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Molecular understanding of anthocyanin biosynthesis activated by PAP1 and regulated by 2, 4-dichlorophenoxyacetic acid in engineered red Artemisia annua cells

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Abstract

Main conclusion

Eight promoters were cloned, from which AC and G-box cis-elements were identified. PAP1 enhanced the promoter activity. 2,4-D reduced the anthocyanin biosynthesis via downregulating the expression of the PAP1 transgene.

Abstract

Artemisia annua is an effective antimalarial medicinal crop. We have established anthocyanin-producing red cell cultures from this plant with the overexpression of Production of Anthocyanin Pigment 1 (PAP1) encoding a R2R3MYB transcription factor. To understand the molecular mechanism by which PAP1 activated the entire anthocyanin pathway, we mined the genomic sequences of A. annua and obtained eight promoters of the anthocyanin pathway genes. Sequence analysis identified four types of AC cis-elements from six promoters, the MYB response elements (MRE) bound by PAP1. In addition, six promoters were determined to have at least one G-box cis-element. Eight promoters were cloned for activity analysis. Dual luciferase assays showed that PAP1 significantly enhanced the promoting activity of seven promoters, indicating that PAP1 turned on the biosynthesis of anthocyanins via the activation of these pathway gene expression. To understand how 2,4-dichlorophenoxyacetic acid (2,4-D), an auxin, regulates the PAP1-activated anthocyanin biosynthesis, five different concentrations (0, 0.05, 0.5, 2.5, and 5 µM) were tested to characterize anthocyanin production and profiles. The resulting data showed that the concentrations tested decreased the fresh weight of callus growth, anthocyanin levels, and the production of anthocyanins per Petri dish. HPLC-qTOF-MS/MS-based profiling showed that these concentrations did not alter anthocyanin profiles. Real-time RT-PCR was completed to characterize the expression PAP1 and four representative pathway genes. The results showed that the five concentrations reduced the expression levels of the constitutive PAP1 transgene and three pathway genes significantly and eliminated the expression of the chalcone synthase gene either significantly or slightly. These data indicate that the constitutive PAP1 expression depends on gradients added in the medium. Based on these findings, the regulation of 2,4-D is discussed for anthocyanin engineering in red cells of A. annua.

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Abbreviations

2,4-D:

2,4-Dichlorophenoxyacetic acid

NAA:

1-Naphthaleneacetic acid

PAP1:

Production of anthocyanin pigment 1

4CL:

4-coumaroyl CoA ligase

ANS:

Anthocyanidin synthase

C4H:

Cinnamate 4-hydroxylase

CHI:

Chalcone isomerase

CHS:

Chalcone synthase

DFR:

Dihydroflavonol reductase

F3H:

Flavanone 3-hydroxylase

F3′H:

Flavonoid 3′-hydroxylase

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Acknowledgements

We thank China Scholar Council for supporting Yilun Dong’s PhD Exchange Scholarship and Yue Zhu PhD study.

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  1. Yilun Dong and Mingzhuo Li have contributed equally to this work.

Authors and Affiliations

  1. Department of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, USA

    Yilun Dong, Mingzhuo Li, Bryanna Cruz, Emily Ye, Yue Zhu & De-Yu Xie

  2. Rice Research Institute, Sichuan Agricultural University, Chengdu, China

    Yilun Dong, Lihua Li & Zhengjun Xu

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Dong, Y., Li, M., Cruz, B. et al. Molecular understanding of anthocyanin biosynthesis activated by PAP1 and regulated by 2, 4-dichlorophenoxyacetic acid in engineered red Artemisia annua cells. Planta 258, 75 (2023). https://doi.org/10.1007/s00425-023-04230-z

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