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RNA G-quadruplex structure contributes to cold adaptation in plants

Author

Listed:
  • Xiaofei Yang

    (Northeast Normal University
    Chinese Academy of Sciences
    Chinese Academy of Sciences
    John Innes Centre, Norwich Research Park)

  • Haopeng Yu

    (Northeast Normal University
    John Innes Centre, Norwich Research Park)

  • Susan Duncan

    (John Innes Centre, Norwich Research Park)

  • Yueying Zhang

    (John Innes Centre, Norwich Research Park)

  • Jitender Cheema

    (John Innes Centre, Norwich Research Park)

  • Haifeng Liu

    (John Innes Centre, Norwich Research Park
    Shandong Agricultural University)

  • J. Benjamin Miller

    (University of East Anglia, Norwich Research Park)

  • Jie Zhang

    (John Innes Centre, Norwich Research Park)

  • Chun Kit Kwok

    (City University of Hong Kong, Kowloon Tong
    Shenzhen Research Institute of City University of Hong Kong)

  • Huakun Zhang

    (Northeast Normal University)

  • Yiliang Ding

    (John Innes Centre, Norwich Research Park)

Abstract

Nucleotide composition is suggested to infer gene functionality and ecological adaptation of species to distinct environments. However, the underlying biological function of nucleotide composition dictating environmental adaptations is largely unknown. Here, we systematically analyze the nucleotide composition of transcriptomes across 1000 plants (1KP) and their corresponding habitats. Intriguingly, we find that plants growing in cold climates have guanine (G)-enriched transcriptomes, which are prone to forming RNA G-quadruplex structures. Both immunofluorescence detection and in vivo structure profiling reveal that RNA G-quadruplex formation in plants is globally enhanced in response to cold. Cold-responsive RNA G-quadruplexes strongly enhanced mRNA stability, rather than affecting translation. Disruption of individual RNA G-quadruplex promotes mRNA decay in the cold, leading to impaired plant cold response. Therefore, we propose that plants adopted RNA G-quadruplex structure as a molecular signature to facilitate their adaptation to the cold during evolution.

Suggested Citation

  • Xiaofei Yang & Haopeng Yu & Susan Duncan & Yueying Zhang & Jitender Cheema & Haifeng Liu & J. Benjamin Miller & Jie Zhang & Chun Kit Kwok & Huakun Zhang & Yiliang Ding, 2022. "RNA G-quadruplex structure contributes to cold adaptation in plants," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34040-y
    DOI: 10.1038/s41467-022-34040-y
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    References listed on IDEAS

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    1. Judah Cohen & Karl Pfeiffer & Jennifer A. Francis, 2018. "Warm Arctic episodes linked with increased frequency of extreme winter weather in the United States," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    2. Hani Goodarzi & Hamed S. Najafabadi & Panos Oikonomou & Todd M. Greco & Lisa Fish & Reza Salavati & Ileana M. Cristea & Saeed Tavazoie, 2012. "Systematic discovery of structural elements governing stability of mammalian messenger RNAs," Nature, Nature, vol. 485(7397), pages 264-268, May.
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    1. Prakash Kharel & Marta Fay & Ekaterina V. Manasova & Paul J. Anderson & Alexander V. Kurkin & Junjie U. Guo & Pavel Ivanov, 2023. "Stress promotes RNA G-quadruplex folding in human cells," Nature Communications, Nature, vol. 14(1), pages 1-10, December.

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