Evaluation of photosynthetic processes in Antarctic mosses and lichens exposed to controlled rate cooling: Species-specific responses

Vol.9,No.1(2019)

Abstract

Antarctic regions involve a great variety of habitats characterized by environmental stressors and life forms of autotrophic organisms with unique survival and functioning mechanisms. Lichens and mosses from these regions, similarly to high altitude alpine locations, have evolved physiological adaptations to perform photosynthesis at subzero temperatures. In this study we applied linear cooling technique in order to analyze interspecific differences in primary photosynthetic processes in Antarctic species affected by low and subzero temperature stress. We exposed Sanionia uncinata, Rhizoplaca aspidophora, Ochrolechia frigida, Cladonia sp., Himantormia lugubris and Umbilicaria decussata to the cooling from 20 to -35°C at a constant rate of 2°C min-1. Fluorometric parameters were measured during the cooling experiments: FV/FM - potential yield of photosynthetic processes in photosystem II, and F0 - minimal chlorophyll fluorescence. All the species showed S-curves for FV/FM in response to decreasing temperature and interspecific differences in the parameters of S-curve equation. Critical temperature for FV/FM was found -35°C for U. decussata, while the other species ranged between -16 to -20°C. The changes of F0 with thallus temperature decrease were species-specific. F0 decrease followed by an increase was found with cooling from 20 to -20°C, and from -20 to -35°C, respectively, in the majority of cases. These results suggest that the experimental moss and lichen species from Antarctica have a high resistance to freezing temperatures. The underlying physiological mechanisms are constitutive features of Antarctic lichens and mosses. They are a crucial part of the adaptation and short-term acclimatory changes in ecophysiological performance of the organisms in harsh polar environments.

 

References

Al-Khatib, K., Paulsen, G. M. (1989): Enhancement of thermal injury to photosynthesis in wheat plants and thylakoids by high light intensity. Plant Physiology, 90(3): 1041-1048.

Atanasiu, L. (1971): Photosynthesis and respiration of three mosses at winter low temperatures. Bryologist, 74(1): 23-27.

Bacior, M., Harańczyk, H., Nowak, P., Kijak, P., Marzec, M., Fitas, J. and Olech, M. A. (2019): Low-temperature immobilization of water in Antarctic Turgidosculum complicatulum and in Prasiola crispa. Part I. Turgidosculum complicatulum. Colloids and Surfaces B: Biointerfaces, 173: 869-875.

Barták, M., Vráblíková, H. and Hájek, J. (2003): Sensitivity of photosystem 2 of Antarctic lichens to high irradiance stress: fluorometric study of fruticose (Usnea antarctica) and foliose (Umbilicaria decussata) species. Photosynthetica, 41(4): 497-504.

Barták, M., Váczi, P., Hájek, J. and Smykla, J. (2007): Low-temperature limitation of primary photosynthetic processes in Antarctic lichens Umbilicaria antarctica and Xanthoria elegans. Polar Biology, 31(1): 47-51.

Block, W. (1994): Terrestrial ecosystems: Antarctica. Polar Biology, 14(5): 293-300.

Braun, C., Mustafa, O., Nordt, A., Pfeiffer, S. and Peter, H. (2012): Environmental monitoring and management proposals for the Fildes Region, King George Island, Antarctica. Polar Research, 31: 18206.

Buchner, O., Neuner, G. (2010): Freezing cytorrhysis and critical temperature thresholds for photosystem II in the peat moss Sphagnum capillifolium. Protoplasma, 243(1-4): 63-71.

Burke, M., Gusta, L., Quamme, H., Weiser, C. and Li, P. (1976): Freezing and injury in plants. Annual Review Plant Physiology, 27: 507-528.

Butler, W. L., Kitajima, M. (1975): Fluorescence quenching in photosystem II of chloroplasts. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 376(1): 116-125.

Butler, W. L. (1978): Energy distribution in the photochemical apparatus of photosynthesis. Annual Review of Plant Physiology, 29(1): 345-378.

Convey, P. (1996): The influence of environmental characteristics on life history attributes of Antarctic terrestrial biota. Biological Reviews, 71(2): 191-225.

Convey, P. (2001): Antarctic ecosystems. In: S. Levin (ed.): Encyclopedia of biodiversity. Academic Press, San Diego, pp. 171-184.

Crowe, J., Carpenter, J., Crowe, L. and Anchordoguy, T. (1990): Are freezing and dehydration similar stress vectors? A comparison of modes of interaction of stabilizing solutes with biomolecules. Cryobiology, 27(3): 219-231.

Davey, M. C. (1989): The effects of freezing & desiccation on photosynthesis and survival of terrestrial Antarctic algae and cyanobacteria. Polar Biology, 10(1): 29-36.

Fork, D. C., Sen, A. and Williams, W. P. (1987): The relationship between heat-stress and photobleaching in green and blue-green algae. Photosynthesis Research, 11(1): 71-87.

Genty, B., Briantais, J. M. and Baker, N. R. (1989): The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA)-General Subjects, 990(1): 87-92.

Hájek, J., Váczi, P. and Barták, M. (2009a): Photosynthetic electron transport at low temperatures in the green algal foliose lichens Lasallia pustulata and Umbilicaria hirsuta affected by manipulated levels of ribitol. Photosynthetica, 47(2): 199-205.

Hájek, J., Váczi, P., Barták, M., Smejkal, L. and Lipavská, H. (2009b): Cryoproective role of ribitol in Xanthoparmelia somloensis. Biologia Plantarum, 53(4): 677-684.

Hájek, J., Barták, M., Hazdrová, J. and Forbelská, M. (2016): Sensitivity of photosynthetic processes to freezing temperature in extremophilic lichens evaluated by linear cooling and chlorophyll fluorescence. Cryobiology, 73(3): 329-334.

Harańczyk, H., Grandjean, J., Olech, M. and Michalik, M. (2003): Freezing of water bound in lichen thallus as observed by 1H NMR. II. Freezing protection mechanisms in a cosmopolitan lichen Cladonia mitis and in Antarctic lichen species at different hydration levels. Colloids and Surfaces B: Biointerfaces, 28(4): 251-260.

Harańczyk, H, Casanova-Katny, A., Olech, M. and Strzałka, K. (2017): Dehydration and freezing resistance of lichenized fungi. In: V. Shukla, S. Kumar, N. Kumar (eds.): Plant Adaptation Strategies in Changing Environment. Springer, Singapore. 386 p. ISBN 978-981-10-6744-0.

Holdgate, M. W. (1970): Vegetation. In: M. W. Holdgate (ed.): Antarctic ecology. Academic Press, London, pp. 729-732.

Holdgate, M. W. (1977): Terrestrial ecosystems in the Antarctic. Philosophical Transactions of the Royal Society of London series B, 279: 5-25.

Kappen, L., Schroeter, B., Scheidegger, C., Sommerkorn, M. and Hestmark, G. (1996): Cold resistance and metabolic activity of lichens below 0°C. Advances in Space Research, 18(12): 119-128.

Kieft, T. L. (1988): Ice nucleation activity in lichens. Applied and Environmental Microbiology, 54(7): 1678-1681.

Kieft, T. L, Ahmadjian, V. (1989): Biological ice nucleation activity in lichen mycobionts and photobionts. Lichenologist, 21: 355-362.

Lamb, I. M. (1964). Antarctic lichens: I. The genera Usnea, Ramalina, Himantormia, Alectoria, Cornicularia. British Antarctic Survey Scientific Reports, 38: 1-34.

Lichtenthaler, H. K. (1988): In vivo chlorophyll fluorescence as a tool for stress detection in plants. In: H. K. Lichtenthaler (ed.): Applications of chlorophyll fluorescence in photosynthesis research, stress physiology, hydrobiology and remote sensing. Springer, Netherlands, pp. 129-142.

Linkosalo, T., Heikkinen, J., Pulkkinen, P. and Mäkipää, R. (2014): Fluorescence measurements show stronger cold inhibition of photosynthetic light reactions in Scots pine compared to Norway spruce as well as during spring compared to autumn. Frontiers in Plant Science, 5: 264.

Longton, R. E. (1988): Biology of polar bryophytes and lichens. Cambridge University Press. CUP Archive. 404 p.

Lovelock, C. E., Jackson, A. E., Melick, D. R. and Seppelt, R. D. (1995): Reversible photoinhibition in Antarctic moss during freezing and thawing. Plant Physiology, 109(3): 955-961.

Ludlow, M. M. (1987): Light stress at high temperature. In: D. J. Kyle, C. B. Osmond, C. J. Arntzen (eds.): Photoinhibition. Elsevier, Amsterdam, pp. 89–109.

Malkin, S., Kok, B. (1966): Fluorescence induction studies in isolated chloroplasts I. Number of components involved in the reaction and quantum yields. Biochimica et Biophysica Acta (BBA)-Biophysics including Photosynthesis, 126(3): 413-432.

Mishra, A., Hájek, J., Tuháčková, T., Barták, M. and Mishra, K. B. (2015): Features of chlorophyll fluorescence transients can be used to investigate low temperature induced effects on photosystem II of algal lichens from polar regions. Czech Polar Reports, 5(1): 99-111.

Moffett, B. F., Getti, G., Henderson-Begg, S. K. and Hill, T. C. J. (2015): Ubiquity of ice nucleation in lichen—possible atmospheric implications. Lindbergia, 38: 39-43.

Nash, T. H., Kappen, L., Losch, R., Larson, W. and Matthes-Sears, U. (1987): Cold resistance of lichens with Trentepohlia or Trebouxia photobionts from the North American west coast. Flora, 179: 241-251.

vstedal, D. O., Lewis Smith, R. I. (2001): Lichens of Antarctica and South Georgia. A Guide to Their Identification and Ecology. Cambridge University Press, Cambridge, 424 p.

Peat, H. J., Clarke, A. and Convey, P. (2007): Diversity and biogeography of the Antarctic flora. Journal of Biogeography, 34(1): 132-146.

Pospíšil, P., Skotnica, J. and Nauš, J. (1998): Low and high temperature dependence of minimum F0 and maximum FM chlorophyll fluorescence in vivo. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1363(2): 95-99.

Robinson, C. H. (2001): Cold adaptation in Arctic and Antarctic fungi. New Phytologist, 151(2): 341-353.

Šabacká, M., Elster, J. (2006): Response of cyanobacteria and algae from Antarctic wetland habitats to freezing and desiccation stress. Polar Biology, 30(1): 31.

Schroeter, B., Scheidegger, C. (1995): Water relations in lichens at subzero temperatures: structural changes and carbon dioxide exchange in the lichen Umbilicaria aprina from continental Antarctica. New Phytologist, 131(2): 273-285.

Wharton, D. A., Goodall, G. and Marshall, C. J. (2002): Freezing rate affects the survival of a short-term freezing stress in Panagrolaimus davidi, an Antarctic nematode that survives intracellular freezing. CryoLetters, 23(1): 5-10.

Wharton, D. A. (2003): The environmental physiology of Antarctic terrestrial nematodes: A review. Journal of Comparative Physiology B, 173(8): 621-628.

Metrics

351

Views

56

PDF views