Interspecific differences in sensitivity of the Antarctic moss Sanionia uncinata from King George Island (KGI) and James Ross Island (JRI) to photoinhibitory treatment were studied in laboratory conditions using chlorophyll fluorescence techniques. Slow (Kautsky) and fast (OJIP) kinetics were used for the measurements. Samples were exposed to a short-term (60 min) photoinhibitory treatment (PIT, 2000 μmol·m-2 ·s-1 PAR). The photoinhibitory treatment (PIT) led to photoinhibition which was indicated by the decrease in FV /FM and ΦPSII in KGI but not in JRI samples. However, this decrease was small and full recovery was reached 90 min after PIT termination. Non-photochemical quenching (NPQ) was activated during the PIT, and rapidly relaxed during recovery. Early stages of photoinhibition showed a drop in FV /FM and ΦPSII to minimum values within the first 10 s of the PIT, with their subsequent increase apparent within fast (0-5 min PIT) and slow (5-50 min PIT) phases of adjustment. The PIT caused a decrease in the performance index (Pi_Abs), photosynthetic electron transport per reaction centre (RC) (ET0 /RC). The PIT induced an increase in thermal dissipation per RC (DI0 /RC), effectivity of thermal dissipation (Phi_D0 ), absorption per RC (ABS/RC) and trapping rate per RC (TR0 /RC). In conclusion, PIT led to only slight photoinhibition followed by fast recovery in S. uncinata from KGI and JRI, since FV /FM and ΦPSII returned to pre-photoinhibitory conditions. Therefore, S. uncinata might be considered resistant to photoinhibition even in the wet state. The KGI samples showed higher resistance to photoinhibition than the JRI samples.

Department of Experimental Biology Division of Plant Physiology and Anatomy Faculty of Science Masaryk University Brno Czech Republic

Laboratory of Plant Ecophysiology Faculty of Natural Resources Catholic University Temuco Campus Luis Rivas del Canto Temuco Chile

See more in PubMed

Alboresi A., Gerotto C., Cazzaniga S., Bassi R., Morosinotto T. (2011) A red-shifted antenna protein associated with photosystem II in Physcomitrella patens. Journal of Biological Chemistry, 286, 28978-28987.

Alboresi A., Gerotto C., Giacometti G.M., Bassi R., Morosinotto T. (2010) Physcomitrella patens mutants affected on heat dissipation clarify the evolution of photoprotection mechanisms upon land colonization. Proceedings of the National Academy of Sciences of United States of America, 107, 11128-11133.

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. Photosynthetica, 52, 538-547.

Barbato R., Tadini L., Cannata R., Peracchio C., Jeran N., Alboresi A., Morosinotto T., Bajwa A.A., Paakkarinen V., Suorsa M., Aro E.-M., Pesaresi P. (2020) Higher order photoprotection mutants reveal the importance of ΔpH-dependent photosynthesis control in preventing light induced damage to both photosystem II and photosystem I. Scientific Reports, 10, 6770.

Barcikowski A., Loro P.M. (1999) Changes in chlorophyll content throughout the year in selected species of mosses on King George Island, South Shetland Islands, maritime Antarctic. Polish Polar Research, 20, 291-299.

Barták M., Hájek J., Očenášová P. (2012) 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.

Barták M., Hájek J., Vráblíková H., Dubová J. (2004) High-light stress and photoprotection in Umbilicaria antarctica monitored by chlorophyll fluorescence imaging and changes in zeaxanthin and glutathione. Plant Biology, 6, 333-341.

Barták M., Solhaug K.A., Vráblíková H., Gauslaa Y. (2006) Curling during desiccation protects the foliose lichen Lobaria pulmonaria against photoinhibition. Oecologia, 149, 553-560.

Barták M., Vráblíková H., 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, 497-504.

Bednaříková M., Folgar-Cameán Y., Kučerová Z., Lazár D., Špundová M., Hájek J., Barták M. (2020) Analysis of K- and L-band appearance in OJIPs in Antarctic lichens in low and high temperature. Photosynthetica, 58(SI), 646-656.

Cannone N., Corinti T., Malfasi F., Gerola P., Vianelli A., Vanetti I., Zaccara S., Convey P., Guglielmin M. (2017) Moss survival through in situ cryptobiosis after six centuries of glacier burial. Scientific Reports, 7, 4438.

Csintalan Z., Proctor M.C.F., Tuba Z. (1999) Chlorophyll fluorescence during drying and rehydration in the mosses Rhytidiadelphus loreus (Hedw.) Warnst., Anomodon viticulosus (Hedw.) Hook. & Tayl. and Grimmia pulvinata (Hedw.) Sm. Annals of Botany, 84, 235-244.

Daughtry C.S.T., Walthall C.L., Kim M.S., Brown D.E., Colstoun E., Mcmurtrey J.E. (2000) Estimating corn leaf chlorophyll concentration from leaf and canopy reflectance. Remote Sensing of Environment, 74, 229-239.

Dikaios I., Schiphorst C., Dall’Osto L., Alboresi A., Bassi R., Pinnola A. (2019) Functional analysis of LHCSR1, a protein catalyzing NPQ in mosses, by heterologous expression in Arabidopsis thaliana. Photosynthesis Research, 142, 249-264.

Elster J., Nedbalová L., Vodrážka R., Láska K., Haloda J., Komárek J. (2016) Unusual biogenic calcite structures in two shallow lakes, James Ross Island, Antarctica. Biogeosciences, 13, 535-549.

Fang S., Yu W., Qi Y. (2015) Spectra and vegetation index variations in moss soil crust in different seasons, and in wet and dry conditions. International Journal of Applied Earth Observation and Geoinformation, 38, 261-266.

Fernandes A.S., Alencar A.S., Evangelista H., Mazzei J.L., Felzenszwalb I. (2015) Photoprotective and toxicological activities of extracts from the Antarctic moss Sanionia uncinata. Pharmacognosy Magazine, 11, 38-43.

Fernandes A.S., Mazzei J.L., Alencar A.S., Evangelista H., Felzenszwalb I. (2011) Effects of Sanionia uncinata extracts in protecting against and inducing DNA cleavage by reactive oxygen species. Redox Report, 16, 201-207.

Fernandes A.S., Mazzei J.L., Oliveira C.G., Evangelista H., Marques M.R.C., Ferraz E.R.A., Felzenszwalb I. (2017) Protection against UV-induced toxicity and lack of mutagenicity of Antarctic Sanionia uncinata. Toxicology, 376, 126-136.

Furukawa R., Aso M., Fujita T., Akimoto S., Tanaka R., Tanaka A., Yokono M., Takabayashi A. (2019) Formation of a PSI-PSII megacomplex containing LHCSR and PsbS in the moss Physcomitrella patens. Journal of Plant Research, 132, 867-880.

Gamon J.A., Peñuelas J., Field C.B. (1992) A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency. Remote Sensing of Environment, 41, 35-44.

Gerotto C., Alboresi A., Giacometti G.M., Bassi R., Morosinotto T. (2012) Coexistence of plant and algal energy dissipation mechanisms in the moss Physcomitrella patens. New Phytologist, 196, 763-773.

Giudici G.N.M. (2019) Photoinhibition of primary photosynthetic processes in hydrated Polytrichum commune: analysis of non-photochemical quenching affecting species resistance. Czech Polar Reports, 9, 160-169.

Glime J.M. (2017) Photosynthesis: Photoinhibition. In: Glime J.M. (Ed), Bryophyte Ecology. Vol. 1, chapter 11-2-1. Physiological Ecology. Ebook sponsored by Michigan Technological University and the International Association of Bryologists. Last updated 11 November 2017. Available from http://digitalcommons.mtu.edu/bryophyte-ecology/.

Haboudane D., Miller J.R., Pattey E., Zarco-Tejada P.J., Strachan I.B. (2004) Hyperspectral vegetation indices and novel algorithms for predicting green LAI of crop canopies: Modeling and validation in the context of precision agriculture. Remote Sensing of Environment, 90, 337-352.

Hájek T., Tuittila E.-S., Ilomets M., Laiho R. (2009) Light responses of mire mosses: a key to survival after water-level drawdown? Oikos, 118, 240-250.

Heber U., Bilger W., Shuvalov V.A. (2006) Thermal energy dissipation in reaction centres and in the antenna of photosystem II protects desiccated poikilohydric mosses against photooxidation. Journal of Experimental Botany, 57, 2993-3006.

Hedenäs L. (1989) The genus Sanionia (Musci) in Northwestern Europe, a taxonomic revision. Annales Botanici Fennici, 26, 399-419.

Hedenäs L. (2003) Amblystegiaceae (Musci). Flora Neotropica Monograph, 89, 1-107.

Hong S.S., Xu D.Q. (1999) Light-induced increase in initial chlorophyll fluorescence Fo level and the reversible inactivation of PSII reaction centers in soybean leaves. Photosynthesis Research, 61, 269-280.

Killi D., Haworth M. (2017) Diffusive and metabolic constraints to photosynthesis in quinoa during drought and salt stress. Plants (Basel), 6, 49.

Kopalová K., Nedbalová L., Nývlt D., Elster J., Van De Vijver B. (2013) Diversity, ecology and biogeography of the freshwater diatom communities from Ulu Peninsula (James Ross Island, NE Antarctic Peninsula). Polar Biology, 36, 933-948.

Lewis Smith R.I., Øvstedal D.O. (1994) Solorina spongiosa in Antarctica: an extremely disjunct bipolar lichen. The Lichenologist, 26, 209-215.

Lichtenthaler H.K., Welburn A.R. (1983) Determination of total carotenoids and chlorophylls a and b of extracts in different solvents. Biochemical Society, 11, 591-592.

Lovelock C.E., Robinson S.A. (2002) Surface reflectance properties of Antarctic moss and their relationship to plant species, pigment composition and photosynthetic function. Plant, Cell and Environment, 25, 1239-1250.

Lud D., Moerdijk T.C.W., Van De Poll W.H., Buma A.G.J., Huiskes A.H.L. (2002) DNA damage and photosynthesis in Antarctic and Arctic Sanionia uncinata (Hedw.) Loeske under ambient and enhanced levels of UV-B radiation. Plant, Cell and Environment, 25, 1579-1589.

Lud D., Schlensog M., Schroeter B., Huiskes A.H.L. (2003) The influence of UV-B radiation on light-dependent photosynthetic performance in Sanionia uncinata (Hedw.) Loeske in Antarctica. Polar Biology, 26, 225-232.

Marschall M., Proctor M.C.F. (2004) Are Bryophytes shade plants? Photosynthetic light responses and proportions of chlorophyll a, chlorophyll b and total carotenoids. Annals of Botany, 94, 593-603.

Mathur S., Allakhverdiev S.I., Jajoo A. (2011) Analysis of high temperature stress on the dynamics of antenna size and reducing side heterogeneity of photosystem II in wheat leaves (Triticum aestivum). Biochimica et Biophysica Acta, 1807, 22-29.

May J.L., Parker T., Unger S., Oberbauer S.F. (2018) Short term changes in moisture content drive strong changes in Normalized Difference Vegetation Index and gross primary productivity in four Arctic moss communities. Remote Sensing of Environment, 212, 114-120.

Murray K.J., Tenhunen J.D., Nowak R.S. (1993) Photoinhibition as a control on photosynthesis and production of Sphagnum mosses. Oecologia, 96, 200-207.

Nabe H., Funabiki R., Kashino Y., Koike H., Satoh K. (2007) Responses to desiccation stress in bryophytes and an important role of dithiothreitol-insensitive non-photochemical quenching against photoinhibition in dehydrated states. Plant and Cell Physiology, 48, 1548-1557.

Newsham K.K. (2003) UV-B radiation arising from stratospheric ozone depletion influences the pigmentation of the Antarctic moss Andreaea regularis. Oecologia, 135, 327-331.

Newsham K.K., Hodgson A.W., Murray A.W.A., Peat H.J., Smith R.I.L. (2002) Response of two Antarctic bryophytes to stratographic ozone depletion. Global Change Biology, 8, 972-983.

Niyogi K.K., Li X.-P., Rosenberg V., Jung H.-S. (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? Journal of Experimental Botany, 56, 375-382.

Núñez-Olivera E., Otero S., Tomás R., Fabón G., Martínez-Abaigar J. (2010) Cyclic environmental factors only partially explain the seasonal variability of photoprotection and physiology in two mosses from an unforested headwater stream. The Bryologist, 113, 277-291.

Peñuelas J., Frederic B., Andfilella I. (1995) Semi-empirical indices to assess carotenoids/chlorophyll a ratio from leaf spectral reflectance. Photosynthetica, 31, 221-230.

Peñuelas J., Gamon J.A., Fredeen A.L., Merino J., Andfield C.B. (1994) Reflectance indices associated with physiological changes in nitrogen- and water-limited sunflower leaves. Remote Sensing of Environment, 48, 135-146.

Perera-Castro A.V., Waterman M.J., Turnbull J.D., Ashcroft M.B., McKinley E., Watling J.R., Bramley-Alves J., Casanova-Katny A., Zuniga G., Flexas J., Robinson S.A. (2020) It is hot in the sun: antarctic mosses have high temperature optima for photosynthesis despite cold climate. Frontiers in Plant Science, 11, 1178.

Pinnola A., Dall'Osto L., Gerotto C., Morosinotto T., Bassi R., Alboresi A. (2013) Zeaxanthin binds to light-harvesting complex stress-related protein to enhance nonphotochemical quenching in Physcomitrella patens. The Plant Cell, 25, 3519-3534.

Pizarro M., Contreras R.A., Köhler H., Zúńiga G.E. (2019) Desiccation tolerance in the Antarctic moss Sanionia uncinate. Biological Research, 52, 46.

Putzke J., Pereira A.B. (2020) The vegetation of the south shetland islands and the climatic change. In: Glaciers and Polar Environment. IntechOpen, 1-22. https://doi.org/10.5772/intechopen.94269.

Robinson S.A., King D.H., Bramley-Alves J., Waterman M.J., Ashcroft M.B., Wasley J., Turnbull J.D., Miller R.E., Ryan-Colton E., Benny T., Mullany K., Clarke L.J., Barry L.A., Hua Q. (2018) Rapid change in east Antarctic terrestrial vegetation in response to regional drying. Nature Climate Change, 8, 879-884.

Robinson S.A., Waterman M.J. (2014) Sunsafe bryophytes: Photoprotection from excess and damaging solar radiation. In: Hanson D.T., Rice S.K. (Eds), Photosynthesis in Bryophytes and Early Land Plants. Springer, Berlin, Germany, pp 113-130.

Rouse J.W., Haas R.H., Schell J.A., Anddeering D.W. (1974) Monitoring vegetation systems in the Great Plains with ERTS. In: Freden S.C., Mercanti E.P., Becker M. (Eds), Third Earth Resources Technology Satellite-1 Symposium. Volume I: Technical Presentations, NASA SP-351, NASA, Washington, DC, USA. pp 309-317.

Singh-Tomar R., Mathur S., Allakhverdiev S.I., Jajoo A. (2012) Changes in PS II heterogeneity in response to osmotic and ionic stress in wheat leaves (Triticum aestivum). Journal of Bioenergetics and Biomembranes, 44, 411-419.

Skácelová K., Barták M. (2014) Gradient of algal and cyanobacterial assemblages in a temporary lake with melting water at Solorina Valley, James Ross Island, Antarctica. Czech Polar Reports, 4, 185-192.

Smith R.I.L. (1996) Terrestrial and freshwater biotic components of the western Antarctic Peninsula. In: Ross R.M., Hofmann E.E., Quentin L.B. (Eds), Foundations of Ecological Research West of the Antarctic Peninsula Antarctic Research Series, Vol 70. American Geophysical Union, Washington DC, USA, pp 15-59.

Smith R.C.G., Adams J., Stephens D.J., Hick P.T. (1995) Forecasting wheat yield in a Mediterranean-type environment from the NOAA satellite. Australian Journal of Agricultural Research, 46, 113-125.

Song L., Liu W.-Y., Ma W.-Z., Qi J.-H. (2012) Response of epiphytic bryophytes to simulated N deposition in a subtropical montane cloud forest in southwestern China. Oecologia, 170, 847-856.

Soriano G., Del-Castillo-Alonso M.-Á., Monforte L., Núñez-Olivera E., Martínez-Abaigar J. (2019) Acclimation of Bryophytes to sun conditions, in comparison to shade conditions, is influenced by both photosynthetic and ultraviolet radiations. Frontiers in Plant Science, 10, 998.

Stella G.R. (2016) Light stress and photoprotection in green algae, mosses and diatoms. Ph.D. thesis, University of Verona and University Pierre et Marie Curie: pp 144.

Strasser R.J., Srivastava A., Tsimilli-Michael M. (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M., Pathre U., Mohanty P. (Eds), Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Taylor & Francis, London, UK, pp 445-483.

Strasser R.J., Tsimilli-Michael M., Srivastava A. (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou G.C., Govindjee (Eds), Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Springer, Dordrecht, the Netherlands, pp 321-362.

Takahashi S., Badger M.R. (2011) Photoprotection in plants: a new light on photosystem II damage. Trends in Plant Science, 16, 53-60.

Torres-Mellado G.A., Jaña R., Casanova-Katny M.A. (2011) Antarctic hair grass expansion in the South Shetland archipelago and Antarctic Peninsula revisited. Polar Biology, 34, 1679-1688.

Uchida M., Muraoka H., Nakatsubo T., Bekku Y., Ueno T., Kanda H., Koizumi H. (2002) Net photosynthesis, respiration, and production of the moss Sanionia uncinata on a Glacier Foreland in the High Arctic, Ny-Ålesund, Svalbard. Arctic, Antarctic, and Alpine Research, 34, 287-292.

Valøen K. (2019) Stochastic rain events increase NDVI through moss water content: a High-Arctic field experiment. Master’s thesis in MLREAL. Norwegian University of Science and Technology: pp 47.

Van Gaalen K.E. (2005) Photosynthetic CO2 exchange and spectral vegetation indices of boreal mosses. Master thesis, Lethbridge, Alberta, Canada. pp 110.

van Kooten O., Snell J.F.H. (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research, 25, 147-150.

Varela Z., Aboal J.R., Rey-Asensio A., Carballeira A., Fernández J.A. (2013) Establishing reference values of spectral reflectance indices in transplants of Pseudoscleropodium purum for potential use in atmospheric biomonitoring. The Bulletin of Environmental Contamination and Toxicology, 91, 345-348.

Virtanen R.J., Lundberg P.A., Moen J., Oksanen L. (1997) Topographic and altitudinal patterns in plant communities on European Arctic islands. Polar Biology , 17, 95-113.

Vredenberg W., Kasalicky V., Durchan M., Prasil O. (2006) The chlorophyll a fluorescence induction pattern in chloroplasts upon repetitive single turnover excitations: accumulation and function of QB-nonreducing centers. Biochimica et Biophysica Acta, 1757, 173-181.

Waterman M.J., Bramley-Alves J., Miller R.E., Keller P.A., Robinson S.A. (2018) Photoprotection enhanced by red cell wall pigments in three east Antarctic mosses. Biological Research, 51, 49.

Waterman M.J., Nugraha A.S., Hendra R., Ball G.E., Robinson S.A., Keller P.A. (2017) Antarctic moss biflavonoids show high antioxidant and ultraviolet-screening activity. Journal of Natural Products, 80, 2224-2231.

Yamakawa H., Fukushima Y., Itoh S., Heber U. (2012) Three different mechanisms of energy dissipation of a desiccation-tolerant moss serve one common purpose: to protect reaction centres against photo-oxidation. Journal of Experimental Botany, 63, 3765-3775.

Yamane Y., Shikanai T., Kashino Y., Koike H., Satoh K. (2000) Reduction of QA in the dark: another cause of fluorescence F0 increases by high temperatures in higher plants. Photosynthesis Research, 63, 23-34.

Yao X., Zhou H., Zhu Q., Li C., Zhang H., Wu J.-J., Xie F. (2017) Photosynthetic response of soybean leaf to wide light-fluctuation in maize--soybean intercropping system. Frontiers in Plant Science, 8, 1695.

Živčák M., Olšovská K., Slamka P., Galambošová J., Rataj V., Shao H.B., Brestič M. (2014) Application of chlorophyll fluorescence performance indices to assess the wheat photosynthetic functions influenced by nitrogen deficiency. Plant, Soil and Environment, 60, 210-215.

Zúñiga-González P., Zúñiga G.E., Pizarro M., Casanova-Katny A. (2016) Soluble carbohydrate content variation in Sanionia uncinata and Polytrichastrum alpinum, two Antarctic mosses with contrasting desiccation capacities. Biological Research, 49, 6.

The combined effect of Cd and high light stress on the photochemical processes in Arabidopsis thaliana

Photosynthetic responses of Eulophia dentata, Bletilla formosana, and Saccharum spontaneum under various photosynthetic photon flux density conditions