Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-27T15:25:23.321Z Has data issue: false hasContentIssue false
  • English
  • Français

Effects of UVC254 nm on the photosynthetic activity of photobionts from the astrobiologically relevant lichens Buellia frigida and Circinaria gyrosa

Published online by Cambridge University Press:  06 October 2014

J. Meeßen ,
T. Backhaus ,
A. Sadowsky ,
M. Mrkalj ,
F.J. Sánchez ,
R. de la Torre  and
S. Ott
J. Meeßen*
Affiliation:
Institut für Botanik, Heinrich-Heine Universität (HHU), Universitätsstr.1, 40225 Düsseldorf, Germany
T. Backhaus
Affiliation:
Institut für Botanik, Heinrich-Heine Universität (HHU), Universitätsstr.1, 40225 Düsseldorf, Germany
A. Sadowsky
Affiliation:
Institut für Botanik, Heinrich-Heine Universität (HHU), Universitätsstr.1, 40225 Düsseldorf, Germany
M. Mrkalj
Affiliation:
Institut für Botanik, Heinrich-Heine Universität (HHU), Universitätsstr.1, 40225 Düsseldorf, Germany
F.J. Sánchez
Affiliation:
Instituto Nacional de Técnica Aeroespacial (INTA), Ctra. de Ajalvir km. 4, 28850 Torrejón de Ardoz, Madrid, Spain
R. de la Torre
Affiliation:
Instituto Nacional de Técnica Aeroespacial (INTA), Ctra. de Ajalvir km. 4, 28850 Torrejón de Ardoz, Madrid, Spain
S. Ott
Affiliation:
Institut für Botanik, Heinrich-Heine Universität (HHU), Universitätsstr.1, 40225 Düsseldorf, Germany
*
e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

In the past decade, various astrobiological studies on different lichen species investigated the impairment of viability and photosynthetic activity by exposure to simulated or real space parameters (as vacuum, polychromatic ultraviolet (UV)-radiation and monochromatic UVC) and consistently found high post-exposure viability as well as low rates of photosynthetic impairment (de Vera et al. 2003, 2004a; 2004b; de la Torre et al. 2010; Onofri et al. 2012; Sánchez et al. 2012, 2014; Brandt et al. 2014). To achieve a better understanding of the basic mechanisms of resistance, the present study subdued isolated and metabolically active photobionts of two astrobiologically relevant lichens to UVC254 nm, examined its effect on photosynthetic activity by chlorophyll a fluorescence and characterized the UVC-induced damages by quantum yield reduction and measurements of non-photochemical quenching. The results indicate a strong impairment of photosynthetic activity, photoprotective mechanisms and overall photobiont vitality when being irradiated in the isolated and metabolically active state. In conclusion, the present study stresses the higher susceptibility of photobionts towards extreme environmental conditions as UVC-exposure, a stressor that does not occur on the Earth. By comparison with previous studies, the present results highlight the importance of protective mechanisms in lichens, such as morphological–anatomical traits (Meeßen et al. 2013), secondary lichen compounds (Meeßen et al. 2014) and the symbiont's pivotal ability to pass into anhydrobiosis when desiccating.

Keywords

astrobiologyBIOMEXextremotolerancelichensphotobiontsphotodamageUVC
Type
Research Article
Information
International Journal of Astrobiology , Volume 13 , Issue 4 , October 2014 , pp. 340 - 352
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmadjian, V. (1967). A guide to the algae occurring as lichen symbionts: isolation, culture, cultural physiology, and identification. Phycologia 6, 127–160.CrossRefGoogle Scholar
Aro, E.M., Virgin, I. & Andersson, B. (1993). Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim. Biophys. Acta 1143, 113–134.Google Scholar
Barták, M., Váczi, P. & Smykla, J. (2007). Low-temperature limitation of primary photosynthetic processes in Antarctic lichens Umbilicaria antarctica and Xanthoria elegans . Polar Biol. 31, 47–51.Google Scholar
Brandt, A., de Vera, J.-P., Onofri, S. & Ott, S. (2014). Viability of the lichen Xanthoria elegans and its symbionts after 18 months of space exposure and simulated Mars conditions on the ISS. Int. J. Astrobiol. this issue doi: 10.1017/S1473550414000214.Google Scholar
Britt, A.B. (1999). Molecular genetics of DNA repair in higher plants. Trends Plant Sci. 4, 20–25.Google Scholar
Caldwell, M.M., Björn, L.O., Bornmann, J.F., Flint, S.D., Kulandaivelu, G., Teramura, A.H. & Tevini, M. (1998). Effects of increased solar ultraviolet radiation on terrestrial ecosystems. J. Photochem. Photobiol. B 46, 40–52.Google Scholar
Cockell, C.S. (2014). Trajectories of martian habitability. Astrobiology 14(2), 182–203.Google Scholar
Cockell, C.S., Catling, D., Davis, W.L., Kepner, R.N., Lee, P.C., Snook, K. & McKay, C.P. (2000). The ultraviolet environment of Mars: biological implications past, present, and future. Icarus 146(2), 343–359.CrossRefGoogle ScholarPubMed
Cruces, E., Huovinen, P. & Gómez, I. (2013). Interactive effects of UV radiation and enhanced temperature on photosynthesis, phlorotannin induction and antioxidant activities of two sub-Antarctic brown algae. Marine Biol. 160(1), 1–13.Google Scholar
Day, T.A., Martin, G. & Vogelmann, T.C. (1993). Penetration of UV-B radiation in foliage: evidence that the epidermis behaves as a non-uniform filter. Plant Cell Environ. 16(6), 735–741.Google Scholar
de la Torre, R., Sancho, L.G., Pintado, A., Rettberg, P., Rabbow, E., Panitz, C., Deutschmann, U., Reina, M. & Horneck, G. (2007). BIOPAN experiment LICHENS on the Foton M2 mission: pre-flight verification tests of the Rhizocarpon geographicum-granite ecosystem. Adv. Space Res. 40(11), 1665–1671.Google Scholar
de la Torre, R. et al. (2010). Survival of lichens and bacteria exposed to outer space conditions – results of the Lithopanspermia experiments. Icarus 208(2), 735–748.Google Scholar
Demming-Adams, B. & Adams, W.W. III (1996). The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sc. 1(1), 21–26.Google Scholar
Demmig-Adams, B. & Adams, W.W. III (2006). Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol. 172(1), 11–21.Google Scholar
de Vera, J.P. (2005). Grenzen des Überlebens: Flechten als Modellorganismen für das Potential von Adaptationsmechanismen unter Extrembedingungen. Dissertation at the Heinrich-Heine University, ULB Düsseldorf, pp. 1–180.Google Scholar
de Vera, J.P. & Ott, S. (2010). Resistance of symbiotic eukaryotes. Survival to simulated space conditions and asteroid impact cataclysms. In Joint ventures in biology. Cellular origin, life in extreme habitats and astrobiology, ed. Seckbach, J. & Grube, M., vol. 17, pp. 595–611. Springer, Netherlands.Google Scholar
de Vera, J.P., Horneck, G., Rettberg, P. & Ott, S. (2003). The potential of the lichen symbiosis to cope with the extreme conditions of outer space I. Influence of UV radiation and space vacuum on the vitality of lichen symbiosis and germination capacity. Int. J. Astrobiol. 1, 285–293.Google Scholar
de Vera, J.P., Horneck, G., Rettberg, P. & Ott, S. (2004 a). The potential of the lichen symbiosis to cope with the extreme conditions of outer space. II: Germination capacity of lichen ascospores in response to simulated space conditions. Adv. Space Res. 33, 1236–1243.Google Scholar
de Vera, J.P., Horneck, G., Rettberg, P. & Ott, S. (2004 b). In the context of panspermia: may lichens serve as shuttles for their bionts in space? In Proc. of the third European Workshop on Astrobiology. ESA SP-545, ESA Publications Division, ESTEC, Noordwijk, pp. 197–198.Google Scholar
de Vera, J.P., Rettberg, P. & Ott, S. (2008). Life at the limits: capacities of isolated and cultured lichen symbionts to resist extreme environmental stresses. Orig. Life Evol. Biosph. 38, 457–468.Google Scholar
de Vera, J.P., Möhlmann, D., Butina, F., Lorek, A., Wernecke, R. & Ott, S. (2010). Survival potential and photosynthetic activity of lichens under Mars-like conditions: a laboratory study. Astrobiology 10(2), 215–227.Google Scholar
Ertl, L. (1951). Über die Lichtverhältnisse in Laubflechten. Planta 39, 245–270.Google Scholar
Fernández-Marín, B., Becerril, J.M. & García-Plazaola, J.I. (2010). Unravelling the roles of desiccation-induced xanthophyll cycle activity in darkness: a case study in Lobaria pulmonaria . Planta 231, 1335–1342.Google Scholar
Hanelt, D., Wienke, C. & Nultsch, W. (1997). Influence of UV-radiation on the photosynthesis of Arctic macroalgae in the field. J. Photochem. Photobiol. B: Biol. 38, 40–47.Google Scholar
Hollósy, F. (2002). Effects of ultraviolet radiation on plant cells. Micron 33, 179–197.Google Scholar
Horneck, G. (1999). European activities in exobiology in earth orbit: results and perspectives. Adv. Space Res. 23(2), 381–386.Google Scholar
Horneck, G., Baumstark-Khan, C. & Facius, R. (2006). Radiation biology. In Fundamentals of Space Biology. Space Technology Library, ed. Clément, G. & Slenska, K., vol. 18, pp. 291–336. Springer, New York.Google Scholar
Horneck, G., Stöffler, D., Ott, S., Hornemann, U., Cockell, C.S., Moeller, R., Meyer, C., de Vera, J.P., Fritz, J., Schade, S. & Artemieva, N.A. (2008). Microbial rock inhabitants survive hypervelocity impacts on Mars-like host planets: first phase of lithopanspermia experimentally tested. Astrobiology 8(1), 17–44.Google Scholar
Jahns, P. & Holzwarth, A.R. (2012). The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim. Biophys. Acta – Bioenergetics 1817(1), 182–193.CrossRefGoogle ScholarPubMed
Jansen, M.A.K., Babu, T.S., Heller, D., Gaba, V., Mattoo, A.K. & Edelman, M. (1996 a). Ultraviolet-B effects on Spirodela oligorhiza: induction of different protection mechanisms. Plant. Sci. 115, 217–223.CrossRefGoogle Scholar
Jansen, M.A.K., Gaba, V., Greenberg, B.M., Mattoo, A.K. & Edelmann, M. (1996 b). Low threshold levels of ultraviolet-B in a background of photosynthetically active radiation trigger rapid degradation of the D2 protein of photosystem-II. Plant J. 9(5), 693–699.Google Scholar
Jansen, M.A.K., Gaba, V. & Greenberg, B.M. (1998). Higher plants and UV-B radiation: balancing damage, repair and acclimation. Trends Plant Sci. 3(4), 131–135.Google Scholar
Jenkins, G.I., Christie, J.M., Fuglevand, G., Long, J.C. & Jackson, J.A. (1995). Plant responses to UV and blue light: biochemical and genetic approaches. Plant Sci. 112, 117–138.Google Scholar
Joshi, P.N., Ramaswamy, N.K., Iyer, R.K., Nair, J.S., Pradhan, M.K., Gartia, S., Biswal, B. & Biswal, U.C. (2007). Partial protection of photosynthetic apparatus from UV-B-induced damage by UV-A radiation. Env. Exp. Bot. 59, 166–172.Google Scholar
Kappen, L. (1988). Ecophysiological relationships in different climatic regions. In CRC Handbook of Lichenology, ed. Galun, M., vol. II, pp. 37–99. CRC Press, Boca Ranton.Google Scholar
Kappen, L. (1993). Plant activity under snow and ice, with particular reference to lichens. Arctic 46(4), 297–302.Google Scholar
Kovács, E. & Keresztes, Á. (2002). Effect of gamma and UV-B/C radiation on plant cells. Micron 33(2), 199–210.Google Scholar
Kranner, I. & Birtić, S. (2005). A modulating role for antioxidants in desiccation tolerance. Integr. Comp. Biol. 45(5), 734–740.Google Scholar
Kranner, I., Cram, W.J., Zorn, M., Wornik, S., Yoshimura, I., Stabentheiner, E. & Pfeifhofer, H.W. (2005). Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proc. Natl. Acad. Sci. USA 102(8), 3141–3146.Google Scholar
Kranner, I., Beckett, R., Hochman, A. & Nash, T.H. III (2008). Desiccation-tolerance in lichens: a review. Bryologist 111(4), 576–593.CrossRefGoogle Scholar
Krause, G.H. & Jahns, P. (2004). Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: characterization and function. In Chlorophyll a Fluorescence, ed. Papageorgioument, G.C. & Govindjee, G., pp. 463–495. Springer, Netherlands.Google Scholar
Kulandaivelu, G., Noorudeen, A.M. (1983). Comparative study of the action of UV-C and UV-B radiation on photosynthetic electron transport. Physiol. Plant 58, 389–394.Google Scholar
Lange, O.L. (1992). Pflanzenleben Unter Stress, pp. 213–217. Echter Würzburg Fränkische Gesellschaftsdruckerei und Verlag, Würzburg.Google Scholar
Lange, O.L., Green, T.G.A. & Reichenberger, H. (1999). The response of lichen photosynthesis to external CO2 concentration and its interaction with thallus water-status. J. Plant Physiol. 154, 157–166.Google Scholar
Lüttge, U. & Büdel, B. (2010). Resurection kinetics of photosynthesis in desiccation-tolerant terrestrial green-algae (Chlorophyta) on tree bark. Plant Biol. 12, 437–444.CrossRefGoogle ScholarPubMed
Lytvyn, D.I., Yemets, A.I. & Blume, Y.B. (2010). UV-B exposure induces programmed cell death in a BY-2 tobacco cell line. Env. Exp. Bot. 68, 51–57.Google Scholar
Maxwell, K. & Johnson, G.N. (2000). Chlorophyll fluorescence – a practical guide. J. Exp. Bot. 51, 659–668.Google Scholar
McEvoy, M., Nybakken, L., Solhaug, K.A. & Gauslaa, Y. (2006). UV triggers the synthesis of the widely distributed secondary lichen compound usnic acid. Mycol. Prog. 5, 221–229.CrossRefGoogle Scholar
McKay, C.P., Friedmann, E.I., Gomez-Silva, B., Caceres-Villanueva, L., Andersen, D.T. & Landheim, R. (2003). Temperature and moisture conditions for life in the extreme arid region of the Atacama Desert: four years of observations including the El Nino of 1997–1998. Astrobiology 3(2), 393–406.Google Scholar
Meeßen, J., Sánchez, F.J., Brandt, A., Balzer, E.M., de la Torre, R., Sancho, L.G., de Vera, J.P. & Ott, S. (2013). Extremotolerance and resistance of lichens: comparative studies on five species used in astrobiological research I. Morphological and anatomical characteristics. Orig. Life Evol. Biosph. 43(3), 283–303.Google Scholar
Meeßen, J., Sánchez, F.J., Sadowsky, A., de la Torre, R., Ott, S. & de Vera, J.P. (2014). Extremotolerance and resistance of lichens: comparative studies on five species used in astrobiological research. II. Secondary lichen compounds. Orig. Life Evol. Biosph. 43(4), 501–526.Google Scholar
Nasibi, F. & M'Kalantari, K.H. (2005). The effects of UV-A, UV-B and UV-C on protein and ascorbate content, lipid peroxidation and biosynthesis of screening compounds in Brassica napus . Iranian J. Sci. Technol., Trans. A 29(A1), 39–48.Google Scholar
Nicholson, W.L., Schuerger, A.C. & Setlow, P. (2005). The solar UV environment and bacterial spore UV resistance: considerations for Earth-to-Mars transport by natural processes and human spaceflight. Mutat. Res. 571, 249–264.Google Scholar
Nogués, S. & Baker, N.R. (1995). Evaluation of the role of damage to photosystem II in the inhibition of CO2 assimilation in pea leaves on exposure to UV-B radiation. Plant Cell Environ. 18, 781–787.Google Scholar
Nybakken, L., Solhaug, K.A., Bilger, W. & Gauslaa, Y. (2004). The lichens Xanthoria elegans and Cetraria islandica maintain a high protection against UV-B radiation in Arctic habitats. Oecologia 140, 211–216.Google Scholar
Onofri, S., Selbmann, L., de Hoog, G.S., Grube, M., Barreca, D., Ruisi, S. & Zucconi, L. (2007). Evolution and adaptation of fungi at boundaries of life. Adv. Space Res. 40(11), 1657–1664.Google Scholar
Onofri, S. et al. (2012). Survival of rock-colonizing organisms after 1.5 years in outer space. Astrobiology 12(5), 508–516.Google Scholar
Øvstedal, D.O. & Lewis Smith, R.I. (2001). Lichens of Antarctica and South Georgia. A Guide to their Identification and Ecology, pp. 66–365. Cambridge University Press, Cambridge.Google Scholar
Pfündel, E.E., Pan, R.S. & Dilley, R.A. (1992). Inhibition of violaxanthin deepoxidation by ultraviolet-B radiation in isolated chloroplasts and intact leaves. Plant Physiol. 98, 1372–1380.Google Scholar
Raggio, J., Pintado, A., Ascaso, C., de la Torre, R., de los Ríos, A., Wierzchos, J., Horneck, G. & Sancho, L.G. (2011). Whole lichen thalli survive exposure to space conditions: results of lithopanspermia experiment with Aspicilia fruticulosa . Astrobiology 11(4), 281–292.Google Scholar
Rahimzadeh, P., Hosseini, S. & Dilmaghani, K. (2011). Effects of UV-A and UV-C radiation on some morphological and physiological parameters in savory (Satureja hortensis L.). Ann. Biol. Res. 2(59), 164–171.Google Scholar
Rao, M.V., Paliyath, G. & Ormrod, D.P. (1996). Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana . Plant Physiol. 110, 125–136.Google Scholar
Richter, M., Rühle, W. & Wild, A. (1990). Studies on the mechanism of Photosystem II photoinhibition. I. A two-step degradation of D1-protein. Photosynthesis Res. 24(3), 229–235.Google Scholar
Roháček, K. (2002). Chlorophyll fluorescence parameters: the definitions, photosynthetic meaning, and mutual relationships. Photosynthetica 40(1), 13–29.Google Scholar
Romeike, J., Friedl, T., Helms, G. & Ott, S. (2002). Genetic diversity of algal and fungal partners in four species of Umbilicaria (lichenized Ascomycetes) along a transect of the Antarctic Peninsula. Mol. Biol. Evol. 19(8), 1209–1217.Google Scholar
Rozema, J., van de Staaij, J., Björn, L.O. & Caldwell, M. (1997). UV-B as an environmental factor in plant life: stress and regulation. TREE 12(1), 22–28.Google Scholar
Sadowsky, A. & Ott, S. (2012). Photosynthetic symbionts in Antarctic terrestrial ecosystems: the physiological response of lichen photobionts to drought and cold. Symbiosis 58, 81–90.Google Scholar
Sánchez, F.J., Mateo-Martí, E., Raggio, J., Meeßen, J., Martínez-Frías, J., Sancho, L.G., Ott, S. & de la Torre, R. (2012). The resistance of the lichen Circinaria gyrosa (nom. provis.) towards simulated Mars conditions – a model test for the survival capacity of an eukaryotic extremophile. Planet. Space Sci. 72(1), 102–110.Google Scholar
Sánchez, F.J., Meeßen, J., Ruiz, M., Sancho, L.G., Ott, S., Vílchez, C., Horneck, G., Sadowsky, A. & de la Torre, R. (2014). UV-C tolerance of symbiotic Trebouxia sp. in the space-tested lichen species Rhizocarpon geographicum and Circinaria gyrosa: role of the hydration state and cortex/screening substances. Int. J. Astrobiol. 13(1), 1–18.Google Scholar
Sancho, L.G., Schroeter, B. & del Prado, R. (2000). Ecophysiology and morphology of the globular erratic lichen Aspicilia fruticulosa (Eversm.) Flag. from Central Spain. Bibl. Lichenol. 75, 137–147.Google Scholar
Sancho, L.G., de la Torre, R., Horneck, G., Ascaso, C., de los Ríos, A., Pintado, A., Wierzchos, J. & Schuster, M. (2007). Lichens survive in space: results from 2005 LICHENS experiment. Astrobiology 7(3), 443–454.Google Scholar
Sancho, L.G., de la Torre, R. & Pintado, A. (2008). Lichens, new and promising material from experiments in astrobiology. Fungal Biol. Rev. 22, 103–109.Google Scholar
Sass, L., Spetea, C., Máté, Z., Nagy, F. & Vass, I. (1997). Repair of UV-B induced damage of Photosystem II via de novo synthesis of D1 and D2 reaction centre subunits in Synechocystis sp. PCC 6803. Photosynthesis Res. 54(1), 55–62.Google Scholar
Scalzi, G., Selbmann, L., Zucconi, L., Rabbow, E., Horneck, G., Albertano, P. & Onofri, S. (2012). The LIFE Experiment: isolation of cryptoendolithic organisms from Antarctic colonized sandstone exposed to space and simulated Mars conditions on the International Space Station. Orig. Life Evol. Biosph. 42, 253–262.Google Scholar
Schmitz-Hoerner, R. & Weissenböck, G. (2003). Contribution of phenolic compounds to the UV-B screening capacity of developing barley primary leaves in relation to DNA damage and repair under elevated UV-B levels. Phytochemistry 64, 243–255.Google Scholar
Schreiber, U., Bilger, W. & Neubauer, C. (1994). Chlorophyll fluorescence as a non-intrusive indicator for rapid assessment of in vivo photosynthesis. Ecol. Stud. 100, 49–70.Google Scholar
Sohrabi, M. (2012). Taxonomy and phylogeny of the manna lichens and allied species (Megasporaceae). PhD Thesis, Publications in Botany from the University of Helsinki. http://urn.fi/URN:ISBN:978-952-10-7400-4 Google Scholar
Solhaug, K.A. & Gauslaa, Y. (2004) Photosynthates stimulate the UV-B induced fungal anthraquinone synthesis in the foliose lichen Xanthoria parietina . Plant. Cell Environ. 27, 167–178.Google Scholar
Stöffler, D., Horneck, G., Ott, S., Hornemann, U., Cockell, C.S., Moeller, R., Meyer, C., de Vera, J.P., Fritz, J. & Artemieva, N.A. (2007). Experimental evidence for the potential impact ejection of viable microorganisms from Mars and Mars-like planets. Icarus 189, 585–588.Google Scholar
Strid, Å., Chow, W.S. & Anderson, J.M. (1994). UV-B damage and protection at the molecular level in plants. Photosynthesis Res. 39(3), 475–489.Google Scholar
Sun, H.J., Nienow, J.A. & McKay, C.P. (2010). The antarctic cryptoendolithic microbial ecosystem. In Life in Antarctic Deserts and other Cold Dry Environments – Astrobiological Analogs, ed. Doran, P.T., Lyons, W.B. & McKnight, D.M., pp. 110–138. Cambridge University Press, Cambridge.Google Scholar
Suzuki, N., Koussevitzki, S., Mittler, R. & Miller, G. (2012). ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ. 35, 259–270.Google Scholar
Takeuchi, Y., Murakami, M., Nakajima, N., Kondo, N. & Nikaido, O. (1996). Induction of repair and damage to DNA in cucumber cotyledons irradiated with UV-B. Plant Cell Physiol. 37(2), 181–187.Google Scholar
Teramura, A.H. & Sullivan, J.H. (1994). Effects of UV-B radiation on photosynthesis and growth of terrestrial plants. Photosynthesis Res. 39, 463–473.Google Scholar
Uchida, Y., Hirayama, J. & Nishina, H. (2010). A common origin: signaling similarities in the regulation of the circadian clock and DNA damage response. Biol. Pharm. Bull 33(4), 535–544.Google Scholar
Vass, I., Sass, L., Spetea, C., Bakou, A., Ghanotakis, D.F. & Petrouleas, V. (1996). UV-B-induced inhibition of photosystem II electron transport studied by EPR and chlorophyll fluorescence. Impairment of donor and acceptor side components. Biochemistry 35, 8964–8973.Google Scholar
Vass, I., Szilárd, A. & Sicora, C. (2005). Adverse effects of UV-B light on the structure and function of the photosynthetic apparatus. In Handbook of Photosynthesis, ed. Pessarakli, M., pp. 931–949. Marcel Dekker, Inc., New York.Google Scholar
Yao, Y., Danna, C.H., Zemp, F.J., Titov, V., Ciftci, O.N., Przybylski, R., Ausubel, F.M. & Kovalchuk, I. (2011). UV-C-irradiated Arabidopsis and Tobacco emits volatiles that trigger genomic instability in neighbouring plants. Plant Cell 23, 3842–3852.Google Scholar
Yoshimura, I., Yamamoto, Y., Nakano, T. & Finnie, J. (2002). Isolation and culture of lichen photobionts and mycobionts. In Protocols in Lichenology. Culturing, Biochemistry, Ecophysiology and Use in Biomonitoring, ed. Krammer, I., Beckett, R. & Varma, A., pp. 3–33. Springer, Berlin.Google Scholar