Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-23T03:27:18.988Z Has data issue: false hasContentIssue false

Photoprotection in lichens: adaptations of photobionts to high light

Published online by Cambridge University Press:  12 March 2021

Richard Peter Beckett*
Affiliation:
School of Life Sciences, University of KwaZulu-Natal, Private Bag X01, Scottsville3209, South Africa Open Lab ‘Biomarker’, Kazan (Volga Region) Federal University, Kremlevskaya str. 18, Kazan420008, Russia
Farida Minibayeva
Affiliation:
Kazan Institute of Biochemistry and Biophysics, Federal Research Center ‘Kazan Scientific Center of RAS’, P.O. Box 261, Kazan420111, Russia
Knut Asbjørn Solhaug
Affiliation:
Faculty of Environmental Sciences and Natural Resource Management, Norwegian University of Life Sciences, P.O. Box 5003, 1432 Ås, Norway
Thomas Roach
Affiliation:
Department of Botany, University of Innsbruck, Sternwartestrasse 15, Innsbruck6020, Austria
*
Author for correspondence: Richard Peter Beckett. E-mail: [email protected]

Abstract

Lichens often grow in microhabitats where they are exposed to severe abiotic stresses such as desiccation and temperature extremes. They are also often exposed to levels of light that are greater than lichen photobionts can use in carbon fixation. Unless regulated, excess energy absorbed by the photobionts can convert ground state oxygen to reactive oxygen species (ROS). These ROS can attack the photosynthetic apparatus, causing photoinhibition and photo-oxidative stress, reducing the ability of the photobionts to fix carbon. Here, we outline our current understanding of the effects of high light on lichens and the mechanisms they use to mitigate or tolerate this stress in hydrated and desiccated states. Tolerance to high light can be achieved first by lowering ROS formation, via synthesizing light screening pigments or by thermally dissipating the excess light energy absorbed; second, by scavenging ROS once formed; or third, by repairing ROS-induced damage. While the primary focus of this review is tolerance to high light in lichen photobionts, our knowledge is rather fragmentary, and therefore we also include recent findings in free-living relatives to stimulate new lines of research in the study of high light tolerance in lichens.

Type
Reviews
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the British Lichen Society

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 (1995) Lichens are more important than you think. Bioscience 45, 124.CrossRefGoogle Scholar
Allorent, G, Tokutsu, R, Roach, T, Peers, G, Cardol, P, Girard-Bascou, J, Seigneurin-Berny, D, Petroutsos, D, Kuntz, M, Breyton, C, et al. (2013) A dual strategy to cope with high light in Chlamydomonas reinhardtii. Plant Cell 25, 545557.CrossRefGoogle ScholarPubMed
Barták, M, Solhaug, KA, Vráblíková, H and Gauslaa, Y (2006) Curling during desiccation protects the foliose lichen Lobaria pulmonaria against photoinhibition. Oecologia 149, 553560.CrossRefGoogle ScholarPubMed
Beckett, RP, Kranner, I and Minibayeva, F (2008) Stress physiology and the symbiosis. In Nash, TH III (ed.), Lichen Biology, 2nd edition. Cambridge: Cambridge University Press, pp. 134151.CrossRefGoogle Scholar
Bergner, SV, Scholz, M, Trompelt, K, Barth, J, Gabelein, P, Steinbeck, J, Xue, HD, Clowez, S, Fucile, G, Goldschmidt-Clermont, M, et al. (2015) STATE TRANSITION7-dependent phosphorylation is modulated by changing environmental conditions, and its absence triggers remodeling of photosynthetic protein complexes. Plant Physiology 168, 615634.CrossRefGoogle ScholarPubMed
Boulay, C, Abasova, L, Six, C, Vass, I and Kirilovsky, D (2008) Occurrence and function of the orange carotenoid protein in photoprotective mechanisms in various cyanobacteria. Biochimica et Biophysica Acta 1777, 13441354.CrossRefGoogle ScholarPubMed
Brandt, A, de Vera, J-P, Onofri, S and Ott, S (2015) Viability of the lichen Xanthoria elegans and its symbionts after 18 months of space exposure and simulated Mars conditions on the ISS. International Journal of Astrobiology 14, 411425.CrossRefGoogle Scholar
Büchel, C (2015) Evolution and function of light harvesting proteins. Journal of Plant Physiology 172, 6275.CrossRefGoogle ScholarPubMed
Büdel, B and Scheidegger, C (2008) Thallus morphology and anatomy. In Nash, TH III (ed.), Lichen Biology, 2nd edition. Cambridge: Cambridge University Press, pp. 4068.CrossRefGoogle Scholar
Büdel, B, Karsten, U and Garcia-Pichel, F (1997) Ultraviolet absorbing scytonemin and mycosporine-like amino acid derivates in exposed rock-inhabiting cyanobacterial lichens. Oecologia 112, 165172.Google Scholar
Buffoni Hall, RS, Paulsson, M, Duncan, K, Tobin, AK, Widell, S and Bornman, JF (2003) Water- and temperature-dependence of DNA damage and repair in the fruticose lichen Cladonia arbuscula ssp. mitis exposed to UV-B radiation. Physiologia Plantarum 118, 371379.CrossRefGoogle Scholar
Calatayud, A, Deltoro, VI, Barreno, E and del Valle-Tascon, S (1997) Changes in in vivo chlorophyll fluorescence quenching in lichen thalli as a function of water content and suggestion of zeaxanthin-associated photoprotection. Physiologia Plantarum 101, 93102.CrossRefGoogle Scholar
Calzadilla, PI, Zhan, J, Sétif, P, Lemaire, C, Solymosi, D, Battchikova, N, Wang, Q and Kirilovsky, D (2019) The cytochrome b 6f complex is not involved in cyanobacterial state transitions. Plant Cell 31, 911931.CrossRefGoogle Scholar
Carniel, FC, Zanelli, D, Bertuzzi, S and Tretiach, M (2015) Desiccation tolerance and lichenization: a case study with the aeroterrestrial microalga Trebouxia sp. (Chlorophyta). Planta 242, 493505.CrossRefGoogle Scholar
Challabathula, D, Zhang, QW and Bartels, D (2018) Protection of photosynthesis in desiccation-tolerant resurrection plants. Journal of Plant Physiology 227, 8492.CrossRefGoogle ScholarPubMed
Cho, SM, Lee, H, Hong, SG 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 9, 85.CrossRefGoogle ScholarPubMed
Cowan, IR, Lange, OL and Green, TGA (1992) Carbon-dioxide exchange in lichens: determination of transport and carboxylation characteristics. Planta 187, 282294.CrossRefGoogle ScholarPubMed
Coxson, DS and Coyle, M (2003) Niche partitioning and photosynthetic response of alectorioid lichens from subalpine spruce-fir forest in north-central British Columbia, Canada: the role of canopy microclimate gradients. Lichenologist 35, 157175.CrossRefGoogle Scholar
Coxson, DS and Stevenson, SK (2007) Influence of high-contrast and low-contrast forest edges on growth rates of Lobaria pulmonaria in the inland rainforest, British Columbia. Forest Ecology and Management 253, 103111.CrossRefGoogle Scholar
Davletova, S, Rizhsky, L, Liang, H, Shengqiang, Z, Oliver, DJ, Coutu, J, Shulaev, V, Schlauch, K, Mittler, R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17, 268281.CrossRefGoogle ScholarPubMed
Demmig-Adams, B, Adams, WW III, Czygan, F-C, Schreiber, U and Lange, OL (1990) Differences in the capacity for radiationless energy dissipation in the photochemical apparatus of green and blue-green algal lichens associated with differences in carotenoid composition. Planta 180, 582589.CrossRefGoogle ScholarPubMed
Demmig-Adams, B, Cohu, CM, Muller, O and Adams, WW III (2012) Modulation of photosynthetic energy conversion efficiency in nature: from seconds to seasons. Photosynthesis Research 113, 7588.CrossRefGoogle ScholarPubMed
Derks, A, Schaven, K and Bruce, D (2015) Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. Biochimica et Biophysica Acta 1847, 468485.CrossRefGoogle ScholarPubMed
Dietz, S, Büdel, B, Lange, OL and Bilger, W (2000) Transmittance of light through the cortex of lichens from contrasting habitats. Bibliotheca Lichenologica 75, 171182.Google Scholar
Erickson, E, Wakao, S and Niyogi, KK (2015) Light stress and photoprotection in Chlamydomonas reinhardtii. Plant Journal 82, 449465.CrossRefGoogle ScholarPubMed
Ertl, L (1951) Über die Lichtverhältnisse in Laubflechten. Planta 39, 245270.CrossRefGoogle Scholar
Färber, L, Solhaug, KA, Esseen, PA, Bilger, W and Gauslaa, Y (2014) Sunscreening fungal pigments influence the vertical gradient of pendulous lichens in boreal forest canopies. Ecology 95, 14641471.CrossRefGoogle ScholarPubMed
Fernandez-Marin, B, Kranner, I, San Sebastian, M, Artetxe, U, Laza, JM, Vilas, JL, Pritchard, HW, Nadajaran, J, Miguez, F, Becerril, JM, et al. (2013) Evidence for the absence of enzymatic reactions in the glassy state. A case study of xanthophyll cycle pigments in the desiccation-tolerant moss Syntrichia ruralis. Journal of Experimental Botany 64, 30333043.CrossRefGoogle Scholar
Foyer, CH (2018) Reactive oxygen species, oxidative signaling and the regulation of photosynthesis. Environmental and Experimental Botany 154, 134142.Google ScholarPubMed
Franz, S, Ignatz, E, Wenzel, S, Zielosko, H, Putu, EPGN, Maestre-Reyna, M, Tsai, MD, Yamamoto, J, Mittag, M and Essen, LO (2018) Structure of the bifunctional cryptochrome aCRY from Chlamydomonas reinhardtii. Nucleic Acids Research 46, 80108022.CrossRefGoogle ScholarPubMed
Garcia-Pichel, F and Castenholz, RW (1991) Characterization and biological implications of scytonemin, a cyanobacterial sheath pigment. Journal of Phycology 27, 395409.CrossRefGoogle Scholar
Gauslaa, Y (1984) Heat resistance and energy budget in different Scandinavian plants. Holarctic Ecology 7, 178.Google Scholar
Gauslaa, Y and Goward, T (2020) Melanic pigments and canopy-specific elemental concentration shape growth rates of the lichen Lobaria pulmonaria in unmanaged mixed forest. Fungal Ecology 47, 100984.CrossRefGoogle Scholar
Gauslaa, Y and Solhaug, KA (1996) Differences in the susceptibility to light stress between epiphytic lichens of ancient and young boreal forest stands. Functional Ecology 10, 344354.CrossRefGoogle Scholar
Gauslaa, Y and Solhaug, KA (2000) High-light-intensity damage to the foliose lichen Lobaria pulmonaria within a natural forest: the applicability of chlorophyll fluorescence methods. Lichenologist 32, 271289.CrossRefGoogle Scholar
Gauslaa, Y and Solhaug, KA (2001) Fungal melanins as a sun screen for symbiotic green algae in the lichen Lobaria pulmonaria. Oecologia 126, 462471.CrossRefGoogle ScholarPubMed
Gauslaa, Y, Coxson, DS and Solhaug, KA (2012) The paradox of higher light tolerance during desiccation in rare old forest cyanolichens than in more widespread co-occurring chloro- and cephalolichens. New Phytologist 195, 812822.CrossRefGoogle ScholarPubMed
Gauslaa, Y, Alam, MA, Lucas, P-L, Chowdhury, DP and Solhaug, KA (2017) Fungal tissue per se is stronger as a UV-B screen than secondary fungal extrolites in Lobaria pulmonaria. Fungal Ecology 26, 109113.CrossRefGoogle Scholar
Gest, N, Gautier, H and Stevens, R (2013) Ascorbate as seen through plant evolution: the rise of a successful molecule? Journal of Experimental Botany 64, 3353.CrossRefGoogle ScholarPubMed
Girolomoni, L, Cazzaniga, S, Pinnola, A, Perozeni, F, Ballottari, M and Bassi, R (2019) LHCSR3 is a nonphotochemical quencher of both photosystems in Chlamydomonas reinhardtii. Proceedings of the National Academy of Sciences of the United States of America 116, 42124217.CrossRefGoogle ScholarPubMed
Gollan, PJ and Aro, E-M (2020) Photosynthetic signalling during high light stress and recovery: targets and dynamics. Philosophical Transactions of the Royal Society B 375, 20190406.CrossRefGoogle ScholarPubMed
Gorelova, O, Baulina, O, Ismagulova, T, Kokabi, K, Lobakova, E, Selyakh, I, Semenova, L, Chivkunova, O, Karpova, O, Scherbakov, P, et al. (2019) Stress-induced changes in the ultrastructure of the photosynthetic apparatus of green microalgae. Protoplasma 256, 261277.CrossRefGoogle ScholarPubMed
Gostinčar, C, Muggia, L and Grube, M (2012) Polyextremotolerant black fungi: oligotrophism, adaptive potential, and a link to lichen symbioses. Frontiers in Microbiology 3, 390.CrossRefGoogle Scholar
Green, TGA, Büdel, B, Meyer, A, Zellner, H and Lange, OL (1997) Temperate rainforest lichens in New Zealand: light response of photosynthesis. New Zealand Journal of Botany 35, 493504.CrossRefGoogle Scholar
Haghjou, MM, Shariati, M and Smirnoff, N (2009) The effect of acute high light and low temperature stresses on the ascorbate-glutathione cycle and superoxide dismutase activity in two Dunaliella salina strains. Physiologia Plantarum 135, 272280.CrossRefGoogle ScholarPubMed
Hasanuzzaman, M, Borhannuddin Bhuyan, MHM, Anee, TI, Parvin, K, Nahar, K, Al Mahmud, J and Fujita, M (2019) Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants 8, 384.CrossRefGoogle ScholarPubMed
Havaux, M, Guedeney, G, Hagemann, M, Yeremenko, N, Matthijs, HCP and Jeanjean, R (2005) The chlorophyll-binding protein IsiA is inducible by high light and protects the cyanobacterium Synechocystis PCC6803 from photooxidative stress. FEBS Letters 579, 22892293.CrossRefGoogle ScholarPubMed
Havurinne, V and Tyystjärvi, E (2020) Photosynthetic sea slugs induce protective changes to the light reactions of the chloroplasts they steal from algae. Elife 9, e57389.CrossRefGoogle ScholarPubMed
Heber, U (2012) Conservation and dissipation of light energy in desiccation-tolerant photoautotrophs, two sides of the same coin. Photosynthesis Research 113, 513.CrossRefGoogle ScholarPubMed
Heber, U, Bilger, W, Bligny, R and Lange, OL (2000) Phototolerance of lichens, mosses and higher plants in an alpine environment: analysis of photoreactions. Planta 211, 770780.CrossRefGoogle Scholar
Heber, U, Bilger, W and Shuvalov, VA (2006) Thermal energy dissipation in reaction centres and in the antenna of photosystem II protects desiccated poikilohydric mosses against photo-oxidation. Journal of Experimental Botany 57, 29933006.CrossRefGoogle ScholarPubMed
Heber, U, Bilger, W, Turk, R and Lange, OL (2010) Photoprotection of reaction centres in photosynthetic organisms: mechanisms of thermal energy dissipation in desiccated thalli of the lichen Lobaria pulmonaria. New Phytologist 185, 459470.CrossRefGoogle ScholarPubMed
Huneck, S and Yoshimura, I (1996) Identification of Lichen Substances. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Huner, NPA, Öquist, G and Sarhan, F (1998) Energy balance and acclimation to light and cold. Trends in Plant Science 3, 224230.CrossRefGoogle Scholar
Jairus, K, Lõhmus, A and Lõhmus, P (2009) Lichen acclimatization on retention trees: a conservation physiology lesson. Journal of Applied Ecology 46, 930936.CrossRefGoogle Scholar
Jeans, J, Campbell, DA and Hoogenboom, MO (2013) Increased reliance upon photosystem II repair following acclimation to high-light by coral-dinoflagellate symbioses. Photosynthesis Research 118, 219229.CrossRefGoogle ScholarPubMed
Kaiser, E, Galvis, VC and Armbruster, U (2019) Efficient photosynthesis in dynamic light environments: a chloroplast's perspective. Biochemical Journal 476, 27252741.CrossRefGoogle ScholarPubMed
Kalaji, HM, Schansker, G, Ladle, RJ, Goltsev, V, Bosa, K, Allakhverdiev, SI, Brestic, M, Bussott, F, Calatayud, A, Dabrowski, P, et al. (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynthesis Research 122, 121158.CrossRefGoogle ScholarPubMed
Kerfeld, CA, Melnicki, MR, Sutter, M and Dominguez-Martin, MA (2017) Structure, function and evolution of the cyanobacterial orange carotenoid protein and its homologs. New Phytologist 215, 937951.CrossRefGoogle ScholarPubMed
Kershaw, KA (1985) Physiological Ecology of Lichens. Cambridge: Cambridge University Press.Google Scholar
Kershaw, KA and MacFarlane, JD (1980) Physiological-environmental interactions in lichens. X. Light as an ecological factor. New Phytologist 84, 687701.CrossRefGoogle Scholar
Kharkongor, D and Ramanujam, P (2015) Spatial and temporal variation of carotenoids in four species of Trentepohlia (Trentepohliales, Chlorophyta). Journal of Botany 2015, 201641.CrossRefGoogle Scholar
Kim, JH, Nemson, JA and Melis, A (1993) Photosystem II reaction center damage and repair in Dunaliella salina (green alga). Analysis under physiological and irradiance-stress conditions. Plant Physiology 103, 181189.CrossRefGoogle ScholarPubMed
Kitajima, S (2008) Hydrogen peroxide-mediated inactivation of two chloroplastic peroxidases, ascorbate peroxidase and 2-cys peroxiredoxin. Journal of Photochemistry and Photobiology B 84, 14041409.CrossRefGoogle ScholarPubMed
Komenda, J and Sobotka, R (2016) Cyanobacterial high-light-inducible proteins — protectors of chlorophyll–protein synthesis and assembly. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1857, 288295.CrossRefGoogle ScholarPubMed
Komura, M, Yamagishia, A, Shibata, Y, Iwasaki, I and Itoha, S (2010) Mechanism of strong quenching of photosystem II chlorophyll fluorescence under drought stress in a lichen, Physciella melanchla, studied by subpicosecond fluorescence spectroscopy. Bioenergetics 1797, 331338.CrossRefGoogle Scholar
Kosanić, M, Ranković, B and Vukojević, J (2011) Antioxidant properties of some lichen species. Journal of Food Science and Technology 48, 584590.CrossRefGoogle ScholarPubMed
Kranner, I (2002) Glutathione status correlates with different degrees of desiccation tolerance in three lichens. New Phytologist 154, 451460.CrossRefGoogle ScholarPubMed
Kranner, I, Zorn, M, Turk, B, Wornik, S, Beckett, RP and Batic, F (2003) Biochemical traits of lichens differing in relative desiccation tolerance. New Phytologist 160, 167176.CrossRefGoogle ScholarPubMed
Kranner, I, Cram, WJ, Zorn, M, Wornik, S, Yoshimura, I, Stabentheiner, E and Pfeifhofer, HW (2005) Antioxidants and photoprotection in a lichen as compared with its isolated symbiotic partners. Proceedings of the National Academy of Sciences of the United States of America 102, 31413146.CrossRefGoogle Scholar
Kromdijk, J, Głowacka, K, Leonelli, L, Gabilly, ST, Iwai, M, Niyogi, KK and Long, SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354, 857861.CrossRefGoogle ScholarPubMed
Lange, OL (2002) Photosynthetic productivity of the epilithic lichen Lecanora muralis: long-term field monitoring of CO2 exchange and its physiological interpretation. I. Dependence of photosynthesis on water content, light, temperature, and CO2 concentration from laboratory measurements. Flora 197, 233249.CrossRefGoogle Scholar
Lange, OL and Green, TGA (2008) Diel and seasonal courses of ambient carbon dioxide concentration and their effect on productivity of the epilithic lichen Lecanora muralis in a temperate, suburban habitat. Lichenologist 40, 449462.CrossRefGoogle Scholar
Leisner, JMR, Green, TGA and Lange, OL (1997) Photobiont activity of a temperate crustose lichen: long-term chlorophyll fluorescence and CO2 exchange measurements in the field. Symbiosis 23, 165182.Google Scholar
Levitt, J (2012) Responses of Plants to Environmental Stresses. Volume I. Chilling, Freezing and High Temperature, 2nd edition. London: Academic Press.Google Scholar
Li, L, Aro, EM and Millar, AH (2018) Mechanisms of photodamage and protein turnover in photoinhibition. Trends in Plant Science 23, 667676.CrossRefGoogle ScholarPubMed
Lin, T, Rao, M, Lu, H, Chiou, C, Lin, S, Chao, H, Zheng, L, Cheng, H and Lee, T (2018) A role for glutathione reductase and glutathione in the tolerance of Chlamydomonas reinhardtii to photo-oxidative stress. Physiologia Plantarum 162, 3548.CrossRefGoogle ScholarPubMed
Liu, J, Lu, Y, Hua, W and Last, RL (2019) A new light on photosystem II maintenance in oxygenic photosynthesis. Frontiers in Plant Science 10, 975.CrossRefGoogle ScholarPubMed
Mafole, TC, Chiang, C, Solhaug, KA and Beckett, RP (2017) Melanisation in the old forest lichen Lobaria pulmonaria (L) Hoffm. reduces the efficiency of photosynthesis. Fungal Ecology 29, 103110.CrossRefGoogle Scholar
Mafole, TC, Solhaug, KA, Minibayeva, FV and Beckett, RP (2019 a) Occurrence and possible roles of melanic pigments in lichenized ascomycetes. Fungal Biology Reviews 33, 159165.CrossRefGoogle Scholar
Mafole, TC, Solhaug, KA, Minibayeva, FV and Beckett, RP (2019 b) Tolerance to photoinhibition within lichen species is higher in melanised thalli. Photosynthetica 57, 96102.CrossRefGoogle Scholar
Marečková, M and Barták, M (2016) Effects of short-term low temperature stress on chlorophyll fluorescence transients in Antarctic lichen species. Czech Polar Reports 6, 5465.CrossRefGoogle Scholar
Maruta, T, Sawa, Y, Shigeoka, S and Ishikawa, T (2016) Diversity and evolution of ascorbate peroxidase functions in chloroplasts: more than just a classical antioxidant enzyme? Plant and Cell Physiology 57, 13771386.Google ScholarPubMed
McEvoy, M, Gauslaa, Y and Solhaug, KA (2007 a) Changes in pools of depsidones and melanins, and their function, during growth and acclimation under contrasting natural light in the lichen Lobaria pulmonaria. New Phytologist 175, 271282.CrossRefGoogle ScholarPubMed
McEvoy, M, Solhaug, KA and Gauslaa, Y (2007 b) Solar radiation screening in usnic acid-containing cortices of the lichen Nephroma arcticum. Symbiosis 43, 143150.Google Scholar
Michelet, L, Roach, T, Fischer, BB, Bedhomme, M, Lemaire, SD and Krieger-Liszkay, A (2013) Down-regulation of catalase activity allows transient accumulation of a hydrogen peroxide signal in Chlamydomonas reinhardtii. Plant Cell and Environment 36, 12041213.CrossRefGoogle ScholarPubMed
Míguez, F, Fernández-Marín, B, Becerril, J-M and García-Plazaola, JI (2017 a) Diversity of winter photoinhibitory responses: a case study in co-occurring lichens, mosses, herbs and woody plants from subalpine environments. Physiologia Plantarum 160, 282296.CrossRefGoogle ScholarPubMed
Míguez, F, Schiefelbein, U, Karsten, U, García-Plazaola, JI and Gustavs, L (2017 b) Unraveling the photoprotective response of lichenized and free-living green algae (Trebouxiophyceae, Chlorophyta) to photochilling stress. Frontiers in Plant Science 8, 1144.CrossRefGoogle ScholarPubMed
Mishra, A, Hájek, J, Tuháčková, T and Barták, M (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, 99111.CrossRefGoogle Scholar
Miyake, C, Michihata, F and Asada, K (1991) Scavenging of hydrogen peroxide in prokaryotic and eukaryotic algae: acquisition of ascorbate peroxidase during the evolution of cyanobacteria. Plant and Cell Physiology 32, 3343.Google Scholar
Molnar, K and Farkas, E (2010) Current results on biological activities of lichen secondary metabolites: a review. Zeitschrift für Naturforschung Section C 65, 157173.CrossRefGoogle ScholarPubMed
Mosca, C, Rothschild, LJ, Napoli, A, Ferré, F, Pietrosanto, M, Fagliarone, C, Baqué, M, Rabbow, E, Rettberg, P and Billi, D (2019) Over-expression of UV-damage DNA repair genes and ribonucleic acid persistence contribute to the resilience of dried biofilms of the desert cyanobacterium Chroococcidiopsis exposed to Mars-like UV flux and long-term desiccation. Frontiers in Microbiology 10, 2312.CrossRefGoogle ScholarPubMed
Müller, P, Li, X-P and Niyogi, KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiology 125, 15581566.CrossRefGoogle ScholarPubMed
Nakamura, S and Izumi, M (2018) Regulation of chlorophagy during photoinhibition and senescence: lessons from mitophagy. Plant and Cell Physiology 59, 11351143.CrossRefGoogle ScholarPubMed
Nath, K, Jajoo, A, Poudyal, RS, Timilsina, R, Park, YS, Aro, EM, Nam, HG and Lee, CH (2013) Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions. FEBS Letters 587, 33723381.CrossRefGoogle ScholarPubMed
Nawrocki, WJ, Buchert, F, Joliot, P, Rappaport, F, Bailleul, B and Wollman, FA (2019) Chlororespiration controls growth under intermittent light. Plant Physiology 179, 630639.CrossRefGoogle ScholarPubMed
Niyogi, KK and Truong, TB (2013) Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Current Opinion in Plant Biology 16, 307314.CrossRefGoogle ScholarPubMed
Noctor, G, Mhamdi, A and Foyer, C (2014) The roles of reactive oxygen metabolism in drought: not so cut and dried. Plant Physiology 164, 16361648.CrossRefGoogle ScholarPubMed
Ohnishi, N, Allakhverdiev, SI, Takahashi, S, Higashi, S, Watanabe, M, Nishiyama, Y and Murata, N (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44, 84948499.CrossRefGoogle Scholar
Öquist, G and Huner, NPA (2003) Photosynthesis of overwintering evergreen plants. Annual Review of Plant Biology 54, 329355.CrossRefGoogle ScholarPubMed
Osmond, B, Badger, M, Maxwell, K, Bjorkman, O and Leegood, R (1997) Too many photos: photorespiration, photoinhibition and photooxidation. Trends in Plant Science 2, 119121.CrossRefGoogle Scholar
Pandey, P, Singh, J, Achary, VMM and Reddy, MK (2015) Redox homeostasis via gene families of ascorbate-glutathione pathway. Frontiers in Environmental Science 3, 25.CrossRefGoogle Scholar
Peers, G, Truong, TB, Ostendorf, E, Busch, A, Elrad, D, Grossman, AR, Hippler, M and Niyogi, KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462, 518521.CrossRefGoogle ScholarPubMed
Pérez-Pérez, ME, Couso, I and Crespo, JL (2017) The TOR signaling network in the model unicellular green alga Chlamydomonas reinhardtii. Biomolecules 7, 54.CrossRefGoogle ScholarPubMed
Phinney, NH, Gauslaa, Y and Solhaug, KA (2019) Why chartreuse? The pigment vulpinic acid screens blue light in the lichen Letharia vulpina. Planta 249, 709718.CrossRefGoogle ScholarPubMed
Piccotto, M and Tretiach, M (2010) Photosynthesis in chlorolichens: the influence of the habitat light regime. Journal of Plant Research 123, 763775.CrossRefGoogle ScholarPubMed
Pospíšil, P (2016) Production of reactive oxygen species by photosystem II as a response to light and temperature stress. Frontiers in Plant Science 7, 1950.CrossRefGoogle ScholarPubMed
Raggio, J, Pintado, A, Ascaso, C, de la Torre, R, de los Ríos, A, Wierzchos, J, Horneck, G and Sancho, LG (2011) Whole lichen thalli survive exposure to space conditions: results of Lithopanspermia experiment with Aspicilia fruticulosa. Astrobiology 11, 281292.CrossRefGoogle ScholarPubMed
Roach, T and Krieger-Liszkay, A (2019) Photosynthetic regulatory mechanisms for efficiency and prevention of photo-oxidative stress. Annual Plant Reviews Online 2, 273306.CrossRefGoogle Scholar
Roach, T and Na, CS (2017) LHCSR3 affects de-coupling and re-coupling of LHCII to PSII during state transitions in Chlamydomonas reinhardtii. Scientific Reports 7, 43145.CrossRefGoogle ScholarPubMed
Roach, T, Na, CS and Krieger-Liszkay, A (2015) High light-induced hydrogen peroxide production in Chlamydomonas reinhardtii is increased by high CO2 availability. Plant Journal 81, 759766.CrossRefGoogle ScholarPubMed
Roach, T, Baur, T, Stöggl, W and Krieger-Liszkay, A (2017) Chlamydomonas reinhardtii responding to high light: a role for 2-propenal (acrolein). Physiologia Plantarum 161, 7587.CrossRefGoogle Scholar
Roach, T, Stöggl, W, Baur, T and Kranner, I (2018) Distress and eustress of reactive electrophiles and relevance to light stress acclimation via stimulation of thiol/disulphide-based redox defences. Free Radical Biology and Medicine 122, 6573.CrossRefGoogle ScholarPubMed
Roach, T, Na, CS, Stöggl, W and Krieger-Liszkay, A (2020) The non-photochemical quenching protein LHCSR3 prevents oxygen-dependent photoinhibition in Chlamydomonas reinhardtii. Journal of Experimental Botany 71, 26502660.CrossRefGoogle ScholarPubMed
Rochaix, J-D (2011) Regulation of photosynthetic electron transport. Biochimica et Biophysica Acta 1807, 375383.CrossRefGoogle ScholarPubMed
Rochaix, J-D and Bassi, R (2019) LHC-like proteins involved in stress responses and biogenesis/repair of the photosynthetic apparatus. Biochemical Journal 476, 581593.CrossRefGoogle ScholarPubMed
Sahu, N, Singh, SN, Singh, P, Mishra, S, Karakoti, N, Bajpai, R, Behera, SK, Nayaka, S and Upreti, DK (2019) Microclimatic variations and their effects on photosynthetic efficiencies and lichen species distribution along elevational gradients in Garhwal Himalayas. Biodiversity and Conservation 28, 19531976.CrossRefGoogle Scholar
Sathasivam, R and Jang-Seu, K (2018) A review of the biological activities of microalgal carotenoids and their potential use in healthcare and cosmetic industries. Marine Drugs 16, 26.CrossRefGoogle ScholarPubMed
Sedoud, A, López-Igual, R, Ur Rehman, A, Wilson, A, Perreau, F, Boulay, C, Vass, I, Krieger-Liszkay, A and Kirilovsky, D (2014) The cyanobacterial photoactive orange carotenoid protein is an excellent singlet oxygen quencher. Plant Cell 26, 17811791.CrossRefGoogle ScholarPubMed
Serrano, A and Llobell, A (1993) Occurrence of 2 isoforms of glutathione-reductase in the green alga Chlamydomonas reinhardtii. Planta 190, 199205.CrossRefGoogle Scholar
Slavov, C, Reus, M and Holzwarth, AR (2013) Two different mechanisms cooperate in the desiccation-induced excited state quenching in Parmelia lichen. Journal of Physical Chemistry B 117, 1132611336.CrossRefGoogle ScholarPubMed
Smirnoff, N (2018) Ascorbic acid metabolism and functions: a comparison of plants and mammals. Free Radical Biology and Medicine 122, 116129.CrossRefGoogle ScholarPubMed
Solhaug, KA and Gauslaa, Y (1996) Parietin, a photoprotective secondary product of the lichen Xanthoria parietina. Oecologia 108, 412418.CrossRefGoogle ScholarPubMed
Solhaug, KA and Gauslaa, Y (2012) Secondary lichen compounds as protection against excess solar radiation and herbivores. Progress in Botany 73, 283304.Google Scholar
Solhaug, KA, Gauslaa, Y, Nybakken, L and Bilger, W (2003) UV-induction of sun-screening pigments in lichens. New Phytologist 158, 91100.CrossRefGoogle Scholar
Solhaug, KA, Larsson, P and Gauslaa, Y (2010) Light screening in lichen cortices can be quantified by chlorophyll fluorescence techniques for both reflecting and absorbing pigments. Planta 231, 10031011.CrossRefGoogle ScholarPubMed
Stålfelt, MG (1938) Der Gasaustausch der Flechten. Planta 29, 1131.CrossRefGoogle Scholar
Štepigová, J, Gauslaa, Y, Cempirková-Vráblíková, H and Solhaug, KA (2008) Irradiance prior to and during desiccation improves the tolerance to excess irradiance in the desiccated state of the old forest lichen Lobaria pulmonaria. Photosynthetica 46, 286290.CrossRefGoogle Scholar
Streb, P, Feierabend, J and Bligny, R (1997) Resistance to photoinhibition of photosystem II and catalase and antioxidative protection in high mountain plants. Plant, Cell and Environment 20, 10301040.CrossRefGoogle Scholar
Takeda, T, Ishikawa, T and Shigeoka, S (1997) Metabolism of hydrogen peroxide by the scavenging system in Chlamydomonas reinhardtii. Physiologia Plantarum 99, 4955.CrossRefGoogle Scholar
Tel-Or, E, Huflejt, M and Packer, L (1985) The role of glutathione and ascorbate in hydroperoxide removal in cyanobacteria. Biochemical and Biophysical Research Communications 132, 533539.CrossRefGoogle ScholarPubMed
Thadhani, VM, Choudhary, MI, Ali, S, Omar, I, Siddique, H and Karunaratne, V (2011) Antioxidant activity of some lichen metabolites. Natural Product Research 25, 18271837.CrossRefGoogle ScholarPubMed
Triantaphylidès, C, Krischke, M, Hoeberichts, FA, Ksas, B, Gresser, G, Havaux, M, Van Breusegem, F and Mueller, MJ (2008) Singlet oxygen is the major reactive oxygen species involved in photooxidative damage to plants. Plant Physiology 148, 960968.CrossRefGoogle ScholarPubMed
Vass, I-Z, Kós, PB, Sass, L, Nagy, CI and Vass, I (2013) The ability of cyanobacterial cells to restore UV-B radiation induced damage to Photosystem II is influenced by photolyase dependent DNA repair. Photochemistry and Photobiology 89, 384390.CrossRefGoogle ScholarPubMed
Vass, I-Z, Kós, PB, Knoppová, J, Komenda, J and Vass, I (2014) The cry-DASH cryptochrome encoded by the sll1629 gene in the cyanobacterium Synechocystis PCC 6803 is required for Photosystem II repair. Journal of Photochemistry and Photobiology B: Biology 130, 318326.CrossRefGoogle ScholarPubMed
Verhoeven, A, Garcia-Plazaola, JI and Fernandez-Marin, B (2018) Shared mechanisms of photoprotection in photosynthetic organisms tolerant to desiccation or to low temperature. Environmental and Experimental Botany 154, 6679.CrossRefGoogle Scholar
Vidal-Meireles, A, Tóth, D, Kovács, L, Neupert, J and Tóth, SZ (2020) Ascorbate deficiency does not limit nonphotochemical quenching in Chlamydomonas reinhardtii. Plant Physiology 182, 597611.CrossRefGoogle Scholar
Vogelmann, TC (1993) Plant-tissue optics. Annual Review of Plant Physiology and Plant Molecular Biology 44, 231251.CrossRefGoogle Scholar
Vráblíková, H, McEvoy, M, Solhaug, KA, Barták, M and Gauslaa, Y (2006) Annual variation in photoacclimation and photoprotection of the photobiont in the foliose lichen Xanthoria parietina. Journal of Photochemistry and Photobiology B: Biology 83, 151162.CrossRefGoogle Scholar
Vráblíková, H, Barták, M and Wonisch, A (2005) Changes in glutathione and xanthophyll cycle pigments in the high light-stressed lichens Umbilicaria antarctica and Lasallia pustulata. Journal of Photochemistry and Photobiology B: Biology 79, 3541.CrossRefGoogle ScholarPubMed
Weissman, L, Garty, J and Hochman, A (2005) Characterization of enzymatic antioxidants in the lichen Ramalina lacera and their response to rehydration. Applied and Environmental Microbiology 71, 65086514.CrossRefGoogle ScholarPubMed
Wieners, PC, Mudimu, O and Bilger, W (2018) Survey of the occurrence of desiccation-induced quenching of basal fluorescence in 28 species of green microalgae. Planta 248, 601612.CrossRefGoogle ScholarPubMed
Williams, L, Colesie, C, Ullmann, A, Westberg, M, Wedin, M and Büdel, B (2017) Lichen acclimation to changing environments: photobiont switching vs. climate-specific uniqueness in Psora decipiens. Ecology and Evolution 7, 25602574.CrossRefGoogle ScholarPubMed
Wilson, A, Punginelli, C, Gall, A, Bonetti, C, Alexandre, M, Routaboul, JM, Kerfeld, CA, van Grondelle, R, Robert, B, Kennis, JTM, et al. (2008) A photoactive carotenoid protein acting as light intensity sensor. Proceedings of the National Academy of Sciences of the United States of America 105, 1207512080.CrossRefGoogle ScholarPubMed
Wolfe-Simon, F, Grzebyk, D, Schofield, O and Falkowski, PG (2005) The role and evolution of superoxide dismutases in algae. Journal of Phycology 41, 453465.CrossRefGoogle Scholar
Yamamoto, H and Higashi, R (1978) Violaxanthin de-epoxidase: lipid composition and substrate specificity. Archives of Biochemistry and Biophysics 190, 514522.CrossRefGoogle ScholarPubMed
Zavafer, A, Chow, WS and Cheah, MH (2015) The action spectrum of Photosystem II photoinactivation in visible light. Journal of Photochemistry and Photobiology B: Biology 152, 247260.CrossRefGoogle ScholarPubMed