Multi-omics reveal key enzymes involved in the formation of phenylpropanoid glucosides in Artemisia annua

Qinggang Yin, Tianze Wu, Ranran Gao, Lan Wu, Yuhua Shi, Xingwen Wang, Mengyue Wang, Zhichao Xu, Yueliang Zhao, Xiaojia Su, Yanyan Su, Xiaoyan Han, Ling Yuan, Li Xiang, Shilin Chen

Research output: Contribution to journalArticlepeer-review

Abstract

Although mainly known for producing artemisinin, Artemisia annua is enriched in phenylpropanoid glucosides (PGs) with significant bioactivities. However, the biosynthesis of A. annua PGs is insufficiently investigated. Different A. annua ecotypes from distinct growing environments accumulate varying amounts of metabolites, including artemisinin and PGs such as scopolin. UDP-glucose:phenylpropanoid glucosyltransferases (UGTs) transfers glucose from UDP-glucose in PG biosynthesis. Here, we found that the low-artemisinin ecotype GS produces a higher amount of scopolin, compared to the high-artemisinin ecotype HN. By combining transcriptome and proteome analyses, we selected 28 candidate AaUGTs from 177 annotated AaUGTs. Using AlphaFold structural prediction and molecular docking, we determined the binding affinities of 16 AaUGTs. Seven of the AaUGTs enzymatically glycosylated phenylpropanoids. AaUGT25 converted scopoletin to scopolin and esculetin to esculin. The lack of accumulation of esculin in the leaf and the high catalytic efficiency of AaUGT25 on esculetin suggest that esculetin is methylated to scopoletin, the precursor of scopolin. We also discovered that AaOMT1, a previously uncharacterized O-methyltransferase, converts esculetin to scopoletin, suggesting an alternative route for producing scopoletin, which contributes to the high-level accumulation of scopolin in A. annua leaves. AaUGT1 and AaUGT25 responded to induction of stress-related phytohormones, implying the involvement of PGs in stress responses.

Original languageEnglish
Article number107795
JournalPlant Physiology and Biochemistry
Volume201
DOIs
StatePublished - Aug 2023

Bibliographical note

Funding Information:
This work was supported by the CACMS Innovation Fund ( CI2021A05108 , CI2021A04117 , CI2021A05103 ), and Fundamental Research Funds for the Central public welfare research institutes ( ZZ13-YQ-097 , ZZ13-YQ-102 , ZZ16-ND-10-14 ), and National key research and development program ( 2019YFC1711100 ), the State Scholarship Fund by China Scholarship Council ( 202009110054 ).

Publisher Copyright:
© 2023 Elsevier Masson SAS

Keywords

  • AlphaFold
  • Artemisia annua
  • Glycosyltransferase
  • Methyltransferase
  • Phenylpropanoid
  • Scopolin

ASJC Scopus subject areas

  • Physiology
  • Genetics
  • Plant Science

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