Skip to main content
SpringerLink
Log in

Lichens and Bryophytes: Light Stress and Photoinhibition in Desiccation/Rehydration Cycles – Mechanisms of Photoprotection

  • Chapter
  • First Online:
Plant Desiccation Tolerance

Part of the book series: Ecological Studies ((ECOLSTUD,volume 215))

Abstract

Many mosses and most of the lichens are desiccation-tolerant poikilohydrous cryptogams. By retaining their chlorophyll and their photosynthetic apparatus during desiccation, they are termed homoiochlorophyllous. In evolutionary terms, this is a primary adaptation. Photosynthetic pigments absorb light, whether the organisms are hydrated or desiccated, but energy conservation by carbon assimilation is possible only in the presence of water. When photosynthetic reaction centers remain intact during desiccation, photoreactions threaten to cause severe photooxidative damage. Shading or the production of sun-protectant pigments reduce but cannot prevent photooxidation. Mechanisms of harmless thermal energy dissipation provide far more efficient photoprotection than shading. Zeaxantin-dependent energy dissipation, usually sufficient to protect higher plants against excess illumination, is also operative in hydrated mosses and in lichens, which contain green algae as photobionts, but is not active in lichens with cyanobacteria as photobionts. During desiccation, other more efficient mechanisms of thermal energy dissipation are activated. They involve reversible changes of the conformation of a pigment protein, which facilitate ultrafast dissipation of the first excitation state of chlorophyll outside the reaction centers. Excitation energy is trapped in dissipation centers that are located in the near far-red region of the spectrum. They are connected to photosystem II. Additional protection may be provided by the reversible conversion of reaction centers into dissipation centers. Rehydration inactivates these mechanisms. Insight into the molecular mechanisms of thermal energy dissipation promises understanding of how oxidative damage is prevented in desiccated photoautotrophs under strong illumination.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

Fm:

Maximum modulated fluorescence under strong actinic illumination, QA reduced

F o :

Minimum modulated chlorophyll fluorescence of hydrated organisms, quinone acceptor QA in the reaction center of photosystem II oxidized

F o′:

Minimum modulated fluorescence in the absence of water, QA oxidized or reduced

F v/F m = (F m − F o)/F m :

Quantum efficiency of charge separation in PSII

PPFD:

Photosynthetically active photon flux density

PS:

Photosystem

RC:

Reaction center

References

  • Ahn TK, Avenson TJ, Ballottari M, Cheng Y-C, Niyogi KK, Bassi R, Fleming GR (2008) Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320:794–797

    Article  PubMed  CAS  Google Scholar 

  • Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134

    Article  PubMed  CAS  Google Scholar 

  • Avenson TJ, Ahn TK, Zigmantas D, Niyogi KK, Li Z, Ballottari M, Bassi R, Fleming GR (2008) Zeaxanthin radical formation in minor light-harvesting complexes of higher plant antenna. J Biol Chem 283:3550–3558

    Article  PubMed  CAS  Google Scholar 

  • Barros T, Royant A, Standfuss J, Dreuw A, Kühlbrandt W (2009) Crystal structure of plant light-harvesting complex shows the active, energy-transmitting state. EMBO J 28:296–306

    Article  Google Scholar 

  • Björkman O, Demmig-Adams B (1994) Regulation of photosynthetic light energy capture, conversion and dissipation in leaves of higher plants. In: Schulze E-D, Caldwell MM (eds) Ecophysiology of photosynthesis, vol 100, Ecological studies. Springer, Heidelberg, Germany, pp 17–70

    Google Scholar 

  • Bukhov NG, Kopecky J, Pfündel EE, Klughammer C, Heber U (2001) Few molecules of zeaxanthin per reaction centre of photosystem II permit effective thermal dissipation of light energy in a poikilohydric moss. Planta 212:739–748

    Article  PubMed  CAS  Google Scholar 

  • Butler WL (1962) Absorption of light by turbid materials. J Opt Soc Am 52:292–299

    Article  CAS  Google Scholar 

  • Cogdell RJ (2006) The structural basis of non-photochemical quenching is revealed? Trends Plant Sci 11:59–60

    Article  PubMed  CAS  Google Scholar 

  • Coughlan SJ, Schreiber U (1984) The differential effects of short-time glutaraldehyde treatments on light-induced thylakoid membrane conformational changes, proton pumping and electron transport properties. Biochim Biophys Acta 767:606–617

    Article  CAS  Google Scholar 

  • Demmig-Adams B (1990) Carotenoids and photoprotection of plants: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Máguas C, Adams WW III, Meyer A, Kilian E, Lange OL (1990a) Effect of high light on the efficiency of photochemical energy conversion in a variety of lichen species with green and blue–green phycobionts. Planta 180:400–409

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III, Czygan F-C, Schreiber U, Lange OL (1990b) 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 180:582–589

    Article  CAS  Google Scholar 

  • Dietz S, Büdel B, Lange OL, Bilger W (2000) Transmittance of light through the cortex of lichens from contrasting habitats. Bibl Lichenol 75:171–182

    Google Scholar 

  • Duysens LMN, Sweers HE (1963) Mechanisms of photochemical reactions in algae as studied by means of fluorescence. In: Studies on microalgae and photosynthetic bacteria, special issue of plant and cell physiology. Tokyo University Press, pp 353–372

    Google Scholar 

  • Faller P, Fufezan C, Rutherford AW (2006) Side path electron donors: cytochrome b559, chlorophyll Z and β-carotene, chapter 15. In: Wydrzynski T, Satoh K (eds) Photosystem II: the water/plastoquinone oxidoreductase in photosynthesis. Kluwer, Dordrecht, pp 347–365

    Google Scholar 

  • Gauslaa Y, Solhaug KA (1999) High-light damage in air-dry thalli of the old forest lichen Lobaria pulmonaria – interactions of irradiance, exposure duration and high temperature. J Exp Bot 50:697–705

    Article  CAS  Google Scholar 

  • Gauslaa Y, Solhaug KA (2001) Fungal melanins as a sun screen for symbiotic green algae in the lichen Lobaria pulmonaria. Oecologia 126:462–471

    Article  Google Scholar 

  • Gauslaa Y, Solhaug KA (2004) Photoinhibition in lichens depends on cortical characteristics and hydration. Lichenologist 36:130–143

    Article  Google Scholar 

  • Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Gilmore AM, Govindjee (1999) How higher plants respond to excess light: energy dissipation in photosystem II. In: Singhal GS, Renger G, Sopory SK, Irrgang K-D, Govindjee (eds) Concepts in photobiology: photosynthesis and photomorphogenesis. Narosa Publishing House, New Delhi, pp 513–548

    Google Scholar 

  • Gray DW, Lewis LA, Cardon ZG (2007) Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives. Plant Cell Environ 30:1240–1255

    Article  PubMed  CAS  Google Scholar 

  • Heber U (2002) Irrungen, Wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants. Photosynth Res 73:223–231

    Article  PubMed  CAS  Google Scholar 

  • Heber U (2008) Photoprotection of green plants: a mechanism of ultra-fast thermal energy dissipation in desiccated lichens. Planta 228:641–650

    Article  PubMed  CAS  Google Scholar 

  • Heber U, Shuvalov VA (2005) Photochemical reactions of chlorophyll in dehydrated photosystem II: two chlorophyll forms (680 and 700 nm). Photosynth Res 84:85–91

    Article  PubMed  CAS  Google Scholar 

  • Heber U, Bukhov NG, Shuvalov VA, Kobayashi Y, Lange OL (2001) Protection of the photosynthetic apparatus against damage by excessive illumination in homoiohydric leaves and poikilohydric mosses and lichens. J Exp Bot 52:1999–2006

    Article  PubMed  CAS  Google Scholar 

  • Heber U, Bilger W, Shuvalov VA (2006a) Thermal energy dissipation in reaction centers of photosystem II protects desiccated poikilohydric mosses against photooxidation. J Exp Bot 57:2993–3006

    Article  PubMed  CAS  Google Scholar 

  • Heber U, Lange OL, Shuvalov VA (2006b) Conservation and dissipation of light energy by plants as complementary processes involved in sustaining plant life: homoiohydric and poikilohydric autotrophs. J Exp Bot 57:1211–1223

    Article  PubMed  CAS  Google Scholar 

  • Heber U, Azarkovich M, Shuvalov VA (2007) Activation of mechanisms of photoprotection by desiccation and by light: poikilohydric photoautotrophs. J Exp Bot 58:2745–2759

    Article  PubMed  CAS  Google Scholar 

  • Heber U, Bilger W, Türk R, Lange OL (2010) Photoprotection of reaction centres in photosynthetic organisms: mechanisms of thermal energy dissipation in desiccated thalli of the lichen Lobaria pulmonaria. New Phytol 185:459–470

    Article  PubMed  CAS  Google Scholar 

  • Holt NE, Fleming GR, Niyogi KK (2004) Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43:8281–8289

    Article  PubMed  CAS  Google Scholar 

  • Holt NE, Tigmantas D, Valkunas L, Li X-P, Niyogi KK, Fleming GR (2005) Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307:433–436

    Article  PubMed  CAS  Google Scholar 

  • Holzwarth AR, Muller MG, Reus M, Nowazyk M, Saner J, Rogner M (2006) Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: pheophytin is the primary electron acceptor. Proc Nat Acad Sci USA 103:6895–6900

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684

    Article  PubMed  CAS  Google Scholar 

  • Horton P, Wentworth M, Ruban A (2005) Control of the light harvesting function of chloroplast membranes: the LHCII-aggregation model for non-photochemical quenching. FEBS Lett 579:4201–4206

    Article  PubMed  CAS  Google Scholar 

  • Ivanov AG, Sane PV, Hurry V, Öquist G, Huner NPA (2008) Photosystem II reaction center quenching: mechanisms and physiological role. Photosynth Res 98:565–574

    Article  PubMed  CAS  Google Scholar 

  • Komura M, Yamagishi A, Shibata Y, Iwasaki I, Itoh S (2010) 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 1797:331–338

    Article  PubMed  CAS  Google Scholar 

  • Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346

    Article  PubMed  CAS  Google Scholar 

  • Krieger-Liszkay A, Fufezan C, Trebst A (2008) Singlet oxygen production in photosystem II and related protection mechanism. Photosynth Res 98:551–564

    Article  PubMed  CAS  Google Scholar 

  • Li X-P, Gilmore AM, Caffari S, Bassi R, Golan T, Kramer D, Niyogi KK (2004) Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J Biol Chem 279:22866–22874

    Article  PubMed  CAS  Google Scholar 

  • Lüttge U, Meirelles ST, de Mattos EA (2008) Strong quenching of chlorophyll fluorescence in the desiccated state in three poikilohydric and homoiochlorophyllous moss species indicates photo-oxidative protection on highly light-exposed rocks of a tropical inselberg. J Plant Physiol 165:172–181

    Article  PubMed  Google Scholar 

  • Ma Y-Z, Holt NE, Li X-P, Niyogi KK, Fleming GR (2003) Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting. Proc Nat Acad Sci USA 100:4377–4382

    Article  PubMed  CAS  Google Scholar 

  • McEvory M, Gauslaa Y, Solhaug KA (2007) Changes in pools of depsidones and melanins, and their function, during growth and acclimation under contrasting natural light in the lichen Lobaria pulmonaria. New Phytol 175:271–282

    Article  Google Scholar 

  • Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359

    Article  PubMed  CAS  Google Scholar 

  • Paillotin G (1976) Movement of excitations in the photosynthetic domains of photosystem II. J Theor Biol 58:237–252

    Article  CAS  Google Scholar 

  • Pascal AA, Liu Z, Broess K, van Oort B, van Amerongen H, Wang C, Horton P, Robert B, Chang W, Ruban A (2005) Molecular basis of photoprotection and control of photosynthetic light-harvesting. Nature 436:134–137

    Article  PubMed  CAS  Google Scholar 

  • Rikkinen J (1995) What’s behind the pretty colours? A study on the photobiology of lichens. Bryobrothera 4:1–239

    Google Scholar 

  • Ruban AV, Berera R, Ilioaia C, van Stokkum IHM, Kennis JTM, Pascal AA, van Amerongen H, Robert B, Horton P, van Grondelle R (2007) Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450:575–578

    Article  PubMed  CAS  Google Scholar 

  • Shuvalov VA, Heber U (2003) Photochemical reactions in dehydrated photosynthetic organisms, leaves, chloroplasts, and photosystem II particles: reversible reduction of pheophytin and chlorophyll and oxidation of β-carotene. Chem Phys 294:227–237

    Article  CAS  Google Scholar 

  • Solhaug KA, Gauslaa Y, Nybakken L, Bilger W (2003) UV-induction of sun-screening pigments in lichens. New Phytol 158:91–100

    Article  CAS  Google Scholar 

  • Stepigova J, Gauslaa Y, Cempirkova-Vrablikova H, 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 46:286–290

    Article  Google Scholar 

  • Terashima I, Fujita T, Inoue T, Chow WS, Oguchi R (2009) Green light drives photosynthesis more efficiently than red light in strong white light: revisiting the enigmatic question of why leaves are green. Plant Cell Physiol 50:684–697

    Article  PubMed  CAS  Google Scholar 

  • Veerman J, Vasil’ev S, Paton GD, Ramanauskas J, Bruce D (2007) Photoprotection in the lichen Parmelia sulcata: the origins of desiccation-induced fluorescence quenching. Plant Physiol 145:997–1005

    Article  PubMed  CAS  Google Scholar 

  • Wirth V (1995) Die Flechten. Verlag Eugen Ulmer, Stuttgart

    Google Scholar 

  • Zinth W, Kaiser W (1993) Time-resolved spectroscopy of the primary electron transfer in reaction centres of Rhodobacter sphaeroides and Rhodopseudomonas viridis. In: Deisenhofer J, Norris JR (eds) The photosynthetic reaction centre. Academic, San Diego, CA, pp 71–88

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Julius-von-Sachs-Institute of Biosciences, University of Würzburg, Julius-von-Sachs-Platz 2, D-97082, Würzburg, Germany

    Ulrich Heber

  2. Institute of Botany, Department of Biology, Technical University of Darmstadt, Schnittspahnstr. 3–5, 64287, Darmstadt, Germany

    Ulrich Lüttge

Authors
  1. Ulrich Heber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ulrich Lüttge
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ulrich Heber .

Editor information

Editors and Affiliations

  1. Inst. Botanik, TU Darmstadt, Schnittspahnstr. 3-5, Darmstadt, 64287, Germany

    Ulrich Lüttge

  2. Inst. Pflanzenphysiologie, Univ. Bayreuth, Bayreuth, 95440, Germany

    Erwin Beck

  3. Inst. Molekulare Physiologie und, Biotechnologie der Pflanzen (IMBIO), Universität Bonn, Kirschallee 1, Bonn, 53115, Germany

    Dorothea Bartels

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Heber, U., Lüttge, U. (2011). Lichens and Bryophytes: Light Stress and Photoinhibition in Desiccation/Rehydration Cycles – Mechanisms of Photoprotection. In: Lüttge, U., Beck, E., Bartels, D. (eds) Plant Desiccation Tolerance. Ecological Studies, vol 215. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19106-0_7

Download citation

Publish with us

Policies and ethics

Search

Navigation