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, Zhihua Liao
Author Information
  1. Fangyuan Zhang: State Key Laboratory of Silkworm Genome Biology, School of Life Sciences, Southwest University, Chongqing, 400715, China.
  2. Fei Qiu: State Key Laboratory of Silkworm Genome Biology, School of Life Sciences, Southwest University, Chongqing, 400715, China.
  3. Junlan Zeng: State Key Laboratory of Silkworm Genome Biology, School of Life Sciences, Southwest University, Chongqing, 400715, China.
  4. Zhichao Xu: Heilongjiang Key Laboratory of Plant Bioactive Substance Biosynthesis and Utilization, Northeast Forestry University, Harbin, Heilongjiang, 150040, China. ORCID
  5. Yueli Tang: State Key Laboratory of Silkworm Genome Biology, School of Life Sciences, Southwest University, Chongqing, 400715, China.
  6. Tengfei Zhao: State Key Laboratory of Silkworm Genome Biology, School of Life Sciences, Southwest University, Chongqing, 400715, China.
  7. Yuqin Gou: State Key Laboratory of Silkworm Genome Biology, School of Life Sciences, Southwest University, Chongqing, 400715, China.
  8. Fei Su: State Key Laboratory of Silkworm Genome Biology, School of Life Sciences, Southwest University, Chongqing, 400715, China.
  9. Shiyi Wang: State Key Laboratory of Silkworm Genome Biology, School of Life Sciences, Southwest University, Chongqing, 400715, China.
  10. Xiuli Sun: State Key Laboratory of Silkworm Genome Biology, School of Life Sciences, Southwest University, Chongqing, 400715, China.
  11. Zheyong Xue: Heilongjiang Key Laboratory of Plant Bioactive Substance Biosynthesis and Utilization, Northeast Forestry University, Harbin, Heilongjiang, 150040, China.
  12. Weixing Wang: College of Horticulture and Landscape Architecture, Southwest University, Chongqing, 400715, China.
  13. Chunxian Yang: State Key Laboratory of Silkworm Genome Biology, School of Life Sciences, Southwest University, Chongqing, 400715, China.
  14. Lingjiang Zeng: State Key Laboratory of Silkworm Genome Biology, School of Life Sciences, Southwest University, Chongqing, 400715, China.
  15. Xiaozhong Lan: TAAHC-SWU Medicinal Plant Joint R&D Centre, Tibetan Collaborative Innovation Centre of Agricultural and Animal Husbandry Resources, Xizang Agricultural and Animal Husbandry College, Nyingchi, Tibet, 860000, China.
  16. Min Chen: College of Pharmaceutical Sciences, Key Laboratory of Luminescent and Real-Time Analytical Chemistry (Ministry of Education), Southwest University, Chongqing, 400715, China.
  17. Junhui Zhou: State Key Laboratory of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing, 100700, China.
  18. Zhihua Liao: State Key Laboratory of Silkworm Genome Biology, School of Life Sciences, Southwest University, Chongqing, 400715, China. zhliao@swu.edu.cn. ORCID

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.

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MeSH Term

Solanaceae
Hyoscyamine
Alkaloids
Tropanes
Scopolamine
Atropa belladonna

Chemicals

Hyoscyamine
Alkaloids
Tropanes
Scopolamine

Word Cloud

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