Transcriptome revealing the dual regulatory mechanism of ethylene on the rhynchophylline and isorhynchophylline in Uncaria rhynchophylla

Li, Xue; Wang, Xiao-hong; Qiang, Wei; Zheng, Hao-jie; ShangGuan, Li-yang; Zhang, Ming-sheng

doi:10.1007/s10265-022-01387-8

Regular Paper – Physiology/Biochemistry/Molecular and Cellular Biology
Published: 05 April 2022

Transcriptome revealing the dual regulatory mechanism of ethylene on the rhynchophylline and isorhynchophylline in Uncaria rhynchophylla

Xue Li¹,
Xiao-hong Wang¹,
Wei Qiang¹,
Hao-jie Zheng¹,
Li-yang ShangGuan¹ &
Ming-sheng Zhang ORCID: orcid.org/0000-0002-7108-5326¹

Journal of Plant Research volume 135, pages 485–500 (2022)Cite this article

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Abstract

Rhynchophylline (RIN) and isorhynchophylline (IRN) are extracted from Uncaria rhynchophylla, which are used to treat Alzheimer's disease. However, the massive accumulation of RIN and IRN in U. rhynchophylla requires exogenous stimulation. Ethylene is a potential stimulant for RIN and IRN biosynthesis, but there is no study on the role of ethylene in RIN or IRN synthesis. This study investigated the regulation of ethylene in RIN and IRN biosynthesis in U. rhynchophylla. An increase in the content of RIN and IRN was observed that could be attributed to the release of ethylene from 18 mM ethephon, while ethylene released from 36 mM ethephon reduced the content of RIN and IRN. The transcriptome and weighted gene co-expression network analysis indicated the up-regulation of seven key enzyme genes related to the RIN/IRN biosynthesis pathway and starch/sucrose metabolism pathway favored RIN/IRN synthesis. In comparison, the down-regulation of these seven key enzyme genes contributed to the reduction of RIN/IRN. Moreover, the inhibition of photosynthesis is associated with a reduction in RIN/IRN. Photosynthesis was restrained owing to the down-regulation of Lhcb1 and Lhcb6 after 36 mM ethephon treatment and further prevented supply of primary metabolites (such as α-d-glucose) for RIN/IRN synthesis. However, uninterrupted photosynthesis ensured a normal supply of primary metabolites at 18 mM ethephon treatment. AP2/ERF1, bHLH1, and bHLH2 may positively regulate the RIN/IRN accumulation, while NAC1 may play a negative regulatory role. Our results construct the potential bidirectional model for ethylene regulation on RIN/IRN synthesis and provide novel insight into the ethylene-mediated regulation of the metabolism of terpenoid indole alkaloids.

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Data availability

The RNA-seq data set has been deposited in NCBI as BioProject under the number PRJNA699101. https://www.ncbi.nlm.nih.gov/search/all/?term=PRJNA699101.

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Acknowledgements

This work was supported by the Major Special Project of Science and Technology Program in Guizhou [2017-5411-06 and 2018-2797]; the Construction Project of State Engineering Technology Institute for Karst Desertification Control of China [2012FU125X13]; the National Key Research and Development Program of China [2016YFC0502604]; the Construction Project of Modern Industry Technology system of traditional Chinese Medicinal Materials in Guizhou [GZCYTX-02]; and the Project of High-level Innovative Talents in Guizhou [2015-4031].

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School of Life Sciences/Key Laboratory of Plant Resource Conservation and Germplasm Innovation in Mountainous Region (Ministry of Education), Guizhou University, Guiyang, 550025, Guizhou, China
Xue Li, Xiao-hong Wang, Wei Qiang, Hao-jie Zheng, Li-yang ShangGuan & Ming-sheng Zhang

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Xue Li
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Xiao-hong Wang
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Wei Qiang
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Hao-jie Zheng
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Li-yang ShangGuan
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Ming-sheng Zhang
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XL was responsible for study designing and manuscript writing. XL, HZ and LSG cultivated and prepared the plant materials. XL and XW analyzed the data. MZ, WQ and XW revised the manuscript. MZ, supervision, funding acquisition.

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Correspondence to Ming-sheng Zhang.

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Li, X., Wang, Xh., Qiang, W. et al. Transcriptome revealing the dual regulatory mechanism of ethylene on the rhynchophylline and isorhynchophylline in Uncaria rhynchophylla. J Plant Res 135, 485–500 (2022). https://doi.org/10.1007/s10265-022-01387-8

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Received: 02 December 2021
Accepted: 10 March 2022
Published: 05 April 2022
Issue Date: May 2022
DOI: https://doi.org/10.1007/s10265-022-01387-8

Keywords

Ethylene
Isorhynchophylline
Rhynchophylline
Transcriptional regulation
Uncaria rhynchophylla