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Understanding the mechanism of red light-induced melatonin biosynthesis facilitates the engineering of melatonin-enriched tomatoes

Author

Listed:
  • Zixin Zhang

    (Sichuan University)

  • Xin Zhang

    (Sichuan University)

  • Yuting Chen

    (Sichuan University)

  • Wenqian Jiang

    (Sichuan University)

  • Jing Zhang

    (Sichuan University)

  • Jiayu Wang

    (Sichuan University)

  • Yanjun Wu

    (Sichuan University)

  • Shouchuang Wang

    (Sanya Nanfan Research Institute of Hainan University, Hainan Yazhou Bay Seed Laboratory)

  • Xiao Yang

    (Chengdu National Agricultural Science & Technology Center)

  • Mingchun Liu

    (Sichuan University)

  • Yang Zhang

    (Sichuan University)

Abstract

Melatonin is a functionally conserved broad-spectrum physiological regulator found in most biological organisms in nature. Enrichment of tomato fruit with melatonin not only enhances its agronomic traits but also provides extra health benefits. In this study, we elucidate the full melatonin biosynthesis pathway in tomato fruit by identifying biosynthesis-related genes that encode caffeic acid O-methyltransferase 2 (SlCOMT2) and N-acetyl-5-hydroxytryptamine-methyltransferases 5/7 (SlASMT5/7). We further reveal that red light supplementation significantly enhances the melatonin content in tomato fruit. This induction relies on the “serotonin—N-acetylserotonin—melatonin” biosynthesis route via the SlphyB2-SlPIF4-SlCOMT2 module. Based on the regulatory mechanism, we design a gene-editing strategy to target the binding motif of SlPIF4 in the promoter of SlCOMT2, which significantly enhances the production of melatonin in tomato fruit. Our study provides a good example of how the understanding of plant metabolic pathways responding to environmental factors can guide the engineering of health-promoting foods.

Suggested Citation

  • Zixin Zhang & Xin Zhang & Yuting Chen & Wenqian Jiang & Jing Zhang & Jiayu Wang & Yanjun Wu & Shouchuang Wang & Xiao Yang & Mingchun Liu & Yang Zhang, 2023. "Understanding the mechanism of red light-induced melatonin biosynthesis facilitates the engineering of melatonin-enriched tomatoes," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41307-5
    DOI: 10.1038/s41467-023-41307-5
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    References listed on IDEAS

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    1. Min Ni & James M. Tepperman & Peter H. Quail, 1999. "Binding of phytochrome B to its nuclear signalling partner PIF3 is reversibly induced by light," Nature, Nature, vol. 400(6746), pages 781-784, August.
    2. Yoshihito Shinozaki & Philippe Nicolas & Noe Fernandez-Pozo & Qiyue Ma & Daniel J. Evanich & Yanna Shi & Yimin Xu & Yi Zheng & Stephen I. Snyder & Laetitia B. B. Martin & Eliel Ruiz-May & Theodore W. , 2018. "High-resolution spatiotemporal transcriptome mapping of tomato fruit development and ripening," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    3. Sara Kim & Geonhee Hwang & Soohwan Kim & Thom Nguyen Thi & Hanim Kim & Jinkil Jeong & Jaewook Kim & Jungmook Kim & Giltsu Choi & Eunkyoo Oh, 2020. "The epidermis coordinates thermoresponsive growth through the phyB-PIF4-auxin pathway," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    4. Rao Fu & Pingyu Zhang & Ge Jin & Lianglei Wang & Shiqian Qi & Yang Cao & Cathie Martin & Yang Zhang, 2021. "Versatility in acyltransferase activity completes chicoric acid biosynthesis in purple coneflower," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
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    Cited by:

    1. Mingyue Guo & Fengjun Yang & Lijuan Zhu & Leilei Wang & Zhichao Li & Zhenyu Qi & Vasileios Fotopoulos & Jingquan Yu & Jie Zhou, 2024. "Loss of cold tolerance is conferred by absence of the WRKY34 promoter fragment during tomato evolution," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

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