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A distal enhancer guides the negative selection of toxic glycoalkaloids during tomato domestication

Author

Listed:
  • Feng Bai

    (Sichuan University)

  • Peng Shu

    (Sichuan University
    Army Medical University)

  • Heng Deng

    (Sichuan University)

  • Yi Wu

    (Sichuan University)

  • Yao Chen

    (Sichuan University)

  • Mengbo Wu

    (Sichuan University)

  • Tao Ma

    (Sichuan University)

  • Yang Zhang

    (Sichuan University)

  • Julien Pirrello

    (Toulouse-INP)

  • Zhengguo Li

    (Chongqing University)

  • Yiguo Hong

    (University of Warwick
    Hebei Agricultural University)

  • Mondher Bouzayen

    (Sichuan University
    Toulouse-INP)

  • Mingchun Liu

    (Sichuan University)

Abstract

Steroidal glycoalkaloids (SGAs) are major plant defense metabolites against pests, while they are considered poisonous in food. The genetic basis that guides negative selection of SGAs production during tomato domestication remains poorly understood. Here, we identify a distal enhancer, GAME Enhancer 1 (GE1), as the key regulator of SGAs metabolism in tomato. GE1 recruits MYC2-GAME9 transcriptional complex to regulate the expression of GAME cluster genes via the formation of chromatin loops located in the neighboring DNA region. A naturally occurring GE176 allelic variant is found to be more active in stimulating GAME expression. We show that the weaker GE1 allele has been the main driver for selecting reduced SGAs levels during tomato domestication. Unravelling the “TFs-Enhancer-Promoter” regulatory mechanism operating in SGAs metabolism opens unprecedented prospects for SGAs manipulation in Solanaceae via precision breeding strategies.

Suggested Citation

  • Feng Bai & Peng Shu & Heng Deng & Yi Wu & Yao Chen & Mengbo Wu & Tao Ma & Yang Zhang & Julien Pirrello & Zhengguo Li & Yiguo Hong & Mondher Bouzayen & Mingchun Liu, 2024. "A distal enhancer guides the negative selection of toxic glycoalkaloids during tomato domestication," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47292-7
    DOI: 10.1038/s41467-024-47292-7
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