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Enhanced thermotolerance of photosystem II in salt-adapted plants of the halophyte Artemisia anethifolia

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Abstract

Thermotolerance of photosystem II (PSII) in leaves of salt-adapted Artemisia anethifolia L. plants (100–400 mM NaCl) was evaluated after exposure to heat stress (30–45°C) for 30 min. After exposure to 30°C, salt adaptation had no effects on the maximal efficiency of PSII photochemistry (Fv/Fm), the efficiency of excitation capture by open PSII centers (Fv′/Fm′), or the actual PSII efficiency (ΦPSII). After pretreatment at 40°C, there was a striking difference in the responses of Fv/Fm, Fv′/Fm′ and ΦPSII to heat stress in non-salt-adapted and salt-adapted leaves. Leaves from salt-adapted plants maintained significantly higher values of Fv/Fm, Fv′/Fm′ and ΦPSII than those from non-salt-adapted leaves. The differences in Fv/Fm, Fv′/Fm′ and ΦPSII between non-salt-adapted and salt-adapted plants persisted for at least 12 h following heat stress. These results clearly show that thermotolerance of PSII was enhanced in salt-adapted plants. This enhanced thermotolerance was associated with an improvement in thermotolerance of the PSII reaction centers, the oxygen-evolving complexes and the light-harvesting complex. In addition, we observed that after exposure to 42.5°C for 30 min, non-salt-adapted plants showed a significant decrease in CO2 assimilation rate while in salt-adapted plants CO2 assimilation rate was either maintained or even increased to some extent. Given that photosynthesis is considered to be the physiological process most sensitive to high-temperature damage and that PSII appears to be the most heat-sensitive part of the photosynthetic apparatus, enhanced thermotolerance of PSII may be of significance for A. anethifolia, a halophyte plant, which grows in the high-salinity regions in the north of China, where the air temperature in the summer is often as high as 45°C.

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Abbreviations

ABS :

Absorption

CS :

Optical cross-section

ET :

Energy flux for electron transport

DI :

Dissipation

F o and F m :

Minimal and maximal fluorescence in the dark-adapted state

F o ′ and F m :

Minimal and maximal fluorescence in the light-adapted state

F s :

Steady-state chlorophyll fluorescence level in the light-adapted state

F v /F m (φ Po ):

Maximal efficiency of PSII photochemistry

F v ′/F m ′:

Efficiency of excitation capture by open PSII centers

Φ PSII :

Actual PSII efficiency

ψ o :

Efficiency with which a trapped exciton can move an electron into the electron transport chain further than QA

φ Eo :

Quantum yield of electron transport beyond QA

RC :

Reaction center

TR :

Energy flux for trapping

References

  • Appenroth KJ, Stockel J, Srivastava A, Strasser RJ (2001) Multiple effects of chromate on the photosynthetic apparatus Spirodela polyrhiza as probed by OJIP chlorophyll a fluorescence measurements. Environ Pollut 115:49–64

    Article  CAS  PubMed  Google Scholar 

  • Armond PA, Björkman O, Staehelin LA (1980) Dissociation of supramolecular complexes in chloroplast membranes. A manifestation of heat damage to the photosynthetic apparatus. Biochim Biophys Acta 601:433–442

    Article  CAS  PubMed  Google Scholar 

  • Baker NR (1991) Possible role of photosystem II in environmental perturbations of photosynthesis. Physiol Plant 81:563–570

    Google Scholar 

  • Belkhodja R, Morales F, Abadía A, Gomez-Aparisi J, Abadía J (1994) Chlorophyll fluorescence as a possible tool for salinity tolerance screening in barley (Hordeum vulgare L.). Plant Physiol 104:667–673

    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 

  • Bilger W, Schreiber U, Lange OL (1987) Chlorophyll fluorescence as an indicator of heat induced limitation of photosynthesis in Arbutus unedo. In: Tenhunen JD, Catarino FM, Lange OL (eds) Plant responses to stress. Springer, Berlin Heidelberg New York, pp 391–399

  • Butler, WL, Kitajima M (1975) Fluorescence quenching in photosystem II of chloroplast. Biochim Biophys Acta 376:116–125

    Article  CAS  PubMed  Google Scholar 

  • Demmig-Adams B, Adams III WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626

    Article  CAS  Google Scholar 

  • Everard JD, Gucci R, Kann SC, Flore JA, Loescher WH (1994) Gas exchange and carbon partitioning in the leaves of celery (Apium graveolens L.) at various levels of root zone salinity. Plant Physiol 106:281–292

    Google Scholar 

  • Feller U, Crafts-Brandner SJ, Salvucci E (1998) Moderately high temperatures inhibit ribulose-1,5-bisphosphate carboxylase/oxygenase activase-mediated activation of Rubisco. Plant Physiol 116:539–546

    Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 99:87–92

    Google Scholar 

  • Havaux M (1993a) Characterization of thermal damage to the photosynthetic electron transport system in potato leaves. Plant Sci 94:19–33

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Krüger GHJ, Tsimilli-Michael M, Strasser RJ (1997) Light stress provokes plastic and elastic modifications in structure and function of photosystem II in camellia leaves. Physiol Plant 101:265–277

    Google Scholar 

  • Lichtenthaler HK, Rindele U (1988) The role of chlorophyll fluorescence in the detection of stress conditions in plants. Crit Rev Anal Chem 19:29–85

    Google Scholar 

  • Long SP, Baker NR (1986) Saline terrestrial environments. In: Baker BR, Long SP (eds) Photosynthesis in contrasting environments. Elsevier, Amsterdam, pp 63–102

  • Lu C-M, Zhang J (2000) Heat-induced multiple effects on PSII in wheat plants. J Plant Physiol 156:259–265

    Google Scholar 

  • Lu C-M, Jiang G, Wang B, Kuang T (2003) Photosystem II photochemistry and photosynthetic pigment composition in salt-adapted halophyte Artemisia anethifolia grown under outdoor conditions. J Plant Physiol 160:403–408

    Google Scholar 

  • Masojidek J, Hall DO (1992) Salinity and drought stresses are amplified by high irradiance in sorghum. Photosynthetica 27:159–171

    CAS  Google Scholar 

  • Salvucci ME, Crafts-Brandner SJ (2004) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant 120:179–186

    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  CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Schreiber U, Bilger W, Neubauer C (1988) Application of the PAM fluorometer in stress detection. In: Lichtenthaler HK (ed) Application of chlorophyll fluorescence. Kluwer, Dordrecht, pp 151–156

  • Schreiber U, Bilger W, Neubauer C (1994) Chlorophyll fluorescence as a non-invasive indicator for rapid assessment of in vivo photosynthesis. In: Schulze E-D, Caldwell MM (eds) Ecophysiology of photosynthesis. Springer, Berlin Heidelberg New York, pp 49–70

  • Srivastava A, Guissé B, Greppin H, Strasser RJ (1997) Regulation of antenna structure and electron transport in photosystem II of Pisum sativum under elevated temperature probed by the fast polyphasic chlorophyll a fluorescence transient: OKJIP. Biochim Biophys Acta 1320:95–106

    Article  CAS  Google Scholar 

  • Srivastava A, Juttner F, Strasser RJ (1998) Action of the allelochemical, fischerellin A, on photosystem II. Biochim Biophys Acta 1364:326–336

    Article  CAS  PubMed  Google Scholar 

  • Srivastava A, Govindjee, Strasser RJ (1999) Greening of peas: parallel measurements on 77 K emission spectra, OJIP chlorophyll a fluorescence transient, period four oscillation of the initial fluorescence level, delayed light emission, and P700. Photosynthetica 37:365–392

    Article  CAS  Google Scholar 

  • Strasser BJ (1997) Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. Photosynth Res 52:147–55

    Article  CAS  Google Scholar 

  • Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP test. In: Mathis P (ed) Photosynthesis: from light to biosphere, vol V. Kluwer, Dordrecht, pp 977–980

  • Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transients in plants and cyanobacteria. Photochem Photobiol 61:32–42

    CAS  Google Scholar 

  • Strasser RJ, Srivatava A, Tsimilli-Michael M (1999) Screening the vitality and photosynthetic activity of plants by fluorescence transient. In: Behl RK, Punia MS, Lather BPS (eds) Crop improvement for food security. AAARM, Hisar, India, pp 72–115

  • Strasser RJ, Srivatava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanism, regulation and adaptation. Taylor & Francis, Bristol, pp 445–483

  • van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150

    Google Scholar 

  • Weis E (1981a) Reversible heat-inactivation of the Calvin cycle: a possible mechanism of the temperature regulation of photosynthesis. Planta 151:33–39

    CAS  Google Scholar 

  • Weis E (1981b) The temperature sensitivity of dark-inactivation and light-activation of the ribulose-1,5-bisphosphate carboxylase in spinach chloroplasts. FEBS Lett 129:197–200

    Article  CAS  Google Scholar 

  • Zhao K-F (1998) The halophytes in China. Science Publisher of China, Beijing

  • Zhao K-F, Li F-Z (1999) The halophytes in China. Science Publisher of China, Beijing

Download references

Acknowledgments

The authors thank the referees for their constructive comments in revising the manuscript and Dr. R Rodriguez for providing the Biolyzer software for the analysis of the JIP test. This study was supported by the Frontier Project of the Knowledge Innovation Engineering of the Chinese Academy of Sciences (KSCXZ-SW-326) and support from the Program of 100 Distinguished Young Scientists of Chinese Academy of Sciences to Congming Lu.

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Wen, X., Qiu, N., Lu, Q. et al. Enhanced thermotolerance of photosystem II in salt-adapted plants of the halophyte Artemisia anethifolia. Planta 220, 486–497 (2005). https://doi.org/10.1007/s00425-004-1382-7

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