Effects of short-term low temperature stress on chlorophyll fluorescence transients in Antarctic lichen species
Vol.6,No.1(2016)
Chlorophyll fluorescence is an effective tool for investigating characteristics of any photosynthesizing organisms and its responses due to different stressors. Here, we have studied a short-term temperature response on two Antarctic green algal lichen species: Umbilicaria antarctica, and Physconia muscigena. We measured slow chlorophyll fluorescence transients in the species during slow a cooling of thallus temperature from 20°C to 5°C with a 10 min. acclimation at each temperature in dark. The measurements were supplemented with saturation pulses for the analysis of chlorophyll fluorescence parameters: maximum yield of PS II photochemistry (FV/FM), effective quantum yield of PS II photochemistry (FPSII) and non-photochemical quenching (NPQ). In response to decreasing thallus temperature, we observed species-specific changes in chlorophyll fluorescence levels P, S, M, T reached during chlorophyll fluorescence transient as well as in the shape of the chlorophyll fluorescence transients. With a decrease in temperature, the time at which M and T chlorophyll fluorescence levels were reached, increased. These changes were attributed to redox state of plastoquinon pool, changes in Calvin-Benson cycle activity, non-photochemical quenching components, state transition in particular. In this study, we present some chlorophyll fluorescence ratios (P/M, M/T, P/T) and chlorophyll fluorescence increase rates (FR1, i.e. O to P, and FR2 - i.e. S to M) as the parameters reflecting direct temperature effects on chloroplastic apparatus of lichen alga sensitively. We proposed that species-specific changes in the slow phase of chlorophyll fluorescence transients could be potentially used as indicators of low temperature effects in photosynthetic apparatus of lichen algal photobionts. Interspecific differences in response to low temperature might be evaluated using the approach as well.
photosynthetic processes; polyphasic kinetics; chlorophyll fluorescence parameters; James Ross Island; Galindez Island
Agati, G., Cerovic, Z. G. and Moya, I. (2000): The effect of decreasing temperature up to chilling values on the in vivo F685/F735 chlorophyll fluorescence ratio in Phaseolus vulgaris and Pisum sativum: The role of the photosystem I contribution to the 735 nm fluorescence band. Photochemistry and Photobiology, 72: 75-84.
Allen, J. F. (1992): Protein phosphorylation in regulation of photosynthesis. Biochimica et Biophysica Acta, 1098: 275–335.
Barták, M., Hájek, J. and 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., 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, 31:47–51.
Barták, M., Váczi, P., Stachoň , Z. and Kubešová, S. (2015): Vegetation mapping of moss-dominated areas of northern part of James Ross Island (Antarctica) and a suggestion of protective measures. Czech Polar Reports, 5: 75-87.
Bolhar-Nordenkampf, H., Öquist, G. (1993): Chlorophyll fluorescence as a tool in photosynthesis research. In: D. O. Hall, J. M. O. Scurlock, H. R. BolharNordenkampf, R. C. Leegood, S.P. Long (eds.): Photosynthesis and Production in a Changing Environment, Chapman & Hall, London, pp. 193-206.
Conti, S., Hazdrová, J., Hájek, J., Očenášová, P., Barták, M., Skácelová, K. and Adamo, P. (2014): Comparative analysis of heterogeneity of primary photosynthetic processes within fruticose lichen thalli: Preliminary study of interspecific differences. Czech Polar Reports, 4: 149-157.
Finazzi, G., Barbagalo, R. P., Bergo, E., Barbato, R. and Forti, G. (2001): Photoinhibition of Chlamydomonas reinhardtii in State 1 and State 2. Damages to the photosynthetic apparatus under linear and cyclic electron flow. The Journal of Biological Chemistry, 276: 22251-22257.
Flexas, J., Escalona, J. M., Evain, S., Gulías, J., Moya, I., Osmond, C.B. and Medrano, H. (2002): Steady-state chlorophyll fluorescence (Fs) measurements as a tool to follow variations of net CO2 assimilation and stomatal conductance during water-stress in C3 plants. Physiologia Plantarum, 114: 231-240.
Kaňa, R., Kotabová, E., Komárek, O., Šedivá, B., Papageorgiou, G. C., Govindjee and Prášil, O. (2012): The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochimica et Biophysica Acta, 1817: 1237-1247.
Krause, G.H. (1988): Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiologia Plantarum, 74: 566-574.
Kodru, S., Malavath, T., Devadasu, E., Nellaepalli , S., Stirbet, A., Subramanyam, R. and Govindjee (2015): The slow S to M rise of chlorophyll a fluorescence reflects transition from state 2 to state 1 in the green alga Chlamydomonas reinhardtii. Photosynthesis Research, 125:219-231.
Lemeille, S., Rochaix, J.-D. (2011): State transitions at the crossroad of thylakoid signaling pathways. Photosynthesis Research, 106: 33-46.
Lichtenthaler, H. K., Buschmann, C. and Knapp, M. (2005): How to correctly determine the different chlorophyll fluorescence parameters and the chlorophyll fluorescence decrease ratio RFd of leaves with the PAM fluorometer. Photosynthetica, 43: 379-393.
Lichtenthaler, H. K., Buschmann, C., Rinderle, U. and Schmuck, G. (1986): Application of chlorophyll fluorescence in ecophysiology. – Radiatiom Environment. Biophysics, 25: 297-308.
Lichtenthaler, H. K., Langsdorf, G., Lenk, S. and Buschmann, C. (2005): Chlorophyll fluorescence imaging of photosynthetic activity with the flash-lamp fluorescence imaging system. Photosynthetica, 43: 355-369.
Marečková, M., Barták, M. (2016): Interspecific differences in photosynthetic parameters of Antarctic foliose lichens at low temperature as evaluated by chlorophyll fluorescence parameters. Students in Polar and Alpine Research, Brno.
Minagawa, J. (2011): State transitions - the molecular remodeling of photosynthetic supercomplexes that controls energy flow in the chloroplast. Biochimica et Biophysica Acta, 1807: 897-905.
Mishra, A., Heyer, A. G. and Mishra, K. B. (2014): Chlorophyll fluorescence emission can screen cold tolerance of cold acclimated Arabidopsis thaliana accessions. Plant Methods, 38:1- 10.
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: 99-111.
Murata, N. (2009): The discovery of state transitions in photosynthesis 40 years ago. Photosynthesis Research, 99: 155-160.
Nabe, H., Funabiki, R., Kashino, Y., Koike, H. and 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 Cell Physiology, 48: 1548–1557.
Noctor G., Horton, P. (1990): Uncouple titration of energy-dependent chlorophyll fluorescence quenching and photosystem II photochemical yield in intact pea chloroplasts. Biochimica et Biophysica Acta, 1016:228-234.
Papageorgiou, G. C., Govindjee (1968): Light-induced changes in the fluorescence yield of chlorophyll a in vivo. I. Anacystis nidulans. Biophysical Journal, 8: 1299-1315.
Papageorgiou, G. C., Govindjee (2011): Photosystem II fluorescence slow changes – scaling from the past. Journal of Photochemistry and Photobiology B: Biology, 104: 258-270.
Riznichenko, G., Lebedeva, G., Pogosyan, S., Sivchenko, M. and Rubin, A. (1996): Fluorescence induction curves registered from individual microalgae cenobiums in the process of population growth. Photosynthesis Research , 49: 151-157.
Roháček, K. (2002): Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica, 40: 13-29.
Roháček, K., Barták, M. (1999): Technique of the modulated chlorophyll fluorescence: basic concepts, useful parameters, and some applications. Photosynthetica, 37: 339-363.
Roháček, K., Soukupová, J. and Barták, M. (2008): Chlorophyll Fluorescence: A wonderful tool to study plant physiology and plant stress. In: B. Schoefs (ed.): Plant Cell Compartments – Selected Topics. Research Signpost, Kerala, India, pp. 41-104.
Seaton G.G., Walker, D.D. (1990) : Chlorophyll fluorescence as a measure of carbon metabolism. Proceedings of Royal Society (London), B242: 29-35.
Smillie, R. M., Hetherington, S. E. (1984). A screening method for chilling tolerance using chlorophyll fluorescence in vivo. In: C. Sybesma (ed.): Advances in Photosynthesis Research. Proceedings of the VIth International Congress on Photosynthesis, Brussels, Belgium, August 1–6, 1983. Volume IV, Publisher Springer Netherlands, pp. 471-474. ISBN 978-90-247-2945-6, DOI: 10.1007/978-94-017-4971-8_104.
Stirbet, A., Riznichenko, G. Yu., Rubin, A. B. and Govindjee (2014): Modeling chlorophyll a fluorescence transient: Relation to photosynthesis. Biochemistry (Moscow), 79: 291-323.
Srand, M., Lundmark, T. (1987): Effects of low night temperature and light on chlorophyll fluorescence of field-grown seedlings of Scots pine (Pinus sylvestris L.). Tree Physiology, 3: 211-224.
Takacs, Z., Csintalan, Z. and Tuba, Z. (1999): Responses of the lichen Cladonia convoluta to high CO2 level and heavy metal treatment. Zeitschrift für Naturforschung, 54c: 797-801.
Tsimilli-Michael, M., Stamatakis, K. and Papageorgiou, G. C. (2009): Dark-to-light transition in Synechococcus sp. PCC 7942 cells studied by fluorescence kinetics assesses plastoquinone redox poise in the dark and photosystem II fluorescence component and dynamics during state 2 to state 1 transition.. Photosynthesis Research, 99: 243-255.Valladares, F., Sanchez-Hoyos, A. and Manrique, E. (1995): Diurnal changes in photosynthetic efficiency and carotenoid composition of the lichen Anaptychia ciliaris: Effects of hydration and light intensity. The Bryologist, 98: 375-382.
Vernotte, C., Etienne, A. L. and Briantais, J. M. (1979): Quenching of the system II chlorophyll fluorescence by the plastoquinone pool. Biochimica et Biophysica Acta, 545: 519-527.,
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