Abstract
The influence of (+)-usnic acid on rates of gas exchange (photosynthesis, respiration, and transpiration) in long-term cultivation of tomato plants was studied. The effect was dose-dependent. Plants grown in media containing the maximum concentration of (+)-usnic acid (30 μM) had photosynthetic and respiration rates reduced by 41% and 80%, respectively. The effect on photosynthesis rate may be the result of a multidirectional effect at various stages of this process, which at the highest usnic acid concentration underwent reduction: content of chlorophylls by 30%, carotenoids by 35%, and Hill reaction activity by 75%. Usnic acid also raises the susceptibility of chlorophyll to photodegradation. Under some conditions, transpiration was reduced by 2.1-fold in light and 3.7-fold in dark. This result was correlated with (1) an increase in the diffusive resistance of the stomata (3.1-fold in upper and 1.5-fold in lower surface of leaf), (2) a reduction of stomata density (by 60% on upper and 40% on lower surface), and (3) a 12.3-fold decrease in root hydraulic conductance.
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Abo-Khatwa, A. N., Al.-Robai, A. A., and Al.-Jawhari, D. A. 1996. Lichen acids as uncouplers of oxidative phosphorylation of mouse-liver mitochondria. Nat. Toxins 4:96–102.
Ascaso, C., Gonzales, C., and Vicente, C. 1980. Epiphytic Evernia prunastri (L.) Ach.: Ultrastructural facts. Cryptogam., Bryol., Lichenol. 1:43–51.
BaČkor, M., Gaburjákowá, J., Hudák, J., and Ziegler, W. 1997. The biological role of secondary metabolites from lichen. I. The influence of usnic acid on biomolecular lipid membranes. Physiol. Plant. 29:67–71.
BaČkor, M., Hudák, J., Repcák, M., Ziegler, W., and Backorová, M. 1998. The influence of pH and lichen metabolites (vulpinic acid and (+)-usnic acid) on the growth of the lichen photobiont Trebouxia irregularis. Lichenologist 30:577–582.
Begora, M. D. and Fahselt, D. 2001. Usnic acid and atranorin concentrations in lichens in relation to bands of UV irradiance. Bryologist 104:134–140.
Bialczyk, J., Lechowski, Z., and Libik, A. 1994. Growth of tomato seedlings under different HCO3 − concentration in the media. J. Plant Nutr. 17:801–816.
Bjerke, J. W. and Dahl, T. 2002. Distribution patterns of usnic acid-producing lichens along local radiation gradients in West Greenland. Nova Hedwig. 75:487–506.
Bjerke, J. W., Lerfall, K., and Elvebakk, A. 2002. Effects of ultraviolet radiation and PAR on the content of usnic and divaricatic acids in two arctic-alpina lichens. Photochem. Photobiol. Sci. 1:678–685.
Carbonnier, J. 1986. Recherche d'une technique d'utilisation de l'acide usnique comme antitranspirant appliqué à des vivriéres, pp. 147–171, in J. Carbonnier and D. Laffray (eds.). Recherches et Applications Dans le Domaine des Antitranspirants Stomatiques. Agence de Coopération Culturelle et Technique, Paris.
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. Cell. Mol. Life Sci. 53:667–672.
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.
Cocchietto, M., Skert, N., and Nimis, P. L. 2002. A review on usnic acid, and interesting natural compound. Naturwissenschaften 89:137–146.
Dawson, H. J., Hrutfiord, B. F., and Ugolini, F. C. 1984. Mobility of lichen compounds from Cladonia mitis in arctic soils. Soil Sci. 138:40–45.
Endo, Y., Hayashi, H., Sato, T., Maruno, M., Ohta, T., and Nozoe, S. 1994. Confluentic acid and 2-O-methylperlatolic acid, monoamine oxidase B inhibitors in a Brazilian plant, Himatanthus sucuuba. Chem. Pharm. Bull. 42:1198–1201.
Fiscus, E. L. 1975. The interaction between osmotic- and pressure-induced water flow in plant roots. Plant Physiol. 55:917–922.
Gardner, C. R. and Müller, D. M. J. 1981. Factors affecting the toxicity of several lichen acids: Effects of pH and lichen acids concentration. Am. J. Bot. 68:87–95.
Ghione, M., Parrello, D., and Grasso, L. 1988. Usnic acid revisited, its activity on oral flora. Chemioterapia 7:302–305.
Huneck, S. and Yoshimura, Y. 1996. Identification of Lichen Substances. Springer, Berlin.
Ingólfsdóttir, K. 2002. Usnic acid. Phytochemistry 61:729–736.
Inoué, H., Noguchi, M., and Kubo, K. 1987. Site of inhibition of usnic acid at oxidizing side of photosystem 2 of spinach chloroplasts. Photosynthetica 21:88–90.
Kinoshita, Y., Yamamoto, Y., Yoshimura, I., Kurokawa, T., and Huneck, S. 1997. Distribution of optical isomers of usnic and isousnic acids analyzed by high performance liquid chromatography. J. Hatt. Bot. Lab. 83:173–178.
Lascève, G. and Gaugain, F. 1990. Effects of usnic acid on sunflower and maize plantlets. J. Plant Physiol. 136:723–727.
Lauterwein, M., Oethinger, M., Belsner, K., Peters, T., and Marre, R. 1995. In vitro activities of the lichen secondary metabolities vulpinic acid, (+)-usnic acid, and (−)-usnic acid against aerobic and anaerobic microorganisms. Antimicrob. Agents Chemother. 39:2541–2543.
Lechowski, Z. and Bialczyk, J. 1990. Photodestruction of chlorophyll in Zea mays L. leaves under different CO2 concentration. Biol. Plant. 33:345–353.
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.
Müller, P., Li, X. P., and Niyogi, K. K. 2001. Non-photochemical quenching: A response to excess light energy. Plant Physiol. 125:1558–1566.
Orús, M. I., Estévez, M. P., and Vicente, P. 1981. Manganese depletion in chloroplasts of Quercus rotundifolia during chemical simulation of lichen epiphytic states. Physiol. Plant. 52:263–266.
Osmond, C. B. 1994. What is photoinhibition ? Some insights from comparison of shade and sun plants. pp. 1–24, in N. N. Baker and J. R. Boweyer (eds.). Photoinhibition of Photosynthesis: From Molecular Mechanisms to the Field. BIOS Scientific, Oxford.
Proksa, B., Sturdíková, M., Prónayová, M., and Liptaj, T. 1996. (−)-Usnic acid and its derivatives. Their inhibition of fungal growth and enzyme activity. Pharmazie 51:195–196.
Rawson, H. M., Begg, J. E., and Woodward, R. G. 1977. The effect of atmospheric humidity on photosynthesis, transpiration and water use efficiency of leaves of several plant species. Planta 134:5–10.
Romagni, J. G., Meazza, G., Dhammika, N. P., Nanayakkara, D., and Dayan, F. E. 2000. The phytotoxic lichen metabolite, usnic acid, is a potent inhibitor of plant p-hydroxyphenylpyruvate dioxygenase. FEBS Lett. 480:301–305.
Romagni, J. G., Rosell, R. C., Nanayakkara, N. P. D., and Dayan, F. E. 2004. Ecophysiology and potential modes of action for selected lichen secondary metabolites, pp. 13–30, in F. A. Macías, J. C. G. Galindo, J. M. G. Molinillo, and H. G. Cutler (eds.). Allelopathy. CRC Press, Boca Raton, FL.
Shibamoto, T. and Wei, C. 1984. Mutagenicity of lichen constituents. Environ. Mutagen. 6:757–762.
Synková, H., Wilhelmová, N., Holá, D., Haisel, D., and Šesták, Z. 1997. Comparison of chlorophyll fluorescence kinetics and photochemical activities of isolated chloroplasts in genetic analysis of Lycopersicon esculentum Mill. hybrids. Photosynthetica 34:427–438.
Toledo Marante, F. J., Garcia Castellano, A., Estévez Rosas, F., Quintana Aguiar, J., and Bermejo Barrera, J. 2003. Identification and quantitation of allelochemicals from the lichen Lethariella canariensis: phytotoxicity and antioxidative activity. J. Chem. Ecol. 29:2049–2071.
Vavasseur, A., Gautier, H., Thibaud, M. C., and Lascève, G. 1991. Effects of usnic acid on the oxygen exchange properties of mesophyll cell protoplast from Commelina communis L. J. Plant Physiol. 139:90–94.
Wellburn, A. R. 1994. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 144:307–313.
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Latkowska, E., Lechowski, Z., Bialczyk, J. et al. Photosynthesis and Water Relations in Tomato Plants Cultivated Long-Term in Media Containing (+)-Usnic Acid. J Chem Ecol 32, 2053–2066 (2006). https://doi.org/10.1007/s10886-006-9128-6
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DOI: https://doi.org/10.1007/s10886-006-9128-6