Transcriptomic and metabolomic analyses reveal the mechanism of anthocyanin metabolism in H18 pepper leaves and the function of CaDFR1

doi:10.1016/j.jia.2025.10.011

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Transcriptomic and metabolomic analyses reveal the mechanism of anthocyanin metabolism in H18 pepper leaves and the function of CaDFR1

Han Wang^1,2,3^*, Dongchen Li⁴^*, Congsheng Yan^1,2,3, Muhammad Aamir Manzoor⁵, Qiangqiang Ding^1,2,3, Yan Wang^1,2,3, Xiujing Hong^1,2,3, Tingting Song^1,2,3, Li Jia^1,2,3^#, Haikun Jiang^1,2,3^#

¹Institute of Vegetables, Anhui Academy of Agricultural Sciences, Hefei 230001, China.

² Key Laboratory of Horticultural Crop Germplasm Innovation and Utilization (Co-construction by Ministry and Province), Hefei 230001, China.

³ Anhui Provincial Key Laboratory for Germplasm Resources Creation and High-Efficiency Cultivation of Horticultural Crops, Hefei 230001, China.

⁴ College of Life Sciences, Anhui Agricultural University, Hefei 230036, China.

⁵ School of Agriculture and Biology, Shanghai Jiao Tong University, Shanghai 200030, China.

Highlights

1. The accumulation of anthocyanins on H18 pepper plants leads to a purple color in their leaves, with anthocyanins on the leaves decreasing as they grow and develop.

2. Anthocyanins produced with DHM as substrate occupy the main component of anthocyanins in H18 pepper leaves.

3. CaDRF1 plays an important role in the anthocyanin synthesis pathway of pepper leaves.

Abstract
References

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摘要

花青苷在植物的生长、发育、繁殖和响应胁迫中发挥着至关重要的作用。此外，花青苷的抗氧化特性还能提高水果和蔬菜的品质。虽然前人对花青苷进行了较多的研究，但有关其成分以及花青苷代谢途径基因 DFR（二氢黄酮醇-4-还原酶）在辣椒叶片中的作用的信息还很有限。在这项研究中，我们使用了一种紫色叶片辣椒栽培品种 H18，其叶片上的花青苷随着生长发育而减少。靶向花青素代谢组学检测显示，飞燕草色素、锦葵色素和牵牛花色素的衍生物的含量与花青苷含量呈相同趋势，其中飞燕草色素衍生物是 H18 辣椒叶片的主要成分。对四个不同发育阶段的 H18 叶片进行了转录组测序。结果表明，不同阶段的差异基因主要与生物过程和类黄酮代谢途径有关。通过进化树和转录组表达量分析，确定了3个DFR候选功能基因。底物催化活性分析结果显示，仅CaDFR1表现出对二氢槲皮素(DHQ)、二氢杨梅素(DHM)和二氢山奈酚(DHK)三种底物的催化能力。VIGS 介导的 CaDFR1 沉默导致 H18 辣椒叶片和茎中花青苷含量显著降低，荧光定量显示花青苷代谢途径中其他候选功能基因的表达水平也有所下降。这项研究确定了 H18 辣椒叶片中的关键花青苷成分，并验证了 CaDFR1 的功能，为通过分子育种改变辣椒植株花青素含量提供了理论基础。

Abstract

Anthocyanins play a crucial role in plant growth, development, reproduction, and stress response. Additionally, anthocyanins enhance the quality of fruits and vegetables due to their antioxidant properties. While numerous previous research has been conducted on anthocyanins, limited information exists regarding their composition and the role of the anthocyanin pathway gene DFR (dihydroflavonol 4-reductase) in chili pepper leaves. In this study, we used a purple leaf pepper cultivar H18 with anthocyanins on the leaves decreasing as they grow and develop. Targeted anthocyanin metabolite assays revealed that the contents of delphinidin, malvidin, and petunidin derivatives followed the same trend as the overall anthocyanin content, with delphinidin derivatives being the predominant component of H18 pepper leaves. Transcriptome sequencing was performed on H18 leaves at four different stages. The results showed that DEGs at various stages were primarily associated with biological processes and flavonoid metabolic pathways. Through evolutionary tree and expression analysis, three candidate genes involved in DFR function were identified. Substrate catalysis assays of CaDFRs demonstrated that only CaDFR1 was active, catalyzing DHQ, DHM, and DHK. VIGS-mediated silencing of CaDFR1 resullted in a significant decrease reduction in anthocyanin levels in H18 pepper leaves and stems and along with a decreased reduction in the expression levels of other candidate functional genes in the anthocyanin metabolic pathway. This study identifies the key anthocyanin components in the leaves of H18 peppers and validates the function of CaDFR1, providing a theoretical foundation for modifying anthocyanin content in pepper plants through molecular breeding.

Keywords: anthocyanins transcriptomic and metabolomic dihydroflavonol 4-reductase functional validation

Online: 22 October 2025

Fund:

This work was supported by Postdoctoral Research Program Support of Anhui Province (2024C863), China Agriculture Research System of MOF and MARA (CARS-23-G40, CARS-23-G49), The Youth Development Fund from Anhui Academy of Agricultural Sciences (QNYC-202121).

About author: #Correspondence Haikun Jiang, Tel/Fax: +86-0551-65160817, E-mail: Jhk211@163.com; Li Jia, Tel/Fax: +86-0551-65160817, E-mail: jiali820@aaas.org.cn * These authors have contributed equally to this work.

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Han Wang, Dongchen Li, Congsheng Yan, Muhammad Aamir Manzoor, Qiangqiang Ding, Yan Wang, Xiujing Hong, Tingting Song, Li Jia, Haikun Jiang. 2025. Transcriptomic and metabolomic analyses reveal the mechanism of anthocyanin metabolism in H18 pepper leaves and the function of CaDFR1. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.10.011

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