Thermal Dissipation of Light Energy is Regulated Differently and by Different Mechanisms in Lichens and Higher Plants

J. Kopecky; M. Azarkovich; E. E. Pfündel; V. A. Shuvalov; U. Heber

doi:10.1055/s-2005-837471

Plant Biology, Table of Contents

Plant Biol (Stuttg) 2005; 7(2): 156-167
DOI: 10.1055/s-2005-837471

Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Thermal Dissipation of Light Energy is Regulated Differently and by Different Mechanisms in Lichens and Higher Plants

J. Kopecky¹ , M. Azarkovich² , E. E. Pfündel³ , V. A. Shuvalov⁴ , U. Heber³

¹Institute of Microbiology, Academy of Sciences, Department of Autotrophic Microorganisms, Opatovicky mlyn, 379 81 Trebon, Czech Republic
²Timiriasev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya Ul., 35, 127276 Moscow, Russia
³Julius-von-Sachs-Institute of Biological Sciences, University of Würzburg, Julius-von-Sachs-Platz 2, 97082 Würzburg, Germany
⁴Institute of Basic Biological Problems, Russian Academy of Sciences, 142290 Pushchino-na-Oke, Moscow Region, Russia

Abstract

Modulated chlorophyll fluorescence was used to compare dissipation of light energy as heat in photosystem II of homoiohydric and poikilohydric photosynthetic organisms which were either hydrated or dehydrated. In hydrated chlorolichens with an alga as the photobiont, fluorescence quenching revealed a dominant mechanism of energy dissipation which was based on a protonation reaction when zeaxanthin was present. CO₂ was effective as a weak protonating agent and actinic light was not necessary. In a hydrated cyanobacterial lichen, protonation by CO₂ was ineffective to initiate energy dissipation. This was also true for leaves of higher plants. Thus, regulation of zeaxanthin-dependent energy dissipation by protonation was different in leaves and in chlorolichens. A mechanism of energy dissipation different from that based on zeaxanthin became apparent on dehydration of both lichens and leaves. Quenching of maximum or Fm fluorescence increased strongly during dehydration. In lichens, this was also true for so-called basal or Fo fluorescence. In contrast to zeaxanthin-dependent quenching, dehydration-induced quenching could not be inhibited by dithiothreitol. Both zeaxanthin-dependent and dehydration-induced quenching cooperated in chlorolichens to increase thermal dissipation of light energy if desiccation occurred in the light. In cyanolichens, which do not possess a zeaxanthin cycle, only desiccation-induced thermal energy dissipation was active in the dry state. Fluorescence emission spectra of chlorolichens revealed stronger desiccation-induced suppression of 685-nm fluorescence than of 720-nm fluorescence. In agreement with earlier reports of [Bilger et al. (1989)], fluorescence excitation data showed that desiccation reduced flow of excitation energy from chlorophyll b of the light harvesting complex II to emitting centres more than flow from chlorophyll a of core pigments. The data are discussed in relation to regulation and localization of thermal energy dissipation mechanisms. It is concluded that desiccation-induced fluorescence quenching of lichens results from the reversible conversion of energy-conserving to energy-dissipating photosystem II core complexes.

Key words

Chlorophyll fluorescence - energy dissipation - lichens - photooxidative damage - photoprotection

Full Text

References

1 Asada K.. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology and Plant Molecular Biology. (1999); 50 601-639
2 Aspinall-O'Dea M., Wentworth M., Pascal A., Robert B., Ruban A., Horton P.. In vitro reconstitution of the activated zeaxanthin state associated with energy dissipation in plants. Proceedings of the National Academy of Sciences of the USA. (2002); 99 16331-16335
3 Barber I., Andersson B.. Too much of a good thing, light, can be bad for photosynthesis. Trends in Biochemical Sciences. (1992); 17 61-66
4 Bilger W., Rimke S., Schreiber U., Lange O. L.. Inhibition of energy transfer to photosystem II in lichens by dehydration: different properties of reversibility with green and blue-green photobionts. Journal of Plant Physiology. (1989); 134 261-268
5 Björkman O., Demmig-Adams B.. Photon yield of oxygen evolution and chlorophyll fluorescence characteristics ar 77 K among vascular plants of diverse origin. Planta. (1987); 170 489-504
6 Björkman O., Demmig-Adams B.. Regulation of photosynthetic light energy capture, conversion, and dissipation in leaves of higher plants. Schulze, E.-D. and Caldwell, M. M., eds. Ecophysiology of Photosynthesis. Berlin; Springer (1994): 17-47
7 Bruce D., Samson G., Carpenter C.. The origins of nonphotochemical quenching of chlorophyll fluorescence in photosynthesis. Direct quenching by P680⁺ in photosystem II enriched membranes at low pH. Biochemistry. (1997); 36 749-755
8 Bukhov N. G., Heber U., Wiese C., Shuvalov V. A.. Energy dissipation in photosynthesis: quenching of chlorophyll fluorescence in reaction centers and antenna complexes. Planta. (2001 a); 212 749-758
9 Bukhov N. G., Kopecky J., Pfündel E. E., Klughammer C., Heber U.. A few molecules of zeaxanthin per reaction centre of pohotosystem II permit effective thermal dissipation of light energy in photosystem II of a poikilohydric moss. Planta. (2001 b); 212 739-748
10 Demmig-Adams B.. Carotenoids and photoprotection of plants: a role for the xanthophyll zeaxanthin. Biochimica et Biophysica Acta. (1990); 1020 1-24
11 Demmig-Adams B., Adams III. W. W., Czygan F.-C., Lange O. L.. 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. (1990 a); 180 582-589
12 Demmig-Adams B., Green T. G. A., Czygan F.-C., Lange O. L.. Differences in the susceptibility to light stress in two lichens forming a phycosymbiodeme, one partner possessing and one lacking the zeaxanthin cycle. Oecologia. (1990 b); 84 451-456
13 Finazzi G., Johnson N. G., Dallosto L., Joliot P., Wollman F.-A., Bassi R.. A zeaxanthin-independent nonphotochemical quenching mechanism localized in the photosystem II core complex. Proceedings of the National Academy of Sciences of the USA. (2004); 101 12375-12380
14 Genty B., Briantais J.-M., Baker N. R.. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta. (1989); 990 87-92
15 Gilmore A. M., Yamamoto H. Y.. Resolution of lutein and zeaxanthin using a non-endcapped lightly carbon-loaded C18 high-performance liquid chromatographic column. Journal of Chromatography. (1991); 543 137-145
16 Gilmore A. M., Govindjee. How higher plants respond to excess light: energy dissipation in photosystem II. Singhal, G. S., Renger, G., Sopory, S. K., Irrgang, K.-D., and Govindjee, eds. Concepts in Photobiology: Photosynthesis and Photomorphogenesis. New Delhi; Narosa Publ. House (1999): 513-548
17 Graßes T., Pesaresi P., Schiavon F., Varotto C., Salamini F., Jahns P., Leister D.. The role of ΔpH-dependent dissipation of excitation energy in protecting photosystem II against light-induced damage in Arabidopsis thaliana. . Plant Physiology and Biochemistry. (2002); 40 41-49
18 Hager A.. Lichtbedingte pH-Erniedrigung in einem Chloroplasten-Kompartiment als Ursache der enzymatischen Violaxanthin/Zeaxanthin-Umwandlung; Beziehungen zur Photophosphorylierung. Planta. (1969); 89 224-243
19 Heber U.. Conformational changes of chloroplasts induced by illumination of leaves in vivo. . Biochimica et Biophysica Acta. (1969); 180 302-319
20 Heber U.. Irrungen, Wirrungen? The Mehler reaction in relation to cyclic electron transport in C3 plants. Photosynthesis Research. (2002); 73 223-231
21 Heber U., Bilger W., Bligny R., Lange O. L.. Phototolerance of lichens, mosses and higher plants in an alpine environment: analysis of photoreactions. Planta. (2000); 211 770-780
22 Holt N. E., Fleming G. R., Niyogi K. K.. Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry. (2004); 43 8281-8289
23 Jagendorf A. T.. Acid-base transition and phosphorylation by chloroplasts. Federation Proceedings. (1967); 26 1361-1369
24 Kaminskaya O., Renger G., Shuvalov V. A.. Effect of dehydration on light-induced reductions in photosystem II: photoreactions of cytochrome b559. Biochemistry. (2003); 42 8119-8132
25 Katona E., Neimanis S., Schönknecht G., Heber U.. Photosystem I-dependent cyclic electron transport is important in controlling photosystem II activity in leaves under conditions of water stress. Photosynthesis Research. (1992); 34 449-464
26 Kitajima K., Butler W.. Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dichromothymoquinone. Biochim. Biochimica et Biophysica Acta. (1975); 376 105-115
27 Krause G. H.. Photoinhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiologia Plantarum. (1988); 74 566-574
28 Krieger A., Weiss E.. The role of calcium in the pH-dependent control of photosystem II. Photosynthesis Research. (1993); 37 117-130
29 Lange O. L., Bilger W., Rimke S., Schreiber U.. Chlorophyll fluorescence of lichens containing green and blue-green algae during hydration by water vapor uptake and by addition of liquid water. Botanica Acta. (1989); 102 306-313
30 Lange O. L., Kilian E.. Reaktivierung der Photosynthese trockener Flechten durch Wasserdampfaufnahme aus dem Luftraum: artspezifisch unterschiedliches Verhalten. Flora. (1985); 176 7-23
31 Lange O. L., Kilian E., Ziegler H.. Water vapor uptake and photosynthesis of lichens: performance differences in species with green and bluegreen algae as phycobionts. Oecologia. (1986); 71 104-110
32 Lee H.-Y., Hong Y.-N., Chow W. S.. Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves. Planta. (2001); 212 332-342
33 Li X.-P., Björkman O., Shih C., Grossman A. R., Rosenquist M., Jannson S., Niyogi K. K.. A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature. (2000); 403 391-395
34 Li X.-P., Müller-Moulé P., Gilmore A. M., Niyogi K. K.. PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proceedings of the National Academy of Sciences of the USA. (2002 a); 99 15222-15227
35 Li X.-P., Phippard A., Pasari J., Niyogi K. K.. Structure-function analysis of photosystem II subunit S (PsbS) in vivo. . Functional Plant Biology. (2002 b); 29 1131-1139
36 Li X.-P., Gilmore A. M., Caffari S., Bassi R., Golan T., Kramer D., Nioyogi K. K.. Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. Journal of Biological Chemistry. (2004); 279 22866-22874
37 Ma Y.-Z., Holt N. E., Li X.-P., Niyogi K. K., Fleming G. R.. Evidence for direct carotenoid involvement in the regulation of photosynthetic light harvesting. Proceedings of the National Academy of Sciences of the USA. (2003); 100 4377-4382
38 Niyogi K. K.. Photoprotection revisited: genetic and molecular approaches. Annual Review of Plant Physiology and Plant Molecular Biology. (1999); 50 333-359
39 Öquist G., Chow W. S., Anderson J. M.. Photoinhibition of photosynthesis represents a mechanism of the long-term regulation of photosystem II. Planta. (1992); 186 450-460
40 Owens T. G.. Processing of excitation energy by antenna pigments. Baker, N. R., ed. Photosynthesis and the Environment. Dordrecht; Kluwer Academic Publishers (1996): 1-23
41 Pfündel E. E., Dilley R. A.. The pH dependence of violaxanthin deepoxidation in isolated pea chloroplasts. Plant Physiology. (1993); 101 65-71
42 Ruban A. V., Pascal A. A., Robert B., Horton P.. Activation of zeaxanthin is an obligatory event in the regulation of photosynthetic light harvesting. Journal of Biological Chemistry. (2002); 277 7785-7789
43 Sass L., Csintalan Z., Tuba Z., Vass I.. Thermoluminescence studies on the function of photosystem II in the desiccation-tolerant lichen Cladonia convoluta. . Photosynthesis Research. (1996); 48 205-212
44 Scheidegger C., Schroeter B., Frey B.. Structural and functional processes during water vapor uptake and desiccation in selected lichens with green algal photobionts. Planta. (1995); 197 399-409
45 Schlensog M., Schroeter B., Green T. A. G.. Water dependent photosynthetic activity of lichens from New Zealand: differences in the green algal and the cyanobacterial parts of photosymbiodemes. Bibliotheca Lichenologica. (2000); 75 149-160
46 Schreiber U., Neubauer C.. O₂-dependent electron flow, membrane energization and the mechanism of nonphotochemical quenching. Photosynthesis Research. (1990); 25 279-293
47 Schreiber U., Schliwa U., Bilger W.. Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynthesis Research. (1986); 10 51-62
48 Shuvalov V. A., Heber U.. Photochemical reactions in dehydrated photosynthetic organisms, leaves, chloroplasts and photosystem II particles: Reversible reduction of pheophytin and chlorophyll and oxidation of β-carotene. Chemical Physics. (2003); 294 227-237
49 Wentworth M., Ruban A. V., Horton P.. Thermodynamic investigation into the mechanisms of the chlorophyll fluorescence quenching in isolated photosystem II light harvesting complexes. Journal of Biological Chemistry. (2003); 278 21845-21850
50 Yamamoto H. Y., Kamite L.. The effects of dithiothreitol on violaxanthin de-epoxidation and absorbance changes in the 500 nm region. Biochimica et Biophysica Acta. (1972); 267 538-543
51 Ziem-Hanck U., Heber U.. Oxygen requirement of photosynthetic CO₂ assimilation. Biochimica et Biophysica Acta. (1980); 591 266-274

U. Heber

Julius-von-Sachs Institute of Biological Sciences
University of Würzburg

Julius-von-Sachs-Platz 2

97082 Würzburg

Germany

Email: heber@botanik.uni-wuerzburg.de

Editor: H. Rennenberg