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

Feng Bai, Peng Shu, Heng Deng, Yi Wu, Yao Chen, Mengbo Wu, Tao Ma, Yang Zhang, Julien Pirrello, Zhengguo Li, Yiguo Hong, Mondher Bouzayen () and Mingchun Liu ()
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Feng Bai: Sichuan University
Peng Shu: Sichuan 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
Mondher Bouzayen: Sichuan University
Mingchun Liu: Sichuan University

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-47292-7

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