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Glycinebetaine mitigates tomato chilling stress by maintaining high-cyclic electron flow rate of photosystem I and stability of photosystem II

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Glycinebetaine alleviates chilling stress by protecting photosystems I and II in BADH -transgenic and GB-treated tomato plants, which can be an effective strategy for improving crop chilling tolerance.

Abstract

Tomato (Solanum lycopersicum) is one of the most cultivated vegetables in the world, but is highly susceptible to chilling stress and does not naturally accumulate glycinebetaine (GB), one of the most effective stress protectants. The protective mechanisms of GB on photosystem I (PSI) and photosystem II (PSII) against chilling stress, however, remain poorly understood. Here, we address this problem through exogenous GB application and generation of transgenic tomatoes (Moneymaker) with a gene encoding betaine aldehyde dehydrogenase (BADH), which is the key enzyme in the synthesis of GB, from spinach. Our results demonstrated that GB can protect chloroplast ultramicrostructure, alleviate PSII photoinhibition and maintain PSII stability under chilling stress. More importantly, GB increased the electron transfer between QA and QB and the redox potential of QB and maintained a high rate of cyclic electron flow around PSI, contributing to reduced production of reactive oxygen species, thereby mitigating PSI photodamage under chilling stress. Our results highlight the novel roles of GB in enhancing chilling tolerance via the protection of PSI and PSII in BADH transgenic and GB-treated tomato plants under chilling stress. Thus, introducing GB-biosynthetic pathway into tomato and exogenous GB application are effective strategies for improving chilling tolerance.

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Funding

Funding for this research were provided by the National Natural Sciences Foundation of China (31870216, 31470341), Open project of State Key Laboratory of Crop Biology of Shandong Agriculture University (2017KF10) and Science and Technology Innovation Project of Colleges and Universities in Shanxi Province (2020L0542).

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  1. Dandan Wei and Tianpeng Zhang contributed equally to this work.

Authors and Affiliations

  1. College of Life Science, State Key Laboratory of Crop Biology, Shandong Key Laboratory of Crop Biology, Shandong Agricultural University, Taian, 271018, Shandong, China

    Dandan Wei, Tianpeng Zhang, Huiling Zhang, Mingyang Ma, Shufen Li, Yang Liu & Xinghong Yang

  2. Xinzhou Teachers University, Xinzhou, 034000, Shanxi, China

    Dandan Wei

  3. Maize Research Institution, Shanxi Academy of Agricultural Sciences, XinzhouShanxi, 034000, China

    Bingquan Wang

  4. Department of Horticulture, Oregon State University, ALS 4017, Corvallis, OR, 97331, USA

    Tony H. H. Chen

  5. Department of Plant Physiology, Slovak University of Agriculture, A. Hlinku 2, Nitra, 94976, Slovak Republic

    Marian Brestic

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  1. Dandan Wei
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  2. Tianpeng Zhang
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  4. Huiling Zhang
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  9. Yang Liu
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  10. Xinghong Yang
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Contributions

XY conceived and supervised the project, and XY, YL and DW designed the experiments. DW and TZ performed most of the experiments. BW, HZ, MM and SL performed some of the experiments. DW, TZ and XY analyzed data and wrote the manuscript. THHC, MB and YL gave positive suggestion about this article. All authors read and approved the manuscript.

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Correspondence to Yang Liu or Xinghong Yang.

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Communicated by Chun-Hai Dong.

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Wei, D., Zhang, T., Wang, B. et al. Glycinebetaine mitigates tomato chilling stress by maintaining high-cyclic electron flow rate of photosystem I and stability of photosystem II. Plant Cell Rep 41, 1087–1101 (2022). https://doi.org/10.1007/s00299-022-02839-0

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