Photosynthesis Research

, Volume 85, Issue 2, pp 191–203 | Cite as

Comparative Study on the Changes in Photosynthetic Activity of the Homoiochlorophyllous Desiccation-Tolerant Haberlea Rhodopensis and Desiccation-Sensitive Spinach Leaves During Desiccation and Rehydration

  • Katya GeorgievaEmail author
  • Liliana Maslenkova
  • Violeta Peeva
  • Yuliana Markovska
  • Detelin Stefanov
  • Zoltan Tuba
Regular paper


The functional peculiarities and responses of the photosynthetic system in the flowering homoiochlorophyllous desiccation-tolerant (HDT) Haberlea rhodopensis and the non-desiccation-tolerant spinach were compared during desiccation and rehydration. Increasing rate of water loss clearly modifies the kinetic parameters of fluorescence induction, thermoluminescence emission, far-red induced P700 oxidation and oxygen evolution in the leaves of both species. The values of these parameters returned nearly to the control level after 24 h rehydration only of the leaves of HDT plant. PS II was converted in a non-functional state in desiccated spinach in accordance with the changes in membrane permeability, malondialdehyde, proline and H2O2 contents. Moreover, our data showed a strong reduction of the total number of PS II centers in Haberlea without any changes in the energetics of the charge recombination. We consider this observation, together with the previously reported unusually high temperature of B-band (S2QB-) emission of Haberlea to reflect some specific adaptive characteristics of the photosynthetic system. As far as we know this is the first time when such adaptive characteristics and mechanism of the photosynthetic system of a flowering HDT higher plant is described. These features of Haberlea can explain the fast recovery of its photosynthesis after desiccation, which enable this HDT plant to rapidly take advantage of frequent changes in water availability.


chlorophyll fluorescence desiccation tolerant plant drought stress photosynthesis thermoluminescence 




DT plants

desiccation tolerant plants

HDT plants

homoiochlorophyllous desiccation tolerant plants

F0, Fm

minimum and maximum dark adapted fluorescence yield, respectively


maximum light adapted fluorescence yield


quantum yield of Photosystem II photochemistry in the dark adapted state


efficiency of excitation capture by open Photosystem II reaction centers

FR light

far-red light


fresh weight



PDT plants

poikilochlorophyllous desiccation tolerant plants


photochemical quenching


quantum yield of Photosystem II photochemistry in the light adapted state


Photosystem I


Photosystem II


fluorescence decrease ratio


relative humidity


relative water content




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  1. Alpert P and Oliver MJ (2002) Drying without dying. In: Black M, and Pritchard (eds) Desiccation and Survival in Plants: Drying without Dying, pp 3–31. CABI PublishingGoogle Scholar
  2. Bates, LS, Waldren, RP, Teare, JD 1973Rapid determination of proline for water stress studiesPlant Soil39205207CrossRefGoogle Scholar
  3. Bernacchia, G, Salamini, F, Bartels, D 1996Molecular characterization of the rehydration process in the resurrection plant Craterostigma plantagineumPlant Physiol11110431050PubMedGoogle Scholar
  4. Bewley, JD 1979Physiological aspects of desiccation toleranceAnnu Rev Plant Physiol30195238CrossRefGoogle Scholar
  5. Boyer, JS 1970Leaf enlargement and metabolic rates in corn, soybean, and sunflower at various leaf water potentialPlant Physiol46233235Google Scholar
  6. Chow, WS, Hope, AB 2004Electron fluxes through Photosystem I in cucumber leaf discs probed at far-red lightPhotosynth Res817789CrossRefGoogle Scholar
  7. Deng, X, Hu, Z-A, Wang, H-X, Wen, X-G, Kuang, T-Y 2003A comparison of photosynthetic apparatus of the detached leaves of the resurrection plant Boea hygrometrica with its non-tolerant relative Chirita heterotrichia in response to dehydration and rehydrationPlant Sci165851861CrossRefGoogle Scholar
  8. Dhindsa, RS, Plumb-Dhindsa, P, Trorpe, TA 1981Leaf senescence correlated with increased levels of membrane permeability and lipid peroxidation and decreased level of superoxide dismutase and catalaseJ Exp Bot3293101Google Scholar
  9. Drazic, G, Mihailovic, N, Stevanovic, B 1999Chlorophyll metabolism in leaves of higher poikilohydric plants Ramonda service Panc. and Ramonda nathaliae Panc. during dehydration and rehydrationJ Plant Physiol154379384Google Scholar
  10. Ducruet, J-M 2003Chlorophyll thermoluminescence of leaf disks: simple instruments and progress in signal interpretation open the way to new ecophysiological indicatorsJ Exp Bot5424192430PubMedGoogle Scholar
  11. Farrant, JM, Cooper, K, Kruger, LA, Sherwin, HW 1999The effect of drying rate on the survival of three desiccation-tolerant angiosperm speciesAnn Bot84371379CrossRefGoogle Scholar
  12. Farrant, GM, Willingen, CV, Loffell, DA, Bartsch, S, Whittaker, A 2003An investigation into the role of light during desiccation of three angiosperm resurrection plantsPlant Cell Environ2612751286CrossRefGoogle Scholar
  13. Gaff, DF 1971Desiccation tolerant plants in Southern AfricaScience17410331034Google Scholar
  14. Genty, B, Briantais, J-M, Baker, NR 1989The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescenceBiochim Biophys Acta9908792Google Scholar
  15. Georgieva, K, Fedina, I, Maslenkova, L, Peeva, V 2003Response of chlorina barley mutants to heat stress under low and high lightFunct Plant Biol30515524CrossRefGoogle Scholar
  16. Giardi, MT, Cona, A, Geiken, B, Kucera, T, Masojidek, J, Mattoo, AK 1996Long-term drought stress induces structural and functional reorganization of Photosystem IIPlanta199118125CrossRefGoogle Scholar
  17. Govindjee, , Koike, H, Ynoue, Y 1985Thermoluminescence and oxygen evolution from a thermophilic blue-green alga obtained after single-turnover light flashesPhotochem Photobiol42579585Google Scholar
  18. Hoekstra, FA, Golovina, EA, Buitink, J 2001Mechanisms of plant desiccation toleranceTrend Plant Sci6431438CrossRefGoogle Scholar
  19. Irigoyen, JJ, Ernerich, DW, Sanchez-Dias, M 1992Water stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plantsPhysiol Plant845560CrossRefGoogle Scholar
  20. Kitajima, H, Butler, WL 1975Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinoneBiochimica Biophysica Acta376105115Google Scholar
  21. Klughammer C and Schreiber U (1998). Measuring P700 absorbance changes in the near infrared region with a dual wavelength pulse modulation system. In: Garab G (ed.), Photosynthesis: Mechanisms and Effects, pp 4357–4360. Kluwer Academic PublishersGoogle Scholar
  22. Lawlor, DW, Cornic, G 2002Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plantsPlant Cell Environ25275294CrossRefPubMedGoogle Scholar
  23. Lichtenthaler HK and Rinderle U (1988). Chlorophyll fluorescence signatures as vitality indicator in forest decline research. In: Lichtenthaler HK (ed.), Application of Chlorophyll Fluorescence in Photosynthesis Research, Stress Physiology, Hydrobiology and Remote Sensing, pp 143–149. Kluwer Academic PublishersGoogle Scholar
  24. Lichtenthaler, KH 1987Chlorophylls and carotenoids: pigments of photosynthetic biomembranesMeth Enzymol148350382Google Scholar
  25. Lu, C, Zhang, J 1998Effects of water stress on photosynthesis, chlorophyll fluorescence and photoinhibition in wheat plantsAust J Plant Physiol25883892Google Scholar
  26. Mannuel, N, Cornic, G, Aubert, S, Choler, P, Bligny, R, Heber, U 1999Protection against photoinhibition in the alpine plant Geum montanumOecologia119149158CrossRefGoogle Scholar
  27. Maslenkova, L, Homann, P 2000Stabilized S2 state in leaves of the desiccation tolerant resurrection fern Polipodium polipodioidesCR Bulg Acad Sci5399102Google Scholar
  28. Peeva, V, Maslenkova, L 2004Thermoluminescence study of Photosystem II activity in Haberlea rhodopensis and spinach leaves during desiccationPlant Biol616CrossRefGoogle Scholar
  29. Proctor, MCF, Tuba, Z 2002Poikilohydry and homoihydry: antithesis or spectrum of possibilities?New Phytologist156327349CrossRefGoogle Scholar
  30. Quartacci, MF, Glisic, O, Stevanovic, B, Navari-Izzo, F 2002Plasma membrane lipids in the resurrection plant Ramonda serbica following dehydration and rehydrationJ Exp Bot5321592166CrossRefPubMedGoogle Scholar
  31. Ramanjulu, S, Bartels, D 2002Drought- and desiccation-induced modulation of gene expression in plantsPlant Cell Environ25141151CrossRefPubMedGoogle Scholar
  32. Sane, PV, Rutherford, AW 1986Thermoluminescence from photosynthetic membranesGovindjee, Amesz JFork, DC eds. Light Emission by Plants and BacteriaAcademic PressNew York329361Google Scholar
  33. Sass, L, Csintalan, Zs, Tuba, Z, Vass, I 1996Thermoluminescence studies on the function of Photosystem II in the desiccation tolerant lichen Cladonia convolutaPhotosynth Res48205212CrossRefGoogle Scholar
  34. Schwab, KB, Schreiber, U, Heber, U 1989Response of photosynthesis and respiration of resurrection plants to desiccation and rehydrationPlanta177217227CrossRefGoogle Scholar
  35. Scotnica, J, Matouskova, M, Naus, J, Lazar, D, Dvorak, L 2000Thermoluminescense and fluorescence study of changes in Photosystem II photochemistry in desiccating barley leavesPhotosynth Res652940CrossRefGoogle Scholar
  36. Scott, P 2000Resurrection plants and the secrets of eternal leafAnn Bot85159166CrossRefGoogle Scholar
  37. Sherwin, HW, Farrant, JM 1996Rehydration of three desiccation-tolerant speciesAnn Bot78703710CrossRefGoogle Scholar
  38. Sherwin, HW, Farrant, JM 1998Protection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscosePlant Growth Regul24203210CrossRefGoogle Scholar
  39. Souza, RP, Machado, EC, Silva, JAB, Lagoa, AMMA, Silveira, JAG 2004Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recoveryEnviron Exp Bot514556CrossRefGoogle Scholar
  40. Tuba, Z, Lichtenthaler, HK, Csintalan, Zs, Nagy, Z, Szente, K 1996Loss of chlorophylls, cessation of photosynthetic CO2 assimilation and respiration in the poikilochlorophyllous plant Xerophyta scabridaPhysiol Plant96383388CrossRefGoogle Scholar
  41. Tuba, Z, Proctor, MCF, Csintalan, Zs 1998Ecophysiological responses of homoiochlorophyllous and poikilochlorophyllous desiccation tolerant plants: a comparison and an ecological perspectivePlant Growth Regul24211217CrossRefGoogle Scholar
  42. Tyystjarvi, E, Karunen, J 1990A microcomputer program and fast analog to digital converter card for the analysis of fluorescence induction transientsPhotosynth Res2627132Google Scholar
  43. Vass, I, Govindjee,  1996Thermoluminescence from the photosynthetic apparatusPhotosynth Res48117126CrossRefGoogle Scholar
  44. Yang, W-L, Hu, Z-A, Wang, H-X, Kuang, T-Y 2003Photosynthesis of resurrection angiospermsActa Botanica Sinica45505508Google Scholar
  45. Zeinalov, Yu, Maslenkova, L 1996A computerised equipment for thermoluminescence investigationsBulg J Plant Physiol228894Google Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • Katya Georgieva
    • 1
    Email author
  • Liliana Maslenkova
    • 1
  • Violeta Peeva
    • 1
  • Yuliana Markovska
    • 2
  • Detelin Stefanov
    • 1
  • Zoltan Tuba
    • 3
  1. 1.Acad. M. Popov Institute of Plant PhysiologyBulgarian Academy of SciencesSofiaBulgaria
  2. 2.Faculty of BiologySofia UniversitySofiaBulgaria
  3. 3.Department of Botany and Plant Physiology, Faculty of Agriculture and Environmental SciencesSzent István UniversityGödöllöGödöllöHungary

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