Jasmonate‐ and abscisic acid‐activated AaGSW1‐AaTCP15/AaORA transcriptional cascade promotes artemisinin biosynthesis in Artemisia annua

Ya‐Nan Ma; Dong‐Bei Xu; Xin Yan; Zhang‐Kuanyu Wu; Sadaf Ilyas Kayani; Qian Shen; Xue‐Qing Fu; Li‐Hui Xie; Xiao‐Long Hao; Danial Hassani; Ling Li; Hang Liu; Qi‐Fang Pan; Zong‐You Lv; Pin Liu; Xiao‐Fen Sun; Ke‐Xuan Tang

doi:10.1111/pbi.13561

journal article Open Access Feb 14, 2021

Jasmonate‐ and abscisic acid‐activated AaGSW1‐AaTCP15/AaORA transcriptional cascade promotes artemisinin biosynthesis in Artemisia annua

Ya‐Nan Ma Dong‐Bei Xu

Xin Yan

Zhang‐Kuanyu Wu Sadaf Ilyas Kayani Qian Shen

Xue‐Qing Fu Li‐Hui Xie Xiao‐Long Hao Danial Hassani Ling Li

Hang Liu

Qi‐Fang Pan Zong‐You Lv Pin Liu Xiao‐Fen Sun Ke‐Xuan Tang

Plant Biotechnology Journal Vol. 19 No. 7 pp. 1412-1428 · Wiley

View at Publisher Save 10.1111/pbi.13561

Abstract

SummaryArtemisinin, a sesquiterpene lactone widely used in malaria treatment, was discovered in the medicinal plant Artemisia annua. The biosynthesis of artemisinin is efficiently regulated by jasmonate (JA) and abscisic acid (ABA) via regulatory factors. However, the mechanisms linking JA and ABA signalling with artemisinin biosynthesis through an associated regulatory network of downstream transcription factors (TFs) remain enigmatic. Here we report AaTCP15, a JA and ABA dual‐responsive teosinte branched1/cycloidea/proliferating (TCP) TF, which is essential for JA and ABA‐induced artemisinin biosynthesis by directly binding to and activating the promoters of DBR2 and ALDH1, two genes encoding enzymes for artemisinin biosynthesis. Furthermore, AaORA, another positive regulator of artemisinin biosynthesis responds to JA and ABA, interacts with and enhances the transactivation activity of AaTCP15 and simultaneously activates AaTCP15 transcripts. Hence, they form an AaORA‐AaTCP15 module to synergistically activate DBR2, a crucial gene for artemisinin biosynthesis. More importantly, AaTCP15 expression is activated by the multiple reported JA and ABA‐responsive TFs that promote artemisinin biosynthesis. Among them, AaGSW1 acts at the nexus of JA and ABA signalling to activate the artemisinin biosynthetic pathway and directly binds to and activates the AaTCP15 promoter apart from the AaORA promoter, which further facilitates formation of the AaGSW1‐AaTCP15/AaORA regulatory module to integrate JA and ABA‐mediated artemisinin biosynthesis. Our results establish a multilayer regulatory network of the AaGSW1‐AaTCP15/AaORA module to regulate artemisinin biosynthesis through JA and ABA signalling, and provide an interesting avenue for future research exploring the special transcriptional regulation module of TCP genes associated with specialized metabolites in plants.

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Published: Feb 14, 2021
Vol/Issue: 19(7)
Pages: 1412-1428
License: View

Authors

Y

Ya‐Nan Ma

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

D

Dong‐Bei Xu

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China; Institute of Ecological Agriculture Sichuan Agricultural University Chengdu China

X

Xin Yan

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

Z

Zhang‐Kuanyu Wu

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

S

Sadaf Ilyas Kayani

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

Q

Qian Shen

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

X

Xue‐Qing Fu

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

L

Li‐Hui Xie

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

X

Xiao‐Long Hao

Laboratory of Medicinal Plant Biotechnology College of Pharmacy Zhejiang Chinese Medical University Hangzhou China

D

Danial Hassani

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

L

Ling Li

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

H

Hang Liu

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

Q

Qi‐Fang Pan

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

Z

Zong‐You Lv

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

P

Pin Liu

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

X

Xiao‐Fen Sun

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

K

Ke‐Xuan Tang

Joint International Research Laboratory of Metabolic and Developmental Sciences Key Laboratory of Urban Agriculture (South) Ministry of Agriculture Plant Biotechnology Research Center Fudan‐SJTU‐Nottingham Plant Biotechnology R&D Center School of Agriculture and Biology Shanghai Jiao Tong University Shanghai China

Cite This Article

Ya‐Nan Ma, Dong‐Bei Xu, Xin Yan, et al. (2021). Jasmonate‐ and abscisic acid‐activated AaGSW1‐AaTCP15/AaORA transcriptional cascade promotes artemisinin biosynthesis in Artemisia annua. Plant Biotechnology Journal, 19(7), 1412-1428. https://doi.org/10.1111/pbi.13561

Jasmonate‐ and abscisic acid‐activated AaGSW1‐AaTCP15/AaORA transcriptional cascade promotes artemisinin biosynthesis in Artemisia annua

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