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N6-methyladenosine RNA modification regulates photosynthesis during photodamage in plants

Author

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  • Man Zhang

    (Guangzhou University of Chinese Medicine
    Sun Yat-sen University
    Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research)

  • Yunping Zeng

    (Guangzhou University of Chinese Medicine)

  • Rong Peng

    (Guangzhou University of Chinese Medicine)

  • Jie Dong

    (Sun Yat-sen University)

  • Yelin Lan

    (Sun Yat-sen University)

  • Sujuan Duan

    (Guangzhou University of Chinese Medicine)

  • Zhenyi Chang

    (Guangzhou University of Chinese Medicine)

  • Jian Ren

    (Sun Yat-sen University)

  • Guanzheng Luo

    (Sun Yat-sen University)

  • Bing Liu

    (Sun Yat-sen University)

  • Kamil Růžička

    (Czech Academy of Sciences)

  • Kewei Zhao

    (The Third Affiliated Hospital of Guangzhou University of Chinese Medicine)

  • Hong-Bin Wang

    (Guangzhou University of Chinese Medicine
    Key Laboratory of Chinese Medicinal Resource from Lingnan (Guangzhou University of Chinese Medicine), Ministry of Education
    Guangzhou University of Chinese Medicine)

  • Hong-Lei Jin

    (Guangzhou University of Chinese Medicine
    The Third Affiliated Hospital of Guangzhou University of Chinese Medicine)

Abstract

N6-methyladenosine (m6A) modification of mRNAs affects many biological processes. However, the function of m6A in plant photosynthesis remains unknown. Here, we demonstrate that m6A modification is crucial for photosynthesis during photodamage caused by high light stress in plants. The m6A modification levels of numerous photosynthesis-related transcripts are changed after high light stress. We determine that the Arabidopsis m6A writer VIRILIZER (VIR) positively regulates photosynthesis, as its genetic inactivation drastically lowers photosynthetic activity and photosystem protein abundance under high light conditions. The m6A levels of numerous photosynthesis-related transcripts decrease in vir mutants, extensively reducing their transcript and translation levels, as revealed by multi-omics analyses. We demonstrate that VIR associates with the transcripts of genes encoding proteins with functions related to photoprotection (such as HHL1, MPH1, and STN8) and their regulatory proteins (such as regulators of transcript stability and translation), promoting their m6A modification and maintaining their stability and translation efficiency. This study thus reveals an important mechanism for m6A-dependent maintenance of photosynthetic efficiency in plants under high light stress conditions.

Suggested Citation

  • Man Zhang & Yunping Zeng & Rong Peng & Jie Dong & Yelin Lan & Sujuan Duan & Zhenyi Chang & Jian Ren & Guanzheng Luo & Bing Liu & Kamil Růžička & Kewei Zhao & Hong-Bin Wang & Hong-Lei Jin, 2022. "N6-methyladenosine RNA modification regulates photosynthesis during photodamage in plants," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35146-z
    DOI: 10.1038/s41467-022-35146-z
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    References listed on IDEAS

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    1. Vera Bonardi & Paolo Pesaresi & Thomas Becker & Enrico Schleiff & Raik Wagner & Thomas Pfannschmidt & Peter Jahns & Dario Leister, 2005. "Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases," Nature, Nature, vol. 437(7062), pages 1179-1182, October.
    2. Guan-Zheng Luo & Alice MacQueen & Guanqun Zheng & Hongchao Duan & Louis C. Dore & Zhike Lu & Jun Liu & Kai Chen & Guifang Jia & Joy Bergelson & Chuan He, 2014. "Unique features of the m6A methylome in Arabidopsis thaliana," Nature Communications, Nature, vol. 5(1), pages 1-8, December.
    3. Harry Smith, 2000. "Phytochromes and light signal perception by plants—an emerging synthesis," Nature, Nature, vol. 407(6804), pages 585-591, October.
    4. Xiao Wang & Zhike Lu & Adrian Gomez & Gary C. Hon & Yanan Yue & Dali Han & Ye Fu & Marc Parisien & Qing Dai & Guifang Jia & Bing Ren & Tao Pan & Chuan He, 2014. "N6-methyladenosine-dependent regulation of messenger RNA stability," Nature, Nature, vol. 505(7481), pages 117-120, January.
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