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

Zixin Zhang, Xin Zhang, Yuting Chen, Wenqian Jiang, Jing Zhang, Jiayu Wang, Yanjun Wu, Shouchuang Wang, Xiao Yang, Mingchun Liu and Yang Zhang ()
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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

Nature Communications, 2023, vol. 14, issue 1, 1-12

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-41307-5

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