1020.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was financially supported by Slovak Grant Agency (VEGA 1/4337/07), Slovak Research and Development Agency (APVV SK-BG-0013-08) and from National Found Research; Ministry of Education, Youth and Science—Bulgaria (D002-38/09). The authors thank Kenneth Dvorsky (Ontario, Canada) for comments on the manuscript.

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Correspondence to Martin Bačkor.

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Bačkor, M., Klemová, K., Bačkorová, M. et al. Comparison of the Phytotoxic Effects of Usnic Acid on Cultures of Free-Living Alga Scenedesmus quadricauda and Aposymbiotically Grown Lichen Photobiont Trebouxia erici . J Chem Ecol 36, 405–411 (2010). https://doi.org/10.1007/s10886-010-9776-4

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