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Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants

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Abstract

Genetically engineered tobacco (Nicotiana tabacum L.) with the ability to accumulate glycinebetaine was established. The wild type and transgenic plants were exposed to heat treatment (25–50°C) for 4 h in the dark and under growth light intensity (300 μmol m−2 s−1). The analyses of oxygen-evolving activity and chlorophyll fluorescence demonstrated that photosystem II (PSII) in transgenic plants showed higher thermotolerance than in wild type plants in particular when heat stress was performed in the light, suggesting that the accumulation of glycinebetaine leads to increased tolerance to heat-enhanced photoinhibition. This increased tolerance was associated with an improvement on thermostability of the oxygen-evolving complex and the reaction center of PSII. The enhanced tolerance was caused by acceleration of the repair of PSII from heat-enhanced photoinhibition. Under heat stress, there was a significant accumulation of H2O2, O −2 and catalytic Fe in wild type plants but this accumulation was much less in transgenic plants. Heat stress significantly decreased the activities of catalase, ascorbate peroxidase, glutathione reductase, dehydroascorbate reductase, and monodehydroascorbate reductase in wild type plants whereas the activities of these enzymes either decreased much less or maintained or even increased in transgenic plants. In addition, heat stress increased the activity of superoxide dismutase in wild type plants but this increase was much greater in transgenic plants. Furthermore, transgenic plants also showed higher content of ascorbate and reduced glutathione than that of wild type plants under heat stress. The results suggest that the increased thermotolerance induced by accumulation of glycinebetaine in vivo was associated with the enhancement of the repair of PSII from heat-enhanced photo inhibition, which might be due to less accumulation of reactive oxygen species in transgenic plants.

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Abbreviations

APX:

Ascorbate peroxidase

CAT:

Catalase

DHAR:

Dehydroascorbate reductase

F o, F m :

Minimal and maximal fluorescence in dark-adapted state

F o′, F m′:

Minimal and maximal fluorescence in light-adapted state

F s :

Steady-state chlorophyll fluorescence level in light-adapted state

F v/F m :

Maximal efficiency of PSII photochemistry

F v′/F m′:

Efficiency of excitation capture by open PSII centers

ΦPSII :

Actual PSII efficiency

GB:

Glycinebetaine

GR:

Glutathione reductase

MDHAR:

Monodehydroascorbate reductase

OEC:

Oxygen-evolving complex of photosystem II

PSII:

Photosystem II

q P :

Photochemical quenching coefficient

RC:

Reaction center of photosystem II

SOD:

Superoxide dismutase

ROS:

Reactive oxygen species

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Acknowledgments

This work was supported by the Frontier Project of the Knowledge Innovation Engineering of the Chinese Academy of Sciences (grant no. KSCXZ-SW-326) and by the Program of 100 Distinguished Young Scientists of Chinese Academy of Sciences to Congming Lu as well as by Innovation Foundation of Shandong Agricultural University for Young Scientists.

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Authors and Affiliations

  1. Photosynthesis Research Center, Key Laboratory of Photosynthesis and Environmental Molecular Physiology, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, People’s Republic of China

    Xinghong Yang, Xiaogang Wen, Hongmei Gong, Qingtao Lu, Zhipan Yang, Yunlai Tang, Zheng Liang & Congming Lu

  2. College of Life Science, Key Laboratory of Crop Biology of Shandong, Shandong Agricultural University, Taian, 217017, People’s Republic of China

    Xinghong Yang

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  1. Xinghong Yang
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  2. Xiaogang Wen
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Correspondence to Congming Lu.

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Yang, X., Wen, X., Gong, H. et al. Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. Planta 225, 719–733 (2007). https://doi.org/10.1007/s00425-006-0380-3

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