Low temperature inhibition of photosystems I, and II in Antarctic lichens of different morphotypes
Vol.14,No.2(2024)
Chlorophyll fluorescence techniques represent an effective tool for photosynthetic performance of extremophilic poikilohydric autotrophs from cold Earth regions. Many parameteres of these techniques can detect the response of photosystem II (PS II) to a great variety of stressors. Chlorophyll fluorescence parametrs related to PS II funcioning are used quite often. For Antarctic lichens, that evolved several physiological mechanisms to cope with close to 0°C or even at sub-zero temperatures. The data gained from both field- and laboratory based studies helps predict ecophysiological consequeces of episodic drops in in situ temperature as well as resistence of Antarctic terrestial autotrophs to low temperature. However, the effect of low and sub-zero temperature on photosystem I (PS I) funcitioning is studied much less frequently than PS II. Therefore, the aim of our study was to evaluate PS II and PS I activities under low temperature and enlarge the knowledge on the low temperature effects on lichen photosynthesis. The focus of our laboratory experiments was to quantify the effect of a short-term treatment by 0°C on chlorophyll fluorescence parameters related to PS II and PS I functioning in two species of chlorolichens from Antarctica (Usnea antarctica, Himantormia lugubris). Our results suggest low temperature-induced decline in physiological processes in chloroplast (Performance index decrease) and activation of protective mechanisms (non-photochemical quenching increase).
Himantormia; Usnea; PS I; PS II; Nelson Island; chlorophyll fluorescence
Agarwal, T., Wang, X., Mildenhall, F., Ibrahim, I. M., Puthiyaveetil, S. and Varala, K. (2023): Chilling stress drives organ-specific transcriptional cascades and dampens diurnal oscillation in tomato. Horticulture Research, 10(8): uhad137. doi: 10.1093/hr/uhad137
Andrzejowska, A., Hájek, J., Puhovkin, A., Harańczyk, H. and Barták, M. (2024): Freezing temperature effects on photosystem II in Antarctic lichens evaluated by chlorophyll fluorescence. Journal of Plant Physiology, 294: 154192. doi: 10.1016/j.jplph.2024.154192
Bacior, M., Harańczyk, H., Nowak, P., Kijak, P., Marzec, M., Fitas, J. and Olech, M. (2022): Low-temperature investigation of residual water bound in free-living Antarctic Prasiola crispa. Antarctic Science, 34(5): 389-400. doi:10.1017/S0954102022000335
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. doi: 10.1007/s00300-007-0331-x
Bednaříková, M., Folgar-Cameán, Y., Kučerová, Z., Lazár, D., Špundová, M., Hájek, J. and Barták, M. (2020): Special issue in honour of Prof. Reto J. Strasser – Analysis of K- and L-band appearance in OJIPs in Antarctic lichens in low and high temperature. Photosynthetica, 58(SI): 646-656. doi: 10.32615/ps.2019.180
Ben-Jabeur, M., Romero, A. G., Vicente, R., Kthiri, Z., Kefauver, S. C., Serret, M. D., Araus, J. and Hamada, W. (2021): MultispeQ for tracing biostimulants effect on growth promoting and water stress tolerance in wheat. Cham: Springer International Publishing. In: Recent Advances in Environmental Science from the Euro-Mediterranean and Surrounding Regions (2nd Edition) Proceedings of 2nd Euro-Mediterranean Conference for Environmental Integration (EMCEI-2), Tunisia 2019.
Bharati, R., Gupta, A., Novy, P., Severová, L., Šrédl, K., Žiarovská, J. and Fernández-Cusimamani, E. (2023): Synthetic polyploid induction influences morphological, physiological, and photosynthetic characteristics in Melissa officinalis L. Frontiers in Plant Science, 14: 1332428. doi: 10.3389/fpls.2023.1332428
Bukhov, N. G., Govindachary, S., Egorova, E. A. and Carpentier, R. (2004): Recovery of photosystem I and II activities during re-hydration of lichen Hypogymnia physodes thalli. Planta, 219(1): 110-120. doi: 10.1007/s00425-003-1195-0
Caspy, I., Schwartz, T., Bayro-Kaiser, V., Fadeeva, M., Kessel, A., Ben-Tal, N. and Nelson, N. (2021). Dimeric and high-resolution structures of Chlamydomonas Photosystem I from a temperature-sensitive Photosystem II mutant. Communications Biology, 4(1): 1380. doi: 10.1038/s42003-021-02911-7
Cho, S. M., Lee, H., Hong, S. G. and Lee, J. (2020): Study of ecophysiological responses of the antarctic fruticose lichen Cladonia borealis using the PAM fluorescence system under natural and laboratory conditions. Plants (Basel, Switzerland), 9(1): 85. doi: 10.3390/plants9010085
Fernández-Calleja, M., Monteagudo, A., Casas, A. M., Boutin, C., Pin, P. A., Morales, F. and Igartua, E. (2020): Rapid On-site phenotyping via field fluorimeter detects differences in photosynthetic performance in a hybrid-parent barley germplasm set. Sensors (Basel, Switzerland), 20(5): 1486. doi: 10.3390/s20051486
Gerotto, C., Alboresi, A., Meneghesso, A., Jokel, M., Suorsa, M., Aro, E. M. and Morosinotto, T. (2016): Flavodiiron proteins act as safety valve for electrons in Physcomitrella patens. Proceedings of the National Academy of Sciences of the United States of America, 113(43): 12322-12327. doi: 10.1073/pnas.1606685113
Guadagno, C. R., Beverly, D. P. and Ewers, B. E. (2021): The love-hate relationship between chlorophyll a and water in PSII affects fluorescence products. Photosynthetica, 59(SI): 409-421. doi: 10.32615/ps.2021.023
Guidici, G. N. M. (2021): Combined chlorophyll fluorescence techniques to study environmental impact on the mountain moss Polytrichum commune. Czech Polar Reports, 11(1): 161-173.
Gupta, A., Bharati, R., Kubes, J., Popelkova, D., Praus, L., Yang, X., Severova, L., Skalicky, M. and Brestic, M. (2024): Zinc oxide nanoparticles application alleviates salinity stress by modulating plant growth, biochemical attributes and nutrient homeostasis in Phaseolus vulgaris L. Frontiers in Plant Science, 15: 1432258. doi: 10.3389/fpls.2024.1432258
Hájek, J., Hojdová, A., Trnková, K., Váczi, P., Bednaříková, M. and Barták, M. (2021): Responses of thallus anatomy and chlorophyll fluorescence-based photosynthetic characteristics of two Antarctic species of genus Usnea to low temperature. Photosynthetica, 59(1): 95-105.
Hájek, J., Puhovkin, A., Giordano, D. and Sekerák, J. (2022): What does critical temperature tell us about the resistance of polar lichens to freezing stress? Applicability of linear cooling method to ecophysiological studies. Czech Polar Reports, 12(2): 246-255. doi: 10.5817/ CPR2022-2-18
Harańczyk, H., Strzałka, K., Kubat, K., Andrzejowska, A., Olech, M., Jakubiec, D., Kijak, P., Palfner, G. and Casanova-Katny, A. (2021): A comparative analysis of gaseous phase hydration properties of two lichenized fungi: Niebla tigrina (Follman) Rundel & Bowler from Atacama Desert and Umbilicaria antarctica Frey & I. M. Lamb from Robert Island, Southern Shetlands Archipelago, maritime Antarctica. Extremophiles: life under extreme conditions, 25(3): 267-283. doi: 10.1007/s00792-021-01227-y
Hovenden, M., Jackson, A. E. and Seppelt, R.D. (1994): Field photosynthetic activity of lichens from the Windmill Island oasis, Wilkies land, Continental Antarctica. Physiologia Plantarum, 90: 567-576.
Hüner, N. P. A., Ivanov, A. G., Szyszka-Mroz, B., Savitch, L. V., Smith, D. R. and Kata, V. (2024): Photostasis and photosynthetic adaptation to polar life. Photosynthesis Research, 161(1-2): 51-64. doi: 10.1007/s11120-024-01104-7
Hussain, M. A., Li, S., Gao, H., Feng, C., Sun, P., Sui, X., Jing, Y., Xu, K., Zhou, Y., Zhang, W., and Li, H. (2023): Comparative analysis of physiological variations and genetic architecture for cold stress response in soybean germplasm. Frontiers in Plant Science, 13: 1095335. doi: 10.3389/fpls.2022.1095335
Ilík, P., Schansker, G., Kotabová, E., Váczi, P., Strasser, R. J. and Barták, M. (2006): A dip in the chlorophyll fluorescence induction at 0.2-2 s in Trebouxia-possessing lichens reflects a fast reoxidation of photosystem I. A comparison with higher plants. Biochimica et Biophysica Acta, 1757(1): 12-20. doi: 10.1016/j.bbabio.2005.11.008
Janeeshma, E., Johnson, R., Amritha, M. S., Noble, L., Aswathi, K. P. R., Telesiński, A., Kalaji, H. M., Auriga, A. and Puthur, J. T. (2022): Modulations in chlorophyll a fluorescence based on intensity and spectral variations of light. International Journal of Molecular Sciences, 23(10): 5599. doi: 10.3390/ijms23105599
Kappen, L., Redon, J. (1987): Photosynthesis and water relations of three maritime antarctic lichen species. Flora, 179(3): 215-229. doi: 10.1016/S0367-2530(17)30240-2
Kubo, S., Masumura, T., Saito, Y., Fukayama, H., Suzuki, Y., Sugimoto, T., Makino, A., Amako, K. and Miyake, C. (2011): Cyclic electron flow around PSI functions in the photoinhibited rice leaves. Soil Science and Plant Nutrition, 57(1): 105-113. doi: 10.1080/00380768.2011.553803
Li, K., Ji, L., Xing, Y., Zuo, Z. and Zhang, L. (2023): Data-independent acquisition proteomics reveals the effects of red and blue light on the growth and development of moso bamboo (Phyllostachys edulis) seedlings. International Journal of Molecular Sciences, 24(6): 5103. doi: 10.3390/ijms24065103
Marečková, M., Barták, M. and Hájek, J. (2019): Temperature effects on photosynthetic performance of Antarctic lichen Dermatocarpon polyphyllizum: A chlorophyll fluorescence study. Polar Biology, 42: 685-701. doi: 10.1007/s00300-019-02464-w
Marín, C., Barták, M., Palfner, G., Vergara-Barros, P., Fernandoy, F., Hájek, J. and Casanova-Katny, A. (2022): Antarctic lichens under long-term passive warming: Species-specific photochemical responses to desiccation and heat shock treatments. Plants (Basel, Switzerland), 11(19): 2463.
Mi, H., Klughammer, C. and Schreiber, U. (2000): Light-induced dynamic changes of NADPH fluorescence in Synechocystis PCC 6803 and its ndhB-defective mutant M55. Plant & Cell Physiology, 41(10): 1129-1135. doi: 10.1093/pcp/pcd038
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. 10.5817/CPR2015-1-10
Miyake C. (2020): Molecular mechanism of oxidation of P700 and suppression of ROS production in photosystem i in response to electron-sink limitations in C3 plants. Antioxidants (Basel, Switzerland), 9(3): 230. doi: 10.3390/antiox9030230
Moon, B. Y., Higashi, S., Gombos, Z. and Murata, N. (1995): Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. Proceedings of the National Academy of Sciences of the United States of America, 92(14): 6219-6223. doi: 10.1073/pnas.92.14.6219
Nepal, N., Yactayo-Chang, J. P., Gable, R., Wilkie, A., Martin, J., Aniemena, C. L., Gaxiola, R. and Lorence, A. (2020): Phenotypic characterization of Arabidopsis thaliana lines overexpressing AVP1 and MIOX4 in response to abiotic stresses. Applications in Plant Sciences, 8(8): e11384. doi: 10.1002/aps3.11384
Ogbaga, C. C., Athar, H.U.R. (2019): Inclusion of photoprotective parameters in photosynthesis-measuring systems to improve the interpretation of photosynthesis and productivity. Photosynthetica, 57(2): 712-713. doi: 10.32615/ps.2019.041
Orekhova, A., Barták, M., Casanova-Katny, A. and Hájek, J. (2021): Resistance of Antarctic moss Sanionia uncinata to photoinhibition: Chlorophyll fluorescence analysis of samples from the western and eastern coasts of the Antarctic Peninsula. Plant Biology (Stuttgart, Germany), 23(4): 653-663. doi: 10.1111/plb.13270
Ott, S. (2004): Early stages of development in Usnea antarctica Du Rietz in the South Shetland Islands, northern maritime Antarctica. The Lichenologist, 36(6): 413-423. doi: 10.1017/ S0024282904014380
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. and 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. doi: 10.3389/ fpls.2020.01178
Reiter, R., Green, A. T. G., Schroeter, B. and Türk, R. (2007): Photosynthesis of three Umbilicaria species from lichen dominated communities of the alpine/nival belt of the Alps measured under controlled conditions. Phyton, 46(2): 247-258.
Sancho, L., de los Ríos, A., Pintado, A., Colesie, C., Raggio, J., Ascaso, C. and Green, A. (2020): Himantormia lugubris, an Antarctic endemic on the edge of the lichen symbiosis. Symbiosis, 82(1, SI): 49-58. doi: 10.1007/s13199-020-00723-7
Sejima, T., Takagi, D., Fukayama, H., Makino, A. and Miyake, C. (2014): Repetitive short-pulse light mainly inactivates photosystem I in sunflower leaves. Plant & Cell Physiology, 55(6): 1184-1193. doi: 10.1093/pcp/pcu061
Shimakawa, G., Miyake, C. (2018): Oxidation of P700 ensures robust photosynthesis. Frontiers in Plant Science, 9: 1617. doi: 10.3389/fpls.2018.01617
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 Antartica. New Phytologist, 131: 275-285. doi: 10.1111/j.1469-8137.1995.tb05729.x
Schroeter, B., Green, T. G., Pintado, A., Türk, R. and Sancho, L. G. (2021): Summer activity patterns for a moss and lichen in the maritime Antarctic with respect to altitude. Polar Biology, 44(11): 2117-2137. doi: 10.1007/s00300-021-02939-9
Sojo, F., Romeike, J. and Ott, S. (2003): Himantormia lugubris (Hue) M. Lamb – vegetative and reproductive habit: Adaptations of an Antarctic endemic. Flora, 198: 118-126.
Sonoike, K. (1996): Photoinhibition of Photosystem I: Its physiological significance in the chilling sensitivity of plants. Plant and Cell Physiology, 37(3): 239-247.
Storti, M., Puggioni, M. P., Segalla, A., Morosinotto, T. and Alboresi, A. (2020): The chloroplast NADH dehydrogenase-like complex influences the photosynthetic activity of the moss Physcomitrella patens. Journal of Experimental Botany, 71(18): 5538-5548. doi: 10.1093/ jxb/eraa274
Strasser, R. J., Srivastava, A. and Tsimilli-Michael, M. (2000): The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: M. Yunus, U. Pathre, P. Mohanty (eds.): Probing Photosynthesis: Mechanism, Regulation and Adaptation. Taylor and Francis, UK, Chapter 25, pp. 445–483.
Sunoj, V.S.J., Wen, Y., Jajoo, A., Short, A.W., Zeng, W.H., Elsheery, N.I. and Cao, K.F. (2023): Moderate photoinhibition of PSII and oxidation of P700 contribute to chilling tolerance of tropical tree species in subtropics of China. Photosynthetica, 61(SPECIAL ISSUE 2023/1): 177-189. doi: 10.32615/ps.2022.039
Terashima, I., Funayama, S. and Sonoike, K. (1994): The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II. Planta, 193: 300-306. doi: 10.1007/BF00192544
Tietz, S., Hall, C. C., Cruz, J. A. and Kramer, D. M. (2017): NPQ(T): A chlorophyll fluorescence parameter for rapid estimation and imaging of non-photochemical quenching of excitons in photosystem-II-associated antenna complexes. Plant, Cell & Environment, 40(8): 1243-1255. doi: 10.1111/pce.12924
Virtanen, O., Khorobrykh, S. and Tyystjärvi, E. (2021): Acclimation of Chlamydomonas reinhardtii to extremely strong light. Photosynthesis Research, 147(1): 91-106. doi: 10.1007/ s11120-020-00802-2
Woodford, R., Watkins, J., Moore, M., Nix, S., Yee, S., Chan, K. X., Pogson, B., Caemmerer, S., Furbank, R. and Ermakova, M. (2024/2025 – preprint): PGR5 promotes energy-dependent non-photochemical quenching to enable efficient C4 photosynthesis under fluctuating light. bioRxiv. doi: 10.1101/2024.09.15.613160; https://www.biorxiv.org/content/10.1101/2024.09. 15.613160v1.full
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