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.
Similar content being viewed by others
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
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
Baker NR (1991) Possible role of photosystem II in environmental perturbations of photosynthesis. Physiol Plant 81:563–570
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
Berry JA, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543
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
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
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
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
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
Havaux M (1993a) Characterization of thermal damage to the photosynthetic electron transport system in potato leaves. Plant Sci 94:19–33
Havaux M (1993b) Rapid photosynthetic adaptation to heat stress triggered in potato leaves by moderately elevated temperatures. Plant Cell Environ 16:461–467
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
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
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
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
Masojidek J, Hall DO (1992) Salinity and drought stresses are amplified by high irradiance in sorghum. Photosynthetica 27:159–171
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
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
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
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
Srivastava A, Juttner F, Strasser RJ (1998) Action of the allelochemical, fischerellin A, on photosystem II. Biochim Biophys Acta 1364:326–336
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
Strasser BJ (1997) Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. Photosynth Res 52:147–55
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
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
Weis E (1981a) Reversible heat-inactivation of the Calvin cycle: a possible mechanism of the temperature regulation of photosynthesis. Planta 151:33–39
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-004-1382-7