Five macrolichens of different thallus morphology from Antarctica (King George Island) were used for this ecophysiological study. The effect of thallus desiccation on primary photosynthetic processes was examined. We investigated the lichens' responses to the relative water content (RWC) in their thalli during the transition from a wet (RWC of 100%) to a dry state (RWC of 0%). The slow Kautsky kinetics of chlorophyll fluorescence (ChlF) that was recorded during controlled dehydration (RWC decreased from 100 to 0%) and supplemented with a quenching analysis revealed a polyphasic species-specific response of variable fluorescence. The changes in ChlF at a steady state (Fs), potential and effective quantum yields of photosystem II (FV/FM, ΦPSII), and nonphotochemical quenching (NPQ) reflected a desiccation-induced inhibition of the photosynthetic processes. The dehydration-dependent fall in FV/FM and ΦPSII was species-specific, starting at an RWC range of 22-32%. The critical RWC for ΦPSII was below 5%. The changes indicated the involvement of protective mechanisms in the chloroplastic apparatus of lichen photobionts at RWCs of below 20%. In both the wet and dry states, the spectral reflectance curves (SRC) (wavelength 400-800 nm) and indices (NDVI, PRI) of the studied lichen species were measured. Black Himantormia lugubris showed no difference in the SRCs between wet and dry state. Other lichens showed a higher reflectance in the dry state compared to the wet state. The lichen morphology and anatomy data, together with the ChlF and spectral reflectance data, are discussed in relation to its potential for ecophysiological studies in Antarctic lichens.

Department of Experimental Biology Faculty of Science Masaryk University Kamenice 5 Building A13 119 625 00 Brno Czech Republic

Laboratory of Mycology and Mycorrhiza Faculty of Natural Sciences and Oceanography Campus Concepción Concepción University 4030000 Concepción Chile

Laboratory of Plant Ecophysiology Faculty of Natural Resources Campus Luis Rivas del Canto Catholic University of Temuco Rudecindo Ortega 03694 4780000 Temuco Chile

See more in PubMed

Øvstedal D., Lewis-Smith R. Lichens of Antarctica and South Georgia, A Guide to their Identification and Ecology. Cambridge University Press; Cambridge, UK: 2001. p. 411.

Olech M. Lichens of King George Island, Antarctica. Drukarnia Uniwersytetu Jagiellńskiego; Kraków, Poland: 2004. p. 391.

Kennedy A.D. Water as a limiting factor in the Antarctic Terrestrial environment: A biogeographical synthesis. Artic Alp. Res. 1993;25:308–315. doi: 10.2307/1551914. DOI

Green T., Sancho L., Pintado A., Schroeter B. Functional and spatial pressures on terrestrial vegetation in Antarctica forced by global warming. Polar Biol. 2011;34:1643–1656. doi: 10.1007/s00300-011-1058-2. DOI

Green T.G.A., Sancho L.G., Pintado A. Ecophysiology of desiccation/rehydration cycles in mosses and lichens. In: Luttge U., Beck E., Bartels D., editors. Plant Desiccation Tolerance. Volume 215. Springer; Berlin/Heidelberg, Germany: 2011. pp. 89–120.

Schroeter B., Scheidegger C. Water relations in lichens at subzero temperatures: Structural changes and carbon dioxide exchange in the lichen Umbilicaria aprina from continental Antartica. New Phytol. 1995;131:275–285. doi: 10.1111/j.1469-8137.1995.tb05729.x. DOI

Green T.G.A., Schroeter B., Sancho L.G. Plant life in Antarctica. In: Pugnaire F.I., Valladares F., editors. Handbook of Functional Plant Ecology. Marcel Dekker Inc.; New York, NY, USA: 2007.

Sancho L., Pintado A., Green A. Antarctic studies show lichens to be excellent biomonitors of climate change. Diversity. 2019;11:42. doi: 10.3390/d11030042. DOI

Casanova-Katny A., Barták M., Gutierrez C. Open top chamber microclimate may limit photosynthetic processes in Antarctic lichen: Case study from King George Island, Antarctica. Czech. Polar Rep. 2019;9:61–77. doi: 10.5817/CPR2019-1-6. DOI

Colesie C., Williams L., Büdel B. Water relations in the soil crust lichen Psora decipiens are optimized via anatomical variability. Lichenologist. 2017;49:483–492. doi: 10.1017/S0024282917000354. DOI

Inoue T., Kudoh S., Uchida M., Tanabe Y., Inoue M., Kanda H. Factors affecting water availability for high Arctic lichens. Polar Biol. 2017;40:853–862. doi: 10.1007/s00300-016-2010-2. DOI

Kappen L. Some aspects of the great success of lichens in Antarctica. Antarct. Sci. 2000;12:314–324. doi: 10.1017/S0954102000000377. DOI

Colesie C., Green T.G.A., Raggio J., Büdel B. Summer activity patterns of Antarctic and high alpine lichen- dominated biological soil crusts—Similar but different? Arct. Antarct. Alp. Res. 2016;48:449–460. doi: 10.1657/AAAR0015-047. DOI

Veerman J., Vasilev S., Paton G.D., Ramanauskas J., Bruce D. Photoprotection in the lichen Parmelia sulcata: The origins of desiccation-induced fluorescence quenching. Plant. Physiol. 2007;145:997–1005. doi: 10.1104/pp.107.106872. PubMed DOI PMC

Heber U., Bilger W., Shuvalov V.A. Thermal energy dissipation in reaction centers of photosystem II protects desiccated poikilohydric mosses against photooxidation. J. Exp. Bot. 2006;57:2993–3006. doi: 10.1093/jxb/erl058. PubMed DOI

Heber U., Azarkovich M., Shuvalov V.A. Activation of mechanisms of photoprotection by desiccation and by light: Poikilohydric photoautotrophs. J. Exp. Bot. 2007;58:2745–2759. doi: 10.1093/jxb/erm139. PubMed DOI

Heber U. Photoprotection of green plants: A mechanism of ultra-fast thermal energy dissipation in desiccated lichens. Planta. 2008;228:641–650. doi: 10.1007/s00425-008-0766-5. PubMed DOI

Heber U., Bilger W., Turk R., Lange O.L. Photoprotection of reaction centres in photosynthetic organisms: Mechanisms of thermal energy dissipation in desiccated thalli of the lichen Lobaria pulmonaria. New Phytol. 2010;185:459–470. doi: 10.1111/j.1469-8137.2009.03064.x. PubMed DOI

Riznichenko G., Lebedeva G., Pogosyan S., Sivchenko M., Rubin A. Fluorescence induction curves registered from individual microalgae cenobiums in the process of population growth. Photosynth. Res. 1996;49:151–157. doi: 10.1007/BF00117665. PubMed DOI

Papageorgiou G.C., Govindjee Photosystem II fluorescence slow changes—Scaling from the past. J. Photochem. Photobiol. B Biol. 2011;104:258–270. doi: 10.1016/j.jphotobiol.2011.03.008. PubMed DOI

Stirbet A., Riznichenko G.Y., Rubin A.B., Govind J. Modeling chlorophyll a fluorescence transient: Relation to photosynthesis. Biochemistry. 2014;79:291–323. doi: 10.1134/S0006297914040014. PubMed DOI

Seaton G.G., Walker D.D. Chlorophyll fluorescence as a measure of photosynthetic carbon assimilation. Proc. R. Soc. 1990;242:29–35.

Noctor G., Horton P. Uncouple titration of energy-dependent chlorophyll fluorescence quenching and photosystem II photochemical yield in intact pea chloroplasts. Biochim. Biophys. Acta. 1990;1016:228–234. doi: 10.1016/0005-2728(90)90063-A. DOI

Allen J.F. Protein phosphorylation in regulation of photosynthesis. Biochim. Biophys. Acta. 1992;1098:275–335. doi: 10.1016/S0005-2728(09)91014-3. PubMed DOI

Krause H.G. Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol. Plant. 1988 doi: 10.1111/j.1399-3054.1988.tb02020.x. DOI

Kodru S., Malavath T., Devadasu E., Nellaepalli S., Stirbet A., Subramanyam R., Govind J. The slow S to M rise of chlorophyll a fluorescence reflects transition from state 2 to state 1 in the green alga Chlamydomonas reinhardtii. Photosynth. Res. 2015;125:219–231. doi: 10.1007/s11120-015-0084-2. PubMed DOI

Ruban A.V., Young A.J., Horton P. Induction of nonphotochemical energy dissipation and absorbance changes in leaves (Evidence for changes in the state of the light-harvesting system of photosystem II in vivo) Plant. Physiol. 1993;102:741–750. doi: 10.1104/pp.102.3.741. PubMed DOI PMC

Tikkanen M., Grieco M., Nurmi P., Rantala M., Suorsa M., Aro E.-M. Regulation of the photosynthetic apparatus under fluctuating growth light. Philos. Trans. R. Soc. Lond. Ser. Biol. Sci. 2012;367:3486–3493. doi: 10.1098/rstb.2012.0067. PubMed DOI PMC

Stirbet A., Govindjee The slow phase of chlorophyll a fluorescence induction in silico: Origin of S-M fluorescence rise. Photosynth. Res. 2016;130:193–213. doi: 10.1007/s11120-016-0243-0. PubMed DOI

Conti S., Hazdrová J., Hájek J., Očenášová P., Barták M., Skácelová K., Adamo P. Comparative analysis of heterogeneity of primary photosynthetic processes within fruticose lichen thalli: Preliminary study of interspecific differences. Czech. Polar Rep. 2014;4:149–157. doi: 10.5817/CPR2014-2-15. DOI

Mishra A., Hájek J., Tuháčková T., Barták M., Mishra K.B. 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 Rep. 2015;5:99–111. doi: 10.5817/CPR2015-1-10. DOI

Nabe H., Funabiki R., Kashino Y., Koike H., Satoh K. Responses to desiccation stress in Bryophytes and an important role of dithiothreitol-insensitive non-photochemical quenching against photoinhibition in dehydrated states. Plant. Cell Physiol. 2007;48:1548–1557. doi: 10.1093/pcp/pcm124. PubMed DOI

Barták M., Hájek J., Morkusová J., Skácelová K., Košuthová A. Dehydration-induced changes in spectral reflectance indices and chlorophyll fluorescence of Antarctic lichens with different thallus color, and intrathalline photobiont. Acta Physiol. Plant. 2018;40:177–187.

Trnková K., Barták M. Desiccation-induced changes in photochemical processes of photosynthesis and spectral reflectance in Nostoc commune (Cyanobacteria, Nostocales) colonies from Antarctica. Phycol. Res. 2017;65:44–50. doi: 10.1111/pre.12157. DOI

Kosugi M., Miyake A., Kasino Y., Shibata Y., Satoh K., Itoh S. Photosynthesis Research for Food, Fuel and the Future. Advanced Topics in Science and Technology in China. Springer; Berlin/Heidelberg, Germany: 2013. Lichens assist the drought-induced fluorescence quenching of their photobiont green algae through arabitol; pp. 514–520.

Rückamp M., Braun M., Suckro S., Blindow N. Observed glacial changes on the King George Island ice cap, Antarctica, in the last decade. Glob. Planet. Chang. 2011;79:99–109. doi: 10.1016/j.gloplacha.2011.06.009. DOI

Ochyra R., Smith R.I.L., Bednarek-Ochyra H. The Illustrated Moss Flora of Antarctica. Cambridge University Press; Cambridge, UK: 2008. p. 704.

Andreyev M.P. The lichens in the vicinity of Bellingshausen Station, King George Island. Polar Geogr. Geol. 1989;13:42–45. doi: 10.1080/10889378909377379. DOI

Beck A., Bechteler J., Casanova-Katny A., Dzhilyanova I. The pioneer lichen Placopsis in maritime Antarctica: Genetic diversity of their mycobionts and green algal symbionts, and their correlation with deglaciation time. Symbiosis. 2019;79:1–24. doi: 10.1007/s13199-019-00624-4. DOI

Marečková M., Barták M. Effects of short-term low temperature stress on chlorophyll fluorescence transients in Antarctic lichen species. Czech. Polar Rep. 2016;6:56–65. doi: 10.5817/CPR2016-1-6. DOI

Rouse J.W., Haas R.H., Schell J.A., Deering D.W. Monitoring vegetation systems in the Great Plains with ERTS; Proceedings of the Third Earth Resources Technology Satellite–1 Syposium. Volume I: Technical Presentations, NASA SP-351, NASA; Washington, DC, USA. 10–14 December 1973; pp. 309–317.

Gamon J.A., Peñuelas J., Fiels C.B. A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency. Remote Sens. Environ. 1992;41:35–44. doi: 10.1016/0034-4257(92)90059-S. DOI

Dufková K., Barták M., Morkusová J., Elster J., Hájek J. Screening of growth phases of Antarctic algae and cyanobacteria cultivated on agar plates by chlorophyll fluorescence imaging. Czech. Polar Rep. 2019;9:170–181. doi: 10.5817/CPR2019-2-15. DOI

Cho S.M., Lee H., Hong S.G., Lee J. Study of ecophysiological responses of the antarctic fruticose lichen Cladonia borealis using the PAM fluorescence system under natural and laboratory conditions. Plants. 2020;9:85. doi: 10.3390/plants9010085. PubMed DOI PMC

Uchida M., Nakatsubo T., Kanda H., Koizumi H. Estimation of the annual primary production of the lichen Cetrariella delisei in a glacier foreland in the high Arctic, Ny-Ålesund, Svalbard. Polar Res. 2006;25:39–49.

Zúñiga-González P., Zúñiga-González G.E., Pizzaro M., Casanova-Katny A. Soluble carbohydrate content variation in Sanionia uncinata and Polytrichastrum alpinum, two Antarctic mosses with contrasting desiccation capacities. Biol. Res. 2016;49:1–9. doi: 10.1186/s40659-015-0058-z. PubMed DOI PMC

Sancho L., De los Ríos A., Pintado A., Colesie C., Raggio J., Ascaso C., Green A. Himantormia lugubris, an Antarctic endemic on the edge of the lichen symbiosis. Symbiosis. 2020;82:49–58. doi: 10.1007/s13199-020-00723-7. DOI

Barták M. Lichen Photosynthesis. Scaling from the cellular to the organism level. In: Hohmann-Marriott M.F., editor. The Structural Basis of Biological Energy Generation. Advances in Photosynthesis and Respiration. Vol. 39. Springer; Dordrecht, The Netherlands: 2014. pp. 379–400. (Advances in Photosynthesis and Respiration). DOI

Barták M., Trnková K., Hansen E.S., Hazdrová J., Skácelová K., Hájek J., Forbelská M. Effect of dehydration on spectral reflectance and photosynthetic efficiency in Umbilicaria arctica and U. hyperborea. Biol. Plant. 2015;59:357–365. doi: 10.1007/s10535-015-0506-1. DOI

Nayaka S., Saxena P. Physiological responses and ecological success of lichen Stereocaulon foliolosum and moss Racomitrium subsecundum growing in same habitat in Himalaya. Indian J. Fundam. Appl. Life Sci. 2014;4:167–179.

Hovind A.B.A., Phinney N.H., Gauslaa Y. Functional trade-off of hydration strategies in old forest epiphytic cephalolichens. Fungal Biol. 2020;124:903–913. doi: 10.1016/j.funbio.2020.07.008. PubMed DOI

Kranner I., Beckett R., Hochman A., Nash T.H. Desiccation-tolerance in lichens: A review. Bryologist. 2008;111:576–593. doi: 10.1639/0007-2745-111.4.576. DOI

Heber U., Lange O.L., Shuvalov V.A. Conservation and dissipation of light energy as complementary processes: Homoiohydric and poikilohydric autotrophs. J. Exp. Bot. 2006;57:1211–1223. doi: 10.1093/jxb/erj104. PubMed DOI

Krause G.H., Jahns P. Chlorophyll a Fluorescence. Volume 19. Springer; Dordrecht, The Netherlands: 2004. Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: Characterization and function; pp. 463–495.

Zorn M., Pfeifhofer H.W., Grill D., Kranner I. Responses of plastid pigments to desiccation and rehydration in the desert lichen Ramalina maciformis. Symbiosis. 2001;31:201–212.

MacKenzie T.D., MacDonald T.M., Dubois L.A., Campbell D.A. Seasonal changes in temperature and light drive acclimation of photosynthetic physiology and macromolecular content in Lobaria pulmonaria. Planta. 2001;214:57–66. doi: 10.1007/s004250100580. PubMed DOI

Kranner I., Zorn M., Turk B., Wornik S., Beckett R.P., Batič F. Biochemical traits of lichens differing in relative desiccation tolerance. New Phytol. 2003;160:167–176. doi: 10.1046/j.1469-8137.2003.00852.x. PubMed DOI

Slavnov C., Reus M., Holzwarth A.R. Two different mechanisms cooperate in the desiccation-induced excited state quenching in Parmelia lichen. J. Phys. Chem. B. 2013;117:11326–11336. doi: 10.1021/jp402881f. PubMed DOI

Komura M., Yamagishi A., Shibata Y., Iwasaki I., Itoh S. Mechanism of strong quenching of photosystem II chlorophyll fluorescence under drought stress in a lichen, Physciella melanchla, studied by subpicosecond fluorescence spectroscopy. Biochim. Biophys. Acta. 2010;1797:331–338. doi: 10.1016/j.bbabio.2009.11.007. PubMed DOI

Heber U. Conservation and dissipation of light energy in desiccation-tolerant photoautotrophs, two sides of the same coin. Photosynth. Res. 2012;113:5–13. doi: 10.1007/s11120-012-9738-5. PubMed DOI

Gauslaa Y., Solhaug K.A. Fungal melanins as a sun screen for symbiotic green algae in the lichen Lobaria pulmonaria. Oecologia. 2001;126:462–471. doi: 10.1007/s004420000541. PubMed DOI

Wieners P.C., Mudimu O., Bilger W. Desiccation-induced non-radiative dissipation in isolated green lichen algae. Photosynth. Res. 2012;113:239–247. doi: 10.1007/s11120-012-9771-4. PubMed DOI

Papageorgiou G.C., Tsimilli-Michael M., Stamatakis K. The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: A viewpoint. Photosynth. Res. 2007;94:275–290. doi: 10.1007/s11120-007-9193-x. PubMed DOI

Mishra K.B., Vítek P., Barták M. A correlative approach, combining chlorophyll a fluorescence, reflectance, and Raman spectroscopy, for monitoring hydration induced changes in Antarctic lichen Dermatocarpon polyphyllizum. Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 2019;208:13–23. doi: 10.1016/j.saa.2018.09.036. PubMed DOI

Tsimilli-Michael M., Stamatakis K., Papageorgiou G.C. 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. Photosynth. Res. 2009;99:243–255. doi: 10.1007/s11120-009-9405-7. PubMed DOI

Kaňa R., Kotabová E., Komárek O., Šedivá B., Papageorgiou G.C., Govindjee , Prášil O. The slow S to M fluorescence rise in cyanobacteria is due to a state 2 to state 1 transition. Biochim. Biophys. Acta. 2012;1817:1237–1247. doi: 10.1016/j.bbabio.2012.02.024. PubMed DOI

Finazzi G., Barbagalo R.P., Bergo E., Barbato R., Forti G. Photoinhibition of Chlamydomonas reinhardtii in State 1 and State 2. Damages to the photosynthetic apparatus under linear and cyclic electron flow. J. Biol. Chem. 2001;276:22251–22257. doi: 10.1074/jbc.M011376200. PubMed DOI

Mishra K.B., Vítek P., Mishra A., Hájek J., Barták M. Chlorophyll a fluorescence and Raman spectroscopy can monitor activation/deactivation of photosynthesis and carotenoids in Antarctic lichens. Spectrochim. Acta Part A Mol. Biomol. Spectrosc. 2020;239:118458. doi: 10.1016/j.saa.2020.118458. PubMed DOI

Ekman S. The corticolous and lignicolous species of Bacidia and Bacidina in North America. Opera Bot. 1996;127:1–139.

Barták M., Hájek J., Amarillo A.M., Hazdrová J., Carreras H. Changes in spectral reflectance of selected Antarctic and South American lichens caused by dehydration and artificially-induced absence of secondary compounds. Czech. Polar Rep. 2016;6:221–230. doi: 10.5817/CPR2016-2-20. DOI

Bechtel R., Rivard B., Sánchez-Azofeifa A. Spectral properties of foliose and crustose lichens based on laboratory experiments. Remote Sens. Environ. 2002;82:389–396. doi: 10.1016/S0034-4257(02)00055-X. DOI

Van Der Veen C.J., Csatho B.M. Spectral characteristics of Greenland Lichens. Géogr. Phys. Quat. 2005;59:63–73. doi: 10.7202/013737ar. DOI

Kiang N.Y., Siefert J., Govindjee , Blankenship R.E. Spectral signatures of photosynthesis. I. Review of earth organisms. Astrobiology. 2007;7:222–251. doi: 10.1089/ast.2006.0105. PubMed DOI

Kiang N.Y., Segura A., Tinetti G., Govindjee , Blankenship R.E., Cohen M., Siefert J., Crisp D., Meadows V.S. Spectral signatures of photosynthesis. II. Coevolution with other stars and the atmosphere on extrasolar worlds. Astrobiology. 2007;7:252–274. doi: 10.1089/ast.2006.0108. PubMed DOI

Barták M., Mishra K.B., Marečková M. Spectral reflectance indices sense desiccation induced changes in the thalli of Antarctic lichen Dermatocarpon polyphyllizum. Czech. Polar Rep. 2018;8:249–259. doi: 10.5817/CPR2018-2-21. DOI

Gloser J., Gloser V. Changes in spectral reflectance of a foliar lichen Umbilicaria hirsuta during desiccation. Biol. Plant. 2007;51:395–398. doi: 10.1007/s10535-007-0085-x. DOI

Jupa R., Hájek J., Hazdrová J., Barták M. Interspecific differences in photosynthetic efficiency and spectral reflectance in two Umbilicaria species from Svalbard during controlled desiccation. Czech. Polar Rep. 2012;2:31–41. doi: 10.5817/CPR2012-1-4. DOI

Granlund L., Keski-Saari S., Kumpula T., Oksanen E., Keinanan M. Imaging lichen water content with visible to mid-wave infrared (400–5500 nm) spectroscopy. Remote Sens. Environ. 2018;216:301–310. doi: 10.1016/j.rse.2018.06.041. DOI

Antarctic Lichens under Long-Term Passive Warming: Species-Specific Photochemical Responses to Desiccation and Heat Shock Treatments