Skip to main content
SpringerLink
Log in

Chlorophyll thermofluorescence and thermoluminescence as complementary tools for the study of temperature stress in plants

  • Review
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

The photosynthetic apparatus, especially the electron transport chain imbedded in the thylakoid membrane, is one of the main targets of cold and heat stress in plants. Prompt and delayed fluorescence emission originating from photosystem II have been used, most often separately, to monitor the changes induced in the photosynthetic membranes during progressive warming or cooling of a leaf sample. Thermofluorescence of F 0 and F M informs on the effects of heat on the chlorophyll antennae and the photochemical centers, thermoluminescence on the stabilization and movements of charges and Delayed Light Emission on the permeability of the thylakoid membranes to protons and ions. Considered together and operated simultaneously, these techniques constitute a powerful tool to characterize the effect of thermal stress on intact photosynthetic systems and to understand the mechanisms of constitutive or induced tolerance to temperature stresses.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

AG:

Afterglow

E a :

Activation energy of charge recombination

DLE:

Delayed light emission (luminescence under modulated excitation)

F 0 :

Minimum fluorescence level

F M :

Maximum fluorescence level

F 0/T curve:

Temperature dependence curve of steady-state chlorophyll fluorescence excited by a dim light

LHCII:

Light-harvesting complex II

PS-II:

Photosystem II

P680 :

PS-II reaction center chlorophyll

QA, QB :

Primary and secondary quinonic acceptors of photosystem II

S1, S2, S3:

State of the manganese oxygen-evolving complex storing 1, 2, 3+ charges resp.

T c :

Critical temperature above which chlorophyll fluorescence starts to rise sharply in the F 0/T curve

T m :

Maximal temperature of a TL band

TL:

Thermoluminescence

References

  • Abbott JA, Campbell TA, Massie DR (1994) Delayed light-emission and fluorescence responses of plants to chilling. Remote Sens Environ 47:87–97

    Article  Google Scholar 

  • Affek HP, Yakir D (2002) Protection by isoprene against singlet oxygen in leaves. Plant Physiol 129:269–277

    Article  PubMed  CAS  Google Scholar 

  • Agati G, Mazzinghi P, Lipucci di Paola M, Fusi F, Cecchi G (1996) The F685/F730 chlorophyll fluorescence ratio as indicator of chilling stress in plants. J Plant Physiol 148:384–390

    CAS  Google Scholar 

  • Agati G, Cerovic ZG, Moya I (2000) The effect of decreasing temperature up to chilling values on the in vivo F685/F735 chlorophyll fluorescence ratio in Phaseolus vulgaris and Pisum sativum: the role of the photosystem I contribution to the 735 nm fluorescence band. Photochem Photobiol 72:75–84

    Article  PubMed  CAS  Google Scholar 

  • Balogi Z, Török Z, Balogh G, Josvay K, Shigapova N, Vierling E, Vigh L, Horvath I (2005) “Heat shock lipid” in cyanobacteria during heat/light-acclimation. Arch Biochem Biophys 436:346–354

    Article  PubMed  CAS  Google Scholar 

  • Barra M, Haumann M, Dau H (2005) Specific loss of the extrinsic 18 kDa protein from Photosystem II upon heating to 47 °C causes inactivation of oxygen evolution likely due to Ca release from Mn complex. Photosynth Res 84:231–237

    Article  PubMed  CAS  Google Scholar 

  • Berry JA, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543

    Article  Google Scholar 

  • Bertsch WF, Azzi JR (1965) A relative maximum in the decay of long-term delayed light emission from the photosynthetic apparatus. Biochim Biophys Acta 94:15–26

    Article  PubMed  CAS  Google Scholar 

  • Bilger HW, Schreiber U, Lange OL (1984) Determination of leaf heat resistance: comparative investigation of chlorophyll fluorescence changes and tissue necrosis methods. Oecologia 63:256–262

    Article  Google Scholar 

  • Bilger W, Schreiber U (1990) Chlorophyll luminescence as an indicator of stress-induced damage the photosynthetic apparatus. Effect of heat-stress in isolated chloroplasts. Photosynth Res 25:161–171

    Article  CAS  Google Scholar 

  • Boussac A, Maison-Peteri B, Vernotte C, Etienne AL (1985) The charge accumulation in NaCl-washed and in Ca 2+-reactivated Photosystem-II particles. Biochim Biophys Acta 808:225–230

    Article  CAS  Google Scholar 

  • Briantais JM, Ducruet JM, Hogdes M, Krause H (1992) Effects of high light at chilling temperature on photosystem II in spinach leaves. Photosynth Res 31:1–10

    Article  CAS  Google Scholar 

  • Briantais JM, Dacosta J, Goulas Y, Ducruet JM, Moya I (1996) Heat stress induces in leaves an increase of the minimum level of chlorophyll fluorescence, F0: a time-resolved analysis. Photosynth Res 48:189–196

    Article  CAS  Google Scholar 

  • Bukhov NG, Sabat SC, Mohanty P (1990) Analysis of chlorophyll a fluorescence changes in weak light in heat treated Amaranthus chloroplasts. Photosynth Res 23:81–87

    Article  CAS  Google Scholar 

  • Bukhov NG, Wiese C, Neimanis S, Heber U (1999) Heat sensitivity of chloroplasts and leaves: leakage of protons from thylakoids and reversible activation of cyclic electron transport. Photosynth Res 59:81–93

    Article  CAS  Google Scholar 

  • Bukhov N, Carpentier R (2004) Alternative Photosystem-I driven electron transport routes: mechanisms and functions. Photosynth Res 82:17–33

    Article  PubMed  CAS  Google Scholar 

  • Cao J, Govindjee (1990) Chlorophyll a fluorescence transient as an indicator of active and inactive Photosystem II in thylakoid membranes. Biochim Biophys Acta 1015:180–188

  • Chamberlain NR, Mehrtens BG, Xiong Z, Kapral FA, Boardman JL, Rearick JI (1991) Correlation of carotenoid production, decreased membrane fluidity, and resistance to oleic acid killing. Infect Immun 59:4332–4337

    PubMed  CAS  Google Scholar 

  • Clerc G, Thompson TE (1995) Permeability of dimyristoyl phosphatidylcholine/dipalmitoyl phosphatidylcholine bilayer membranes with coexisting gel and liquid-crystalline phases. Biophys J 68:2333–2341

    CAS  Google Scholar 

  • Colbow K (1973) Chlorophyll in phospholipid vesicles. Biochim Biophys Acta 318:4–9

    Article  PubMed  CAS  Google Scholar 

  • Demmig-Adams B, Adams WW III (2000) Harvesting sunlight safely. Nature 403:371–374

    Article  PubMed  CAS  Google Scholar 

  • DeVault D, Govindjee (1990) Photosynthetic glow peaks and their relationship with the free energy changes. Photosynth Res 24:175–181

  • DeVault D, Govindjee, Arnold W (1983) Energetics of photosynthesis glow peaks. Proc Natl Acad Sci USA 80:983–987

  • Downton WJS, Berry JA (1982) Chlorophyll fluorescence at high temperatures. Biochim Biophys Acta 679:474–478

    Article  CAS  Google Scholar 

  • Downton WJS, Berry JA, Seemann R (1984) Tolerance of photosynthesis to high temperature in desert plants. Plant Physiol 74:786–790

    PubMed  CAS  Google Scholar 

  • Ducruet JM (1999) Relation between the heat-induced increase of F0 fluorescence and a shift of the electronic equilibrium at the acceptor side of photosystem 2. Photosynthetica 37:335–338

    Article  CAS  Google Scholar 

  • Ducruet JM (2003) Chlorophyll thermoluminescence of leaf discs: simple instruments and progress in signal interpretation open the way to new ecophysiological indicators. J Exp Bot 54:2419–2430

    Article  PubMed  CAS  Google Scholar 

  • Ducruet JM, Lemoine Y (1985) Increased heat sensitivity of the photosynthetic apparatus in triazine-resistant biotypes from different plant species. Plant Cell Physiol 26:419–429

    CAS  Google Scholar 

  • Ducruet JM, Miranda T (1992) Graphical and numerical analysis of thermoluminescence and fluorescence F0 emission from photosynthetic material. Photosynth Res 33:15–27

    Article  CAS  Google Scholar 

  • Ducruet JM, Roman M, Havaux M, Janda T, Gallais A (2005) Cyclic electron flow around PS-I monitored by afterglow luminescence in leaves of maize inbred lines (Zea mays L.): correlation with chilling tolerance. Planta 221:567–579

    Article  PubMed  CAS  Google Scholar 

  • Fork DC, Murata N (1990) The effect of light intensity on the assay of the low temperature limit of photosynthesis using msec delayed light emission. Photosynth Res 23:319–323

    Article  Google Scholar 

  • Fork DC, Mohanty P, Hoshina S (1985) The detection of early events in heat disruption of thylakoid membranes by delayed light emission. Physiol Veg 23:511–521

    CAS  Google Scholar 

  • Fork DC, Van Ginkel G, Harvey G (1981) Phase transition temperature determined for chloroplast thylakoid membranes and for lyposomes prepared from charged lipid extracted from thylakoid membranes of higher plants. Plant Cell Physiol 22:1035–1042

    CAS  Google Scholar 

  • Franck F, Juneau P, Popovic R (2002) Resolution of the Photosystem I and Photosystem II contributions to chlorophyll fluorescence in intact leaves at room temperature. Biochim Biophys Acta 1556:239–246

    Article  PubMed  CAS  Google Scholar 

  • Georgieva K, Yordanov I (1993) Temperature dependence of chlorophyll fluorescence parameters of pea seedlings. J Plant Physiol 142:151–155

    CAS  Google Scholar 

  • Glémin A, Miranda T, Ducruet JM (1992) Temperature behavior of photosystem II in chilling-resistant and chilling-susceptible plant species, studied by fluorescence and luminescence methods. In: Murata N (ed) Research in photosynthesis, vol IV. Kluwer, Utrecht, pp 185–188

    Google Scholar 

  • Gounaris K, Brain APR, Quinn PJ, Williams WP (1984) Structural reorganization of chloroplast thylakoid membranes in response to heat stress. Biochim Biophys Acta 766:198–208

    Article  CAS  Google Scholar 

  • Govindjee (1995) Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 22:131–160

  • Gruszecki WI, Strzalka K (1991) Does the xanthophylls cycle take part in the regulation of fluidity of the thylakoid membrane? Biochim Biophys Acta 1060:310–314

    Article  CAS  Google Scholar 

  • Gruszecki WI, Strzalka K (2005) Carotenoids as modulators of lipid membrane physical properties. Biochim Biophys Acta 1740:108–115

    PubMed  CAS  Google Scholar 

  • Haldimann P, Feller U (2005) Growth at moderately elevated temperature alters the physiological response of the photosynthetic apparatus to heat stress in pea (Pisum sativum L.) leaves. Plant Cell Environ 28:302–317

    Article  CAS  Google Scholar 

  • Harvey GW, Gusta LV, Fork DC, Berry JA (1982) The relationship between membrane lipid phase separation and frost tolerance of cereals and other cool climate plant species. Plant Cell Environ 5:241–244

    CAS  Google Scholar 

  • Havaux M (1992) Stress tolerance of photosystem II in vivo. Antagonistic effects of water, heat and photoinhibition stresses. Plant Physiol 100:424–432

    PubMed  CAS  Google Scholar 

  • Havaux M (1993) Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures. Plant Cell Environ 16:461–467

    Article  Google Scholar 

  • Havaux M (1995) Temperature sensitivity of the photochemical function of photosynthesis in potato (Solanum tuberosum) and a cultivated Andean hybrid (Solanum x juzepczukii). J Plant Physiol 146:47–53

    CAS  Google Scholar 

  • Havaux M (1996) Short-term response of photosystem I to heat stress. Photosynth Res 47:85–97

    Article  CAS  Google Scholar 

  • Havaux M (1998) Carotenoids as membrane stabilizers in chloroplasts. Trends Plant Sci 3:147–151

    Article  Google Scholar 

  • Havaux M (2003) Spontaneous and thermoinduced photon emission: new methods to detect and quantify oxidative stress in plants. Trends Plant Sci 8:409–413

    Article  PubMed  CAS  Google Scholar 

  • Havaux M, Gruszecki WI (1993) Heat- and light-induced chlorophyll a fluorescence changes in potato leaves containing high or low levels of the carotenoid zeaxanthin: indications of a regulatory effect of zeaxanthin on thylakoid membrane fluidity. Photochem Photobiol 58:607–614

    CAS  Google Scholar 

  • Havaux M, Lannoye R (1983) Temperature dependence of delayed chlorophyll fluorescence in intact leaves of higher plants. A rapid method for detecting the phase transition of thylakoid membrane lipids. Photosynth Res 4:257–263

    CAS  Google Scholar 

  • Havaux M, Tardy F (1996) Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments. Planta 198:324–333

    Article  CAS  Google Scholar 

  • Havaux M, Ernez M, Lannoye R (1988) Correlation between heat tolerance and drought tolerance in cereals demonstrated by rapid chlorophyll fluorescence tests. J Plant Physiol 133:555–560

    CAS  Google Scholar 

  • Havaux M, Rumeau D, Ducruet JM (2005a) Probing the FQR and NDH activities involved in cyclic electron transport around Photosystem I by the “afterglow” luminescence. Biochim Biophys Acta 1709:203–213

    Article  CAS  Google Scholar 

  • Havaux M, Eymery F, Rey P, Porfirova S, Dörmann P (2005b) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17:3451–3469

    Article  CAS  Google Scholar 

  • Havaux M, Tardy F, Ravenel J, Chanu D, Parot P (1996) Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochromic shift in intact potato leaves: influence of xanthophylls content. Plant Cell Environ 19:1359–1368

    Article  CAS  Google Scholar 

  • Hays LM, Crowe JH, Wolkers W, Rudenko S (2001) Factors affecting leakage of trapped solutes from phospholipids vesicles during thermotropic phase transitions. Cryobiology 42:88–102

    Article  PubMed  CAS  Google Scholar 

  • Heckathorn SA, Downs CA, Sharkey TD, Coleman JS (1998) The small, methionine-rich chloroplast heat-shock protein protects photosystem II electron transport during heat stress. Plant Physiol 116:439–444

    Article  PubMed  CAS  Google Scholar 

  • Homann PH (1999) Reliability of photosystem II thermoluminescence measurements after sample freezing: few artifacts with Photosystem II membranes but gross distortions with certain leaves. Photosynth Res 62:219–229

    Article  CAS  Google Scholar 

  • Houghton JT et al. (2001) Climate Change 2001: the Scientific Basis. Cambridge University Press, Cambridge, UK, pp 1–881

    Google Scholar 

  • Hüve K, Bichele I, Tobias M, Niinemets U (2006) Heat sensitivity of photosynthetic electron transport varies during the day due to changes in sugars and osmotic potential. Plant Cell Environ 29:212–228

    Article  PubMed  CAS  Google Scholar 

  • Iba K (2002) Acclimative response to temperature stress in higher plants: approaches of gene engineering to temperature tolerance. Annu Rev Plant Biol 53:225–245

    Article  PubMed  CAS  Google Scholar 

  • Ilik P, Kouril R, Kruk J, Mysliwa-Kurdziel B, Popelkova H, Strzalka K, Naus J (2003) Origin of chlorophyll fluorescence in plants at 55–75°C. Photochem Photobiol 77:68–76

    Article  PubMed  CAS  Google Scholar 

  • Ivanov AG, Velitchkova MY (1990) Heat-induced changes in the efficiency of P700 photo-oxidation in pea chloroplast membranes. J Photochem Photobiol B-Biol 4:307–320

    Article  CAS  Google Scholar 

  • Ivanov AG, Sane P, Hurry H, Krol M, Sveshnikov D, Huner NPA, Öquist G (2003) Low-temperature modulation of the redox properties of the acceptor side of photosystem II: photoprotection through reaction centre quenching of excess energy. Physiol Plant 119:376–383

    Article  CAS  Google Scholar 

  • Janda T, Szalai G, Papp N, Pal M, Paldi E (2004) Effect of freezing on thermoluminescence in various plant species. Photochem Photobiol 80:525–530

    Article  PubMed  CAS  Google Scholar 

  • Joet T, Cournac L, Peltier G, Havaux M (2002) Cyclic electron transport around photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. Plant Physiol 128:760–769

    Article  PubMed  CAS  Google Scholar 

  • Kobza J, Edwards GE (1987) Influence of leaf temperature on photosynthetic carbon metabolism in wheat. Plant Physiol 83:69–74

    PubMed  CAS  Google Scholar 

  • Kouril R, Lazar D, Ilik P, Skotnica J, Krchnak P, Naus J (2004) High-temperature induced chlorophyll fluorescence rise in plants at 40–50 °C: experimental and theoretical approach. Photosynth Res 81:49–66

    Article  PubMed  CAS  Google Scholar 

  • Kratsch HA, Wise RR (2000) The ultrastructure of chilling stress. Plant Cell Environ 23:337–350

    Article  CAS  Google Scholar 

  • Krieger A, Weis E, Demeter S (1993) Low-pH-induced Ca2+ ion release in the water-splitting system is accompanied by a shift in the midpoint redox potential of the primary quinone acceptor QA. Biochim Biophys Acta 1144:411–418

    Article  CAS  Google Scholar 

  • Krieger A, Bolte S, Dietz KJ, Ducruet JM (1998) Thermoluminescence studies on the facultative CAM plant Mesembryanthenum crystallinum L. Planta 205:587–594

    Article  CAS  Google Scholar 

  • Krivosheeva AA, Venediktov PS, Alekseev AA (1992) High-temperature fluorescence of chlorophyll in plant tissues and chloroplasts isolated from them. Soviet Plant Physiol 39:47–50

    Google Scholar 

  • Ladjal M, Epron D, Ducrey M (2000) Effects of drought preconditioning on thermotolerance of photosystem II and susceptibility of photosynthesis to heat stress in cedar seedlings. Tree Physiol 20:1235–1241

    PubMed  CAS  Google Scholar 

  • Larcher W, Wagner J, Thammathaworn A (1990) Effects of superimposed temperature stress on in vivo chlorophyll fluorescence of Vigna unguiculata under saline stress. J Plant Physiol 136:92–102

    CAS  Google Scholar 

  • Lavorel J (1969) On a relation between fluorescence and luminescence in photosynthetic systems. Prog Photosynth Res 2:883–898

    CAS  Google Scholar 

  • Law RD, Crafts-Brandner SJ (1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of ribulose-1,5-biphosphate carboxylase/oxygenase. Plant Physiol 120:173–181

    Article  PubMed  CAS  Google Scholar 

  • Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:1781–1787

    Article  PubMed  CAS  Google Scholar 

  • Mannar Mannan R, Periyanan S, Kulandaivelu G, Bose S (1986) Species specific chlorophyll a fluorescence-temperature profile at high temperatures in leaves. Photosynth Res 8:87–92

    Article  Google Scholar 

  • Melcarek PK, Brown GN (1977) Effects of chill stress on prompt and delayed chlorophyll fluorescence from leaves. Plant Physiol 60:822–825

    PubMed  CAS  Google Scholar 

  • Miranda T, Ducruet JM (1995) Characterization of the chlorophyll thermoluminescence afterglow in dark-adapted or far-red-illuminated plant leaves. Plant Physiol Biochem 33:689–699

    CAS  Google Scholar 

  • Monson RK, Jaeger CH, Adams WW, Driggers EM, Silver GM, Fall R (1992) Relationship among isoprene emission rate, photosynthesis, and isoprene synthase activity as influenced by temperature. Plant Physiol 98:1175–1180

    PubMed  CAS  Google Scholar 

  • Murata N, Fork DC (1975) Temperature dependence of chlorophyll a fluorescence in relation to the physical phase of membrane lipids in algae and higher plants. Plant Physiol 56:791–796

    PubMed  CAS  Google Scholar 

  • Murata N, Troughton JH, Fork DC (1975) Relationships between the transition of the physical phase of membrane lipids and photosynthetic parameters in Anacystis nidulans and lettuce and spinach chloroplasts. Plant Physiol 56:508–517

    PubMed  CAS  Google Scholar 

  • Neuner G, Pramsohler M (2006) Freezing and high temperature thresholds of photosystem 2 compared to ice nucleation, frost and heat damage in evergreen subalpine plants. Physiol Plant 126:196–204

    Article  CAS  Google Scholar 

  • Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47:541–568

    Article  PubMed  CAS  Google Scholar 

  • Ono T, Murata N (1977) Temperature dependence of the delayed fluorescence of chlorophyll a in blue-green algae. Biochim Biophys Acta 460:220–229

    Article  PubMed  CAS  Google Scholar 

  • Palmqvist K, Sundblad LG, Samuelsson G, Sundbom E (1986) A correlation between changes in luminescence decay kinetics and the appearance of a CO2-accumulating mechanism in Scenedesmus obliquus. Photosynth Res 10:113–123

    Article  Google Scholar 

  • Pastenes C, Horton P (1996) Effect of high temperature on photosynthesis in beans. Plant Physiol 112:1245–1260

    PubMed  CAS  Google Scholar 

  • Pearcy RW, Berry JA, Fork DC (1977) Effects of growth temperature on the thermal stability of the photosynthetic apparatus of Atriplex lentiformis (Torr.) Wats. Plant Physiol 59:873–878

    PubMed  CAS  Google Scholar 

  • Penuelas J, Munné-Bosch S (2005) Isoprenoids: an evolutionary pool for photoprotection. Trends Plant Sci 10:166–169

    Article  PubMed  CAS  Google Scholar 

  • Penuelas J, Llusia J, Asensio D, Munné-Bosch S (2005) Linking isoprene with plant thermotolerance, antioxidants and monoterpene emissions. Plant Cell Environ 28:278–286

    Article  CAS  Google Scholar 

  • Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53:523–550

    Article  PubMed  CAS  Google Scholar 

  • Pospisil P, Skotnica J, Naus J (1998) Low and high temperature dependence of minimum Fo and maximum FM chlorophyll fluorescence in vivo. Biochim Biophys Acta 1363:95–98

    Article  PubMed  CAS  Google Scholar 

  • Pospisil P, Tyystjärvi E (1999) Molecular mechanisms of high-temperature-induced inhibition of acceptor side of Photosystem II. Photosynth Res 62:55–66

    Article  CAS  Google Scholar 

  • Raison JK, Orr GR (1986) Phase transitions in thylakoid polar lipids of chilling-sensitive plants. A comparison of detection methods. Plant Physiol 80:638–645

    PubMed  CAS  Google Scholar 

  • Raison JK, Roberts JKM, Berry JA (1982) Correlations between the thermal stability of chloroplast (thylakoid) membranes and the composition and fluidity of their polar lipids upon acclimation of the higher plant, Nerium oleander, to growth temperature. Biochim Biophys Acta 688:218–228

    Article  CAS  Google Scholar 

  • Rappaport F, Cuni A, Xiong L, Sayre R, Lavergne J (2005) Charge recombination and thermoluminescence in photosystem II. Biophys J 88:1948–1958

    Article  PubMed  CAS  Google Scholar 

  • Rekika D, Monneveux P, Havaux M (1997) The in vivo tolerance of photosynthetic membranes to high and low temperatures in cultivated and wild wheats of the Triticum and Aegilops genera. J Plant Physiol 150:734–738

    CAS  Google Scholar 

  • Rokka A, Aro EM, Herrmann RG, Anderson B, Vener AV (2000) Dephosphorylation of PS-II in plant photosynthetic membranes as an intermediate response to abrupt elevation of temperature. Plant Physiol 123:1525–1535

    Article  PubMed  CAS  Google Scholar 

  • Rottem S, Markowitz O (1979) Carotenoids act as reinforcers of the Acholeplasma laidlawii. J Bacteriol 140:944–948

    PubMed  CAS  Google Scholar 

  • Ruban R, Trach VV (1991) Heat-induced reversible changes in Photosystem I absorption cross-section of pea chloroplasts and sub-chloroplast preparations. Evidence from excitation fluorescence spectra. Photosynth Res 29:157–169

    CAS  Google Scholar 

  • Rutherford AW, Govindjee, Inoue Y (1984) Charge accumulation and photochemistry in leaves studied by thermoluminescence and delayed light emission. Proc Natl Acad Sci USA 81:1107–1111

  • Sane PV, Desai TS, Tatake G, Govindjee (1984) Heat induced reversible increase in Photosystem I emission in algae, leaves and chloroplasts: spectra, activities and relation to state changes. Photosynthetica 18:439–444

  • Sane P, Rutherford AW (1986) Thermoluminescence from photosynthetic membranes. In: Govindjee, Amesz J, Fork DC (eds) Light emission by plants and bacteria. Academic Press, Orlando, pp 291–329

  • Sasaki K, Ohara K, Yazaki K (2005) Gene expression and characterization of isoprene synthase from Populus alba. FEBS Lett 579:2514–2518

    Article  PubMed  CAS  Google Scholar 

  • Schrader SM, Wise RR, Wacholtz WF, Ort DR, Sharkey TD (2004) Thylakoid membrane responses to moderately high leaf temperature in Pima cotton. Plant Cell Environ 27:725–735

    Article  CAS  Google Scholar 

  • Schreiber U, Armond PA (1978) Heat-induced changes of chlorophyll fluorescence in isolated chloroplasts and related heat-damage at the pigment level. Biochim Biophys Acta 502:138–151

    Article  PubMed  CAS  Google Scholar 

  • Schreiber U, Berry JA (1977) Heat-induced changes in chlorophyll fluorescence in intact leaves correlated with damage of the photosynthetic apparatus. Planta 136:233–238

    Article  CAS  Google Scholar 

  • Seeman JR, Downton WJS, Berry JA (1986) Temperature and leaf osmotic potential as factors in the acclimation of photosynthesis to high temperature in desert plants. Plant Physiol 80:926–930

    Google Scholar 

  • Sharkey TD (2005) Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, Rubisco activation, reactive oxygen species, and thermotolerance provided by isoprene. Plant Cell Environ 28:269–277

    Article  CAS  Google Scholar 

  • Singsaas EL, Lerdau M, Winter K, Sharkey TD (1997) Isoprene increases thermotolerance of isoprene-emitting species. Plant Physiol 115:1413–1420

    PubMed  CAS  Google Scholar 

  • Singsaas EL, Sharkey TD (2000) The effects of high temperature on isoprene synthesis in oak leaves. Plant Cell Environ 23:751–757

    Article  CAS  Google Scholar 

  • Smillie RM, Nott R (1979) Heat injury in leaves of alpine, temperature and tropical plants. Aust J Plant Physiol 6:135–141

    Article  CAS  Google Scholar 

  • Sundblad LG, Schröder WP, Akerlung HE (1988) S-state distribution and redox state of QA in barley in relation to luminescence decay kinetics. Biochim Biophys Acta 973:47–52

    Google Scholar 

  • Sundbom E, Strand M, Hällgreen JE (1982) Temperature-induced fluorescence changes. A screening method for frost tolerance of potato (Solanum sp.). Plant Physiol 70:1299–1302

    PubMed  Google Scholar 

  • Sundby C, Melis A, Mäenpää P, Andersson B (1986) Temperature-dependent changes in the antenna size of photosystem II. Reversible conversion of photosystem IIα to photosystem IIβ. Biochim Biophys Acta 851:475–483

    Article  CAS  Google Scholar 

  • Tardy F, Havaux M (1997) Thylakoid membrane fluidity and thermostability during the operation of the xanthophylls cycle in higher-plant chloroplasts. Biochim Biophys Acta 1330:179–193

    Article  PubMed  CAS  Google Scholar 

  • Terzaghi WB, Fork DC, Berry JA, Field CB (1989) Low and high temperature limits to PSII. Plant Physiol 91:1494–1500

    PubMed  CAS  Google Scholar 

  • Tyystjärvi E, Vass I (2003) Light emission as a probe of charge separation and recombination in the photosynthetic apparatus: relation of prompt fluorescence to delayed light emission and thermoluminescence. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a probe of photosynthesis. Springer, Dordrecht, The Netherlands, pp 363–388

  • Valladares F, Pearcy RW (1997) Interactions between water stress, sun-shade acclimation, heat tolerance and photoinhibition in the sclerophyll Heteromeles arbutifolia. Plant Cell Environ 20:25–36

    Article  Google Scholar 

  • Vass I, Horvath G, Herczeg T, Demeter S (1981) Photosynthetic energy conservation investigated by thermoluminescence activation energies and half-lives of thermoluminescence bands of chloroplasts determined by mathematical resolution of glow curve. Biochim Biophys Acta 634:140–152

    Article  PubMed  CAS  Google Scholar 

  • Vass I, Govindjee (1996) Thermoluminescence of the photosynthetic apparatus. Photosynth Res 48:117–126

  • Vavilin DV, Matorin DN, Kafarov RS, Bautina AL, Venediktov PS (1991) High-temperature thermoluminescence of chlorophyll in lipid peroxidation. Biologischke Membranyii 8:89–98

    Google Scholar 

  • Velikova V, Loreto F (2005) On the relationship between isoprene emission and thermotolerance in Phragmites australis leaves exposed to high temperatures and during the recovery from a heat stress. Plant Cell Environ 28:318–327

    Article  CAS  Google Scholar 

  • Wada H, Gombos Z, Murata N (1990) Enhancement of chilling tolerance of a cyanobacterium by genetic manipulation of fatty acid desaturation. Nature 347:200–203

    Article  PubMed  CAS  Google Scholar 

  • Weis E (1984) Short term acclimation of spinach to high temperatures. Plant Physiol 74:402–407

    Article  PubMed  CAS  Google Scholar 

  • Weis E (1985) Light- and temperature-induced changes in the distribution of excitation energy between Photosystem I and Photosystem II in spinach leaves. Biochim Biophys Acta 807:118–126

    Article  CAS  Google Scholar 

  • Wiest SC (1986) Kinetic and proteolytic identification of heat-induced conformational changes in the urea herbicide binding site of isolated Phaseolus vulgaris chloroplast thylakoids. Physiol Plant 66:527–535

    Article  CAS  Google Scholar 

  • Williams WP, Brain APR, Dominy PJ (1992) Induction of non-bilayer lipid phase separation in chloroplats thylakoid membranes by compatible co-solutes and its relation to the thermal stability of photosystem II. Biochim Biophys Acta 1099:137–144

    Article  CAS  Google Scholar 

  • Yamane Y, Kashino Y, Koike H, Satoh K (1997) Increases in the fluorescence F0 level and reversible inhibition of Photosystem II reaction center by high-temperature treatments in higher plants. Photosynth Res 52:57–64

    Article  CAS  Google Scholar 

  • Yordanov I, Dilova S, Petkova R, Pangelova T, Goltsev V, Suss KH (1986) Mechanisms of the temperature damage and acclimation of the photosynthetic apparatus. Photobiochem Photobiophys 12:147–155

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Service de Bioénergétique, INRA-CEA Saclay, 91191, Gif-sur-Yvette cedex, France

    Jean-Marc Ducruet

  2. ESE, Biospectroscopie Végétale, Université Paris-Sud, 91405, Orsay, France

    Jean-Marc Ducruet

  3. Institute of Plant Physiology, BAS, G. Bonchev str., Bl. 21, Sofia, 1113, Bulgaria

    Violeta Peeva

  4. CEA/Cadarache, DSV, IBEB, SBVME, Laboratoire d’Ecophysiologie Moléculaire des Plantes, UMR 6191 CNRS-CEA-Aix Marseille Univ., 13108, Saint-Paul-lez-Durance, France

    Michel Havaux

Authors
  1. Jean-Marc Ducruet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Violeta Peeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michel Havaux
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jean-Marc Ducruet.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ducruet, JM., Peeva, V. & Havaux, M. Chlorophyll thermofluorescence and thermoluminescence as complementary tools for the study of temperature stress in plants. Photosynth Res 93, 159–171 (2007). https://doi.org/10.1007/s11120-007-9132-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-007-9132-x

Keywords

Search

Navigation