Photosynthetica 2014, 52(4):538-547 | DOI: 10.1007/s11099-014-0060-7

Changes in photosynthesis, pigment composition and glutathione contents in two Antarctic lichens during a light stress and recovery

K. Balarinová1, M. Barták1,*, J. Hazdrová1, J. Hájek1, J. Jílková1
1 Faculty of Science, Department of Experimental Biology, Laboratory of Photosynthetic Processes, Masaryk University, Brno, Czech Republic

Over last decades, several studies have been focused on short-term high light stress in lichens under laboratory conditions. Such studies reported a strong photoinhibition of photosynthesis accompanied by a partial photodestruction of PSII, involvement of photoprotective mechanisms, and resynthetic processes into gradual recovery. In our paper, we applied medium [800 μmol(photon) m-2 s-1] light stress to induce negative changes in PSII funcioning as well as pigment and glutathione (GSH) content in two Antarctic fruticose lichen species. Chlorophyll (Chl) fluorescence parameters, such as potential and effective quantum yield of photosynthetic processes and fast transients (OJIP) recorded during high light exposition and recovery, revealed that Usnea antarctica was less susceptible to photoinhibition than U. aurantiaco-atra. This might be supported by a more pronounced high light-induced reduction in Chl a and b contents in U. aurantiaco-atra compared with U. antarctica. In both experimental species, total GSH showed an initial increase during the first 30-40 min of high light treatment followed by a decrease (60 min) and an increase during dark recovery. Full GSH recovery, however, was not finished in U. aurantiaco-atra even after 5 h indicating lower capacity of photoprotective mechanisms in the species. OJIP curves showed high light-induced decrease in both species, however, the recovery of the OJIPs shape to pre-photoinhibitory values was faster and more apparent in U. antarctica than in U. aurantiaco-atra. The results are discussed in terms of sensitivity of the two species to photoinhibition and their photosynthetic performance in natural environment.

Additional key words: carotenoids; chlorophyll fluorescence; performance index; thallus

Received: December 20, 2013; Accepted: July 16, 2014; Published: December 1, 2014  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Balarinová, K., Barták, M., Hazdrová, J., Hájek, J., & Jílková, J. (2014). Changes in photosynthesis, pigment composition and glutathione contents in two Antarctic lichens during a light stress and recovery. Photosynthetica52(4), 538-547. doi: 10.1007/s11099-014-0060-7
Download citation

References

  1. Barták, M.: Lichen photosynthesis. Scaling from the cellular to the organism level. - In: Hohmann-Marriott, M. (ed.): The Structural Basis of Biological Energy Generation. Advances in Photosynthesis and Respiration. Pp. 379-400. Springer, Dordrecht 2014. Go to original source...
  2. Barták, M., Solhaug, K.-A., Vráblíková, H., Gauslaa, Y.: Curling during desiccation protects the foliose lichen Lobaria pulmonaria against photoinhibition. - Oecologia 149: 553-560, 2006. Go to original source...
  3. Barták, M., Hájek, J., Očenášová, P.: Photoinhibition of photosynthesis in Antarctic lichen Usnea antarctica. I. Light intensity- and light duration-dependent changes in functioning of photosystem II. - Czech Polar Reports 2: 42-51, 2011. Go to original source...
  4. Barták, M., Hájek, J., Vráblíková, H. et al.: High-light stress and photoprotection in Umbilicaria antarctica monitored by chlorophyll fluorescence imaging and changes in zeaxanthin and glutathione. - Plant Biol. 6: 333-341, 2004. Go to original source...
  5. Barták, M., Vráblíková, H., Hájek, J.: Sensitivity of photosystem 2 of Antarctic lichens to high irradiance stress: Fluorometric study of fruticose (Usnea antarctica) and foliose (Umbilicaria decussata) species. - Photosynthetica 41: 497-504 2003. Go to original source...
  6. Barták, M., Vráblíková-Cempírková, H., Štepigová, J. et al.: Duration of irradiation rather than quantity and frequency of high irradiance inhibits photosynthetic processes in the lichen Lasallia pustulata. - Photosynthetica 46: 161-169, 2008. Go to original source...
  7. Bilger, W., Rimke, S., Schreiber, U. et al.: Inhibition of energytransfer to photosystem II in lichens by dehydration. - J. Plant Physiol. 134: 261-268, 1989. Go to original source...
  8. Bjerke, J.W., Joly, D., Nilsen, L. et al.: Spatial trends in usnic acid concentrations of the lichen Flavocetraria nivalis along local climatic gradients in the Arctic (Kongsfjorden, Svalbard). - Polar Biol. 27: 409-417, 2004. Go to original source...
  9. Bohuslavová, O.: Ecology of lichens on deglaciated parts of James Ross Island, the Antarctic. Ph.D. Thesis. Pp. 1-73. Masaryk University, Brno 2012.
  10. Burrit, D.J., MacKenzie, S.: Antioxidant metabolism during acclimation of Begonia × erythrophylla to high light levels. - Ann. Bot. 91: 783-794, 2003. Go to original source...
  11. Carreras, H.A., Wannaz, E.D., Perez, C.A. et al.: The role of urban air pollutants on the performance of heavy metal accumulation in Usnea amblyoclada. - Environ. Pollut. 97: 50-57, 2005. Go to original source...
  12. Colville, L., Kranner, I.: Desiccation tolerant plants as model systems to study redox regulation of protein thiols. - Plant Growth Regul. 62: 241-255, 2010. Go to original source...
  13. Davies, B.J., Glasser, N.F., Carrivick, J.L. et al.: Landscape evolution and ice-sheet behaviour in a semi-arid polar environment: James Ross Island, NE Antarctic Peninsula. - In: Hambrey, M.H., Barker, P.F., Barrett, P.J. et al. (ed.): Antarctic Palaeoenvironments and Earth-Surface Processes. Pp. 353-395. Geological Society, London 2013. Go to original source...
  14. Del Hoyo, A., Álvarez, R., Del Campo, E.M. et al.: Oxidative stress induces distinct physiological responses in the two Trebouxia phycobionts of the lichen Ramalina farinacea. - Ann. Bot. 107: 109-118, 2011. Go to original source...
  15. Demmig-Adams, B., Maguas, C., Adams, W.W. et al.: Effect of high light on the efficiency of photochemical energyconversion in a variety of lichen species with green and bluegreen phycobionts. - Planta 180: 400-409, 1990. Go to original source...
  16. Hauck, M., Dulamsuren, C., Mühlenberg, M.: Lichen diversity on steppe slopes in the northern Mongolian mountain taiga and its dependence on microclimate. - Flora 202: 530-546, 2007. Go to original source...
  17. Heber, U., Azarkovich, M., Shuvalov, V.: Activation of mechanisms of photoprotection by desiccation and by light: poikilohydric photoautotrophs. - J. Exp. Bot. 58: 2745-2759, 2007. Go to original source...
  18. Holm, G.: Chlorophyll mutations in barley. - Acta Agr. Scand. 4: 457-471, 1954. Go to original source...
  19. Huneck, S.: Progress in the chemistry of lichen substances, 2000-2005. - J. Hattori Bot. Lab. 100: 671-694, 2006.
  20. Kappen L., Breuer M., Bölter M.: Ecological and physiological investigations in continental antarctic cryptogams. 3. Photosynthetic production of Usnea sphacelata: diurnal courses, models, and the effect of photoinhibition. - Polar Biol. 11: 393-402, 1991. Go to original source...
  21. Košler, J., Magna, T., Mlčoch, B. et al.: Combined Sr, Nd, Pb, and Li isotope geochemistry of alkaline lavas from northern James Ross Island (Antarctic Peninsula) and implications for back-arc magma formation. - Chem. Geol. 258: 207-218, 2009. Go to original source...
  22. Krábková, G.: [Content of UV-absorbing compounds and pigments in extracts from lichens from different Earth regions.] Pp. 1-67. Diploma Thesis. Masaryk University, Brno 2013. [In Czech]
  23. Kranner, I.: Determination of glutathione, glutathione disulphide and two related enzymes, glutathione reductase and glucose-6-phosphate dehydrogenase, in fungal and plant cells. - In: Varma, A. (ed.): Mycorrhiza Manual. Pp. 227-241. Springer, Berlin 1998. Go to original source...
  24. Kranner, I.: Glutathione status correlates with different degrees of desiccation tolerance in three lichens. - New Phytol. 154: 451-460, 2002. Go to original source...
  25. Kranner, I., Birtić, S.: A modulating role for antioxidants in desiccation tolerance. - Integr. Comp. Biol. 45: 734-740, 2005. Go to original source...
  26. Kranner, I., Cram, W.J., Zorn, M. et al.: Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. - P. Natl. Acad. Sci. USA 102: 3141-3146, 2005. Go to original source...
  27. Láska, K., Barták, M., Hájek, J. et al.: Climatic and ecological characteristics of deglaciated area of James Ross Island, Antarctica, with a special respect to vegetation cover. - Czech Polar Reports 1: 49-62, 2011. Go to original source...
  28. Manrique, E., Balaguer, L., Barnes, J. et al.: Photoinhibition studies in lichens using chlorophyll fluorescence analysis. - Bryologist 96: 443-449, 1993. Go to original source...
  29. May, M.J., Vernoux, T., Leaver, C. et al.: Glutathione homeostasis in plants: implications for environmental sensing and plant development. - J. Exp. Bot. 49: 649-667, 1998. Go to original source...
  30. Mrak, T., Jeran, Z., Batič, F. et al.: Arsenic accumulation and thiol status in lichens exposed to As(V) in controlled conditions. - Biometals 23: 207-219, 2010. Go to original source...
  31. Müller, M., Zechmann, B., Zellnig, G.: Ultrastructural localization of glutathione in Cucurbita pepo plants. - Protoplasma 223: 213-219, 2004. Go to original source...
  32. Noctor, G., Foyer, C.H.: Ascorbate and glutathione: Keeping active oxygen under control. - Annu. Rev. Plant Phys. 49: 249-279, 1998. Go to original source...
  33. Noctor, G., Gomez, L., Vanacker, H. et al.: Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signalling. - J. Exp. Bot. 53: 1283-1304, 2002. Go to original source...
  34. Onofri, S., Fenice, M., Cicalini, A.R. et al.: Ecology and biology of microfungi from Antarctic rocks and soils. - Ital. J. Zool. 67: 163-167, 2000. Go to original source...
  35. Palmqvist, K., Dahlman, L., Valladares, F. et al.: CO2 exchange and thallus nitrogen across 75 contrasting lichen associations from different climate zones. - Oecologia 133: 295-306, 2002. Go to original source...
  36. Rausch, T., Wachter, A.: Sulfur metabolism: a versatile platform for launching defence operations. - Trends Plant Sci. 10: 503-509, 2005. Go to original source...
  37. Riddell, J., Padgett, P.E., Nash III, T.H.: Physiological responses of lichens to factorial fumigations with nitric acid and ozone. - Environ. Pollut. 170: 202-210, 2012. Go to original source...
  38. Rikkinen, J.: What's Behind the Pretty Colours. A Study on the Photobiology of Lichens. Edition 4: Bryobrothera. Pp. 239, The Finnish Bryological Society, Helsinki 1995.
  39. Singh, J., Dubey, A.K., Singh, R.P.: Antarctic terrestrial ecosystem and role of pigments in enhanced UV-B radiations. - Rev. Environ. Sci. Biotechnol. 10: 63-77, 2011. Go to original source...
  40. Singh, R., Ranjan, S., Nayaka, S. et al.: Functional characteristics of a fruticose type of lichen, Stereocaulon foliolosum Nyl., in response to light and water stress. - Acta Physiol. Plant. 35: 1605-1615, 2013. Go to original source...
  41. Smellie, J.L., Johnson, J.S., McIntosh, W.C. et al.: Six million years of glacial history recorded in volcanic lithofacies of the James Ross Island Volcanic Group, Antarctic Peninsula. - Palaeogeogr. Palaeoclimatol. Palaeoecol. 260: 122-148, 2008. Go to original source...
  42. Štepigová, J., Vráblíková, H., Lang, J. et al.: Glutathione and zeaxanthin formation during high light stress in foliose lichens. - Plant Soil Environ. 53: 340-344, 2007. Go to original source...
  43. Stirbet, A.: Excitonic connectivity between photosystem II units: what is it, and how to measure it? - Photosynth. Res. 116: 189-214, 2013. Go to original source...
  44. Strasser, R.J., Shrivastava, A., Tsimilli-Michael, M.: The fluorescence transient as a tool to characterize and screen photosynthetic samples. - In: Yunus, M., Pathre, U., Mohanty, P. (ed): Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Pp. 445-483. Taylor and Francis, London 2000.
  45. Szalai, G., Kellös, T., Galiba, G. et al.: Glutathione as an antioxidant and regulatory molecule in plants under abiotic stress conditions. - Plant Growth Regul. 28: 66-80, 2009. Go to original source...
  46. Tausz, M.: The role of glutathione in plant response and adaptation to natural stress. - In: Grill, D., Tausz, M., De Kok, L.J.: Significance of Glutathione to Plant Adaptation to the Environment. Pp. 101-122. Springer, Dordrecht 2001. Go to original source...
  47. Terauds, A., Chown, S.L., Morgan, F. et al.: Conservation biogeography of the Antarctic. - Diversity Distrib. 18: 726-741, 2012. Go to original source...
  48. Tretiach, M., Baruffo, L., Piccotto, M.: Effects of Mediterranean summer conditions on chlorophyll a fluorescence emission in the epiphytic lichen Flavoparmelia soredians: a field study. - Plant Biosyst. 146: 171-180, 2012. Go to original source...
  49. Veerman, J., Vasil'ev, S., Paton, G.D. et al.: Photoprotection in the lichen Parmelia sulcata: The origins of desiccation-induced fluorescence quenching. - Plant Physiol. 145: 997-1005, 2007. Go to original source...
  50. Vráblíková, H., Barták, M., Wönisch, A.: Changes in glutathione and xanthophyll cycle pigments in the high light-stressed lichens Umbilicaria antarctica and Lassalia pustulata. - J. Photoch. Photobiol. B 79: 35-41, 2005. Go to original source...
  51. Wendler, J., Holzwarth, A.R.: State transitions in the green alga Scenedesmus obliquus probed by time-resolved chlorophyll fluorescence spectroscopy and global data analysis. - Biophys. J. 52: 717-728, 1987. Go to original source...