Skip to main content

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

Abstract

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.

This is a preview of subscription content, access via your institution.

Abbreviations

Chl:

chlorophyll

DT plants:

desiccation tolerant plants

HDT plants:

homoiochlorophyllous desiccation tolerant plants

F0, Fm:

minimum and maximum dark adapted fluorescence yield, respectively

F′ m :

maximum light adapted fluorescence yield

Fv/Fm:

quantum yield of Photosystem II photochemistry in the dark adapted state

F′v/F′m:

efficiency of excitation capture by open Photosystem II reaction centers

FR light:

far-red light

FW:

fresh weight

MDA:

malondialdehyde

PDT plants:

poikilochlorophyllous desiccation tolerant plants

qP:

photochemical quenching

ΦPS II:

quantum yield of Photosystem II photochemistry in the light adapted state

PSI:

Photosystem I

PS II:

Photosystem II

Rfd:

fluorescence decrease ratio

RH:

relative humidity

RWC:

relative water content

TL:

thermoluminescence

References

  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 Publishing

  2. LS Bates RP Waldren JD Teare (1973) ArticleTitleRapid determination of proline for water stress studies Plant Soil 39 205–207 Occurrence Handle10.1007/BF00018060

    Article  Google Scholar 

  3. G Bernacchia F Salamini D Bartels (1996) ArticleTitleMolecular characterization of the rehydration process in the resurrection plant Craterostigma plantagineum Plant Physiol 111 1043–1050 Occurrence Handle12226346

    PubMed  Google Scholar 

  4. JD Bewley (1979) ArticleTitlePhysiological aspects of desiccation tolerance Annu Rev Plant Physiol 30 195–238 Occurrence Handle10.1146/annurev.pp.30.060179.001211

    Article  Google Scholar 

  5. JS Boyer (1970) ArticleTitleLeaf enlargement and metabolic rates in corn, soybean, and sunflower at various leaf water potential Plant Physiol 46 233–235

    Google Scholar 

  6. WS Chow AB Hope (2004) ArticleTitleElectron fluxes through Photosystem I in cucumber leaf discs probed at far-red light Photosynth Res 81 77–89 Occurrence Handle10.1023/B:PRES.0000028396.83954.36

    Article  Google Scholar 

  7. X Deng Z-A Hu H-X Wang X-G Wen T-Y Kuang (2003) ArticleTitleA 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 rehydration Plant Sci 165 851–861 Occurrence Handle10.1016/S0168-9452(03)00284-X

    Article  Google Scholar 

  8. RS Dhindsa P Plumb-Dhindsa TA Trorpe (1981) ArticleTitleLeaf senescence correlated with increased levels of membrane permeability and lipid peroxidation and decreased level of superoxide dismutase and catalase J Exp Bot 32 93–101

    Google Scholar 

  9. G Drazic N Mihailovic B Stevanovic (1999) ArticleTitleChlorophyll metabolism in leaves of higher poikilohydric plants Ramonda service Panc. and Ramonda nathaliae Panc. during dehydration and rehydration J Plant Physiol 154 379–384

    Google Scholar 

  10. J-M Ducruet (2003) ArticleTitleChlorophyll thermoluminescence of leaf disks: simple instruments and progress in signal interpretation open the way to new ecophysiological indicators J Exp Bot 54 2419–2430 Occurrence Handle14565948

    PubMed  Google Scholar 

  11. JM Farrant K Cooper LA Kruger HW Sherwin (1999) ArticleTitleThe effect of drying rate on the survival of three desiccation-tolerant angiosperm species Ann Bot 84 371–379 Occurrence Handle10.1006/anbo.1999.0927

    Article  Google Scholar 

  12. GM Farrant CV Willingen DA Loffell S Bartsch A Whittaker (2003) ArticleTitleAn investigation into the role of light during desiccation of three angiosperm resurrection plants Plant Cell Environ 26 1275–1286 Occurrence Handle10.1046/j.0016-8025.2003.01052.x

    Article  Google Scholar 

  13. DF Gaff (1971) ArticleTitleDesiccation tolerant plants in Southern Africa Science 174 1033–1034

    Google Scholar 

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

    Google Scholar 

  15. K Georgieva I Fedina L Maslenkova V Peeva (2003) ArticleTitleResponse of chlorina barley mutants to heat stress under low and high light Funct Plant Biol 30 515–524 Occurrence Handle10.1071/FP03024

    Article  Google Scholar 

  16. MT Giardi A Cona B Geiken T Kucera J Masojidek AK Mattoo (1996) ArticleTitleLong-term drought stress induces structural and functional reorganization of Photosystem II Planta 199 118–125 Occurrence Handle10.1007/BF00196888

    Article  Google Scholar 

  17. Govindjee H Koike Y Ynoue (1985) ArticleTitleThermoluminescence and oxygen evolution from a thermophilic blue-green alga obtained after single-turnover light flashes Photochem Photobiol 42 579–585

    Google Scholar 

  18. FA Hoekstra EA Golovina J Buitink (2001) ArticleTitleMechanisms of plant desiccation tolerance Trend Plant Sci 6 431–438 Occurrence Handle10.1016/S1360-1385(01)02052-0

    Article  Google Scholar 

  19. JJ Irigoyen DW Ernerich M Sanchez-Dias (1992) ArticleTitleWater stress induced changes in concentrations of proline and total soluble sugars in nodulated alfalfa (Medicago sativa) plants Physiol Plant 84 55–60 Occurrence Handle10.1034/j.1399-3054.1992.840109.x

    Article  Google Scholar 

  20. H Kitajima WL Butler (1975) ArticleTitleQuenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone Biochimica Biophysica Acta 376 105–115

    Google 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 Publishers

  22. DW Lawlor G Cornic (2002) ArticleTitlePhotosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants Plant Cell Environ 25 275–294 Occurrence Handle10.1046/j.0016-8025.2001.00814.x Occurrence Handle11841670

    Article  PubMed  Google 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 Publishers

  24. KH Lichtenthaler (1987) ArticleTitleChlorophylls and carotenoids: pigments of photosynthetic biomembranes Meth Enzymol 148 350–382

    Google Scholar 

  25. C Lu J Zhang (1998) ArticleTitleEffects of water stress on photosynthesis, chlorophyll fluorescence and photoinhibition in wheat plants Aust J Plant Physiol 25 883–892

    Google Scholar 

  26. N Mannuel G Cornic S Aubert P Choler R Bligny U Heber (1999) ArticleTitleProtection against photoinhibition in the alpine plant Geum montanum Oecologia 119 149–158 Occurrence Handle10.1007/s004420050771

    Article  Google Scholar 

  27. L Maslenkova P Homann (2000) ArticleTitleStabilized S2 state in leaves of the desiccation tolerant resurrection fern Polipodium polipodioides CR Bulg Acad Sci 53 99–102

    Google Scholar 

  28. V Peeva L Maslenkova (2004) ArticleTitleThermoluminescence study of Photosystem II activity in Haberlea rhodopensis and spinach leaves during desiccation Plant Biol 6 1–6 Occurrence Handle10.1055/s-2004-815737

    Article  Google Scholar 

  29. MCF Proctor Z Tuba (2002) ArticleTitlePoikilohydry and homoihydry: antithesis or spectrum of possibilities? New Phytologist 156 327–349 Occurrence Handle10.1046/j.1469-8137.2002.00526.x

    Article  Google Scholar 

  30. MF Quartacci O Glisic B Stevanovic F Navari-Izzo (2002) ArticleTitlePlasma membrane lipids in the resurrection plant Ramonda serbica following dehydration and rehydration J Exp Bot 53 2159–2166 Occurrence Handle10.1093/jxb/erf076 Occurrence Handle12379782

    Article  PubMed  Google Scholar 

  31. S Ramanjulu D Bartels (2002) ArticleTitleDrought- and desiccation-induced modulation of gene expression in plants Plant Cell Environ 25 141–151 Occurrence Handle10.1046/j.0016-8025.2001.00764.x Occurrence Handle11841659

    Article  PubMed  Google Scholar 

  32. PV Sane AW Rutherford (1986) Thermoluminescence from photosynthetic membranes Amesz J Govindjee DC Fork (Eds) Light Emission by Plants and Bacteria Academic Press New York 329–361

    Google Scholar 

  33. L Sass Zs Csintalan Z Tuba I Vass (1996) ArticleTitleThermoluminescence studies on the function of Photosystem II in the desiccation tolerant lichen Cladonia convoluta Photosynth Res 48 205–212 Occurrence Handle10.1007/BF00041010

    Article  Google Scholar 

  34. KB Schwab U Schreiber U Heber (1989) ArticleTitleResponse of photosynthesis and respiration of resurrection plants to desiccation and rehydration Planta 177 217–227 Occurrence Handle10.1007/BF00392810

    Article  Google Scholar 

  35. J Scotnica M Matouskova J Naus D Lazar L Dvorak (2000) ArticleTitleThermoluminescense and fluorescence study of changes in Photosystem II photochemistry in desiccating barley leaves Photosynth Res 65 29–40 Occurrence Handle10.1023/A:1006472129684

    Article  Google Scholar 

  36. P Scott (2000) ArticleTitleResurrection plants and the secrets of eternal leaf Ann Bot 85 159–166 Occurrence Handle10.1006/anbo.1999.1006

    Article  Google Scholar 

  37. HW Sherwin JM Farrant (1996) ArticleTitleRehydration of three desiccation-tolerant species Ann Bot 78 703–710 Occurrence Handle10.1006/anbo.1996.0180

    Article  Google Scholar 

  38. HW Sherwin JM Farrant (1998) ArticleTitleProtection mechanisms against excess light in the resurrection plants Craterostigma wilmsii and Xerophyta viscose Plant Growth Regul 24 203–210 Occurrence Handle10.1023/A:1005801610891

    Article  Google Scholar 

  39. RP Souza EC Machado JAB Silva AMMA Lagoa JAG Silveira (2004) ArticleTitlePhotosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery Environ Exp Bot 51 45–56 Occurrence Handle10.1016/S0098-8472(03)00059-5

    Article  Google Scholar 

  40. Z Tuba HK Lichtenthaler Zs Csintalan Z Nagy K Szente (1996) ArticleTitleLoss of chlorophylls, cessation of photosynthetic CO2 assimilation and respiration in the poikilochlorophyllous plant Xerophyta scabrida Physiol Plant 96 383–388 Occurrence Handle10.1034/j.1399-3054.1996.960305.x

    Article  Google Scholar 

  41. Z Tuba MCF Proctor Zs Csintalan (1998) ArticleTitleEcophysiological responses of homoiochlorophyllous and poikilochlorophyllous desiccation tolerant plants: a comparison and an ecological perspective Plant Growth Regul 24 211–217 Occurrence Handle10.1023/A:1005951908229

    Article  Google Scholar 

  42. E Tyystjarvi J Karunen (1990) ArticleTitleA microcomputer program and fast analog to digital converter card for the analysis of fluorescence induction transients Photosynth Res 26 27–132

    Google Scholar 

  43. I Vass Govindjee (1996) ArticleTitleThermoluminescence from the photosynthetic apparatus Photosynth Res 48 117–126 Occurrence Handle10.1007/BF00041002

    Article  Google Scholar 

  44. W-L Yang Z-A Hu H-X Wang T-Y Kuang (2003) ArticleTitlePhotosynthesis of resurrection angiosperms Acta Botanica Sinica 45 505–508

    Google Scholar 

  45. Yu Zeinalov L Maslenkova (1996) ArticleTitleA computerised equipment for thermoluminescence investigations Bulg J Plant Physiol 22 88–94

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Katya Georgieva.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Georgieva, K., Maslenkova, L., Peeva, V. et al. Comparative Study on the Changes in Photosynthetic Activity of the Homoiochlorophyllous Desiccation-Tolerant Haberlea Rhodopensis and Desiccation-Sensitive Spinach Leaves During Desiccation and Rehydration. Photosynth Res 85, 191–203 (2005). https://doi.org/10.1007/s11120-005-2440-0

Download citation

Keywords

  • chlorophyll fluorescence
  • desiccation tolerant plant
  • drought stress
  • photosynthesis
  • thermoluminescence