Revealing evolution of tropane alkaloid biosynthesis by analyzing two genomes in the Solanaceae family

Fangyuan Zhang, Fei Qiu, Junlan Zeng, Zhichao Xu, Yueli Tang, Tengfei Zhao, Yuqin Gou, Fei Su, Shiyi Wang, Xiuli Sun, Zheyong Xue, Weixing Wang, Chunxian Yang, Lingjiang Zeng, Xiaozhong Lan, Min Chen, Junhui Zhou and Zhihua Liao ()
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Fangyuan Zhang: Southwest University
Fei Qiu: Southwest University
Junlan Zeng: Southwest University
Zhichao Xu: Northeast Forestry University
Yueli Tang: Southwest University
Tengfei Zhao: Southwest University
Yuqin Gou: Southwest University
Fei Su: Southwest University
Shiyi Wang: Southwest University
Xiuli Sun: Southwest University
Zheyong Xue: Northeast Forestry University
Weixing Wang: Southwest University
Chunxian Yang: Southwest University
Lingjiang Zeng: Southwest University
Xiaozhong Lan: Xizang Agricultural and Animal Husbandry College
Min Chen: Southwest University
Junhui Zhou: China Academy of Chinese Medical Sciences
Zhihua Liao: Southwest University

Nature Communications, 2023, vol. 14, issue 1, 1-18

Abstract: Abstract Tropane alkaloids (TAs) are widely distributed in the Solanaceae, while some important medicinal tropane alkaloids (mTAs), such as hyoscyamine and scopolamine, are restricted to certain species/tribes in this family. Little is known about the genomic basis and evolution of TAs biosynthesis and specialization in the Solanaceae. Here, we present chromosome-level genomes of two representative mTAs-producing species: Atropa belladonna and Datura stramonium. Our results reveal that the two species employ a conserved biosynthetic pathway to produce mTAs despite being distantly related within the nightshade family. A conserved gene cluster combined with gene duplication underlies the wide distribution of TAs in this family. We also provide evidence that branching genes leading to mTAs likely have evolved in early ancestral Solanaceae species but have been lost in most of the lineages, with A. belladonna and D. stramonium being exceptions. Furthermore, we identify a cytochrome P450 that modifies hyoscyamine into norhyoscyamine. Our results provide a genomic basis for evolutionary insights into the biosynthesis of TAs in the Solanaceae and will be useful for biotechnological production of mTAs via synthetic biology approaches.

Date: 2023
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DOI: 10.1038/s41467-023-37133-4

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