Unveiling the regulatory mechanisms of nodules development and quality formation in Panax notoginseng using multi-omics and MALDI-MSI

Muyao Yu; Chunxia Ma; Badalahu Tai; Xueqing Fu; Qi Liu; Guanhua Zhang; Xiuteng Zhou; Liyuan Du; Yan Jin; Yang Han; Han Zheng; Luqi Huang

doi:10.1016/j.jare.2024.04.003

Unveiling the regulatory mechanisms of nodules development and quality formation in Panax notoginseng using multi-omics and MALDI-MSI

J Adv Res. 2024 Apr 7:S2090-1232(24)00132-2. doi: 10.1016/j.jare.2024.04.003. Online ahead of print.

Authors

Muyao Yu¹, Chunxia Ma², Badalahu Tai³, Xueqing Fu⁴, Qi Liu⁵, Guanhua Zhang⁶, Xiuteng Zhou⁵, Liyuan Du⁷, Yan Jin⁵, Yang Han⁵, Han Zheng⁸, Luqi Huang⁹

Affiliations

¹ State Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China; School of Chinese Materia Medica, Beijing University of Chinese Medicine, Beijing 102488, China.
² Shandong Analysis and Test Center, Qilu University of Technology (Shandong Academy of Sciences), Jinan 250014, China.
³ State Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China; Mongolian Medical College, Inner Mongolia Minzu University, Tongliao 028000, China.
⁴ School of Design, Shanghai Jiao Tong University, Shanghai 200240, China.
⁵ State Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China.
⁶ State Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China; Shandong Analysis and Test Center, Qilu University of Technology (Shandong Academy of Sciences), Jinan 250014, China.
⁷ Create (Beijing) Technology Co., Limited, Beijing 102200, China.
⁸ State Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China. Electronic address: zhenghan@nrc.ac.cn.
⁹ State Key Laboratory for Quality Ensurance and Sustainable Use of Dao-di Herbs, National Resource Center for Chinese Materia Medica, China Academy of Chinese Medical Sciences, Beijing 100700, China. Electronic address: huanglq@cacms.cn.

PMID: 38588849
DOI: 10.1016/j.jare.2024.04.003

Abstract

Introduction: Renowned for its role in traditional Chinese medicine, Panax notoginseng exhibits healing properties including bidirectional regulatory effects on hematological system diseases. However, the presence of nodular structures near the top of the main root, known as nail heads, may impact the quality of the plant's valuable roots.

Objectives: In this paper, we aim to systematically analyze nail heads to identify their potential correlation with P. notoginseng quality. Additionally, we will investigate the molecular mechanisms behind nail head development.

Methods: Morphological characteristics and anatomical features were analyzed to determine the biological properties of nail heads. Active component analysis and MALDI mass spectrometry imaging (MALDI-MSI) were performed to determine the correlation between nail heads and P. notoginseng quality. Phytohormone quantitation, MALDI-MSI, RNA-seq, and Arabidopsis transformation were conducted to elucidate the mechanisms of nail head formation. Finally, protein-nucleic acid and protein-protein interactions were investigated to construct a transcriptional regulatory network of nodule development and quality formation.

Results: Our analyses have revealed that nail heads originate from an undeveloped lateral root. The content of ginsenosides was found to be positively associated with the amount of nail heads. Ginsenoside Rb₁ specifically accumulated in the cortex of nail heads, while IAA, tZR and JAs also showed highest accumulation in the nodule. RNA-seq analysis identified PnIAA14 and PnCYP735A1 as inhibitors of lateral root development. PnMYB31 and PnMYB78 were found to form binary complexes with PnbHLH31 to synergistically regulate the expression of PnIAA14, PnCYP735A1, PnSS, and PnFPS.

Conclusion: Our study details the major biological properties of nodular structures in P. notoginseng and outlines their impact on the quality of the herb. It was also determined that PnMYB31- and PnMYB78-PnbHLH31 regulate phytohormones and ginsenosides accumulation, further affecting plant development and quality. This research provides insights for quality evaluation and clinical applications of P. notoginseng.

Keywords: Ginsenoside; MALDI-MSI; Nodular structure; Panax notoginseng; Transcriptional regulation.