Transcriptomic and metabolomic analyses provide new insights into the appropriate harvest period in regenerated bulbs of Fritillaria hupehensis

Yuanyuan Duan; Jiaqi Wu; Fanfan Wang; Kaiqi Zhang; Xiaoliang Guo; Tao Tang; Sen Mu; Jingmao You; Jie Guo

doi:10.3389/fpls.2023.1132936

Transcriptomic and metabolomic analyses provide new insights into the appropriate harvest period in regenerated bulbs of Fritillaria hupehensis

Front Plant Sci. 2023 Feb 15:14:1132936. doi: 10.3389/fpls.2023.1132936. eCollection 2023.

Authors

Yuanyuan Duan^{1

2

3}, Jiaqi Wu¹, Fanfan Wang^{1

3}, Kaiqi Zhang¹, Xiaoliang Guo¹, Tao Tang^{1

3}, Sen Mu¹, Jingmao You^{1

3}, Jie Guo^{1

2}

Affiliations

¹ Key Laboratory of Biology and Cultivation of Chinese Herbal Medicines, Ministry of Agriculture and Rural Affairs, Institute of Chinese Herbal Medicines, Hubei Academy of Agricultural Sciences, Enshi, China.
² Hubei Engineering Research Center of Under-forest Economy, Hubei Academy of Agricultural Sciences, Wuhan, China.
³ Hubei Engineering Research Center of Good Agricultural Practices (GAP) Production for Chinese Herbal Medicines, Institute of Chinese Herbal Medicines, Hubei Academy of Agricultural Sciences, Enshi, China.

Abstract

Introduction: The bulb of Fritillaria hupehensis, a traditional cough and expectorant medicine, is usually harvested from June to September according to traditional cultivation experience, without practical scientific guidance. Although steroidal alkaloid metabolites have been identified in F. hupehensis, the dynamic changes in their levels during bulb development and their molecular regulatory mechanisms are poorly understood.

Methods: In this study, integrative analyses of the bulbus phenotype, bioactive chemical investigations, and metabolome and transcriptome profiles were performed to systematically explore the variations in steroidal alkaloid metabolite levels and identify the genes modulating their accumulation and the corresponding regulatory mechanisms.

Results: The results showed that weight, size, and total alkaloid content of the regenerated bulbs reached a maximum at IM03 (post-withering stage, early July), whereas peiminine content reached a maximum at IM02 (withering stage, early June). There were no significant differences between IM02 and IM03, indicating that regenerated bulbs could be harvested appropriately in early June or July. Peiminine, peimine, tortifoline, hupehenine, korseveramine, delafrine, hericenone N-oxide, korseveridine, puqiedinone, pingbeinone, puqienine B, puqienine E, pingbeimine A, jervine, and ussuriedine levels were upregulated in IM02 and IM03, compared with IM01 (vigorous growth stage, early April). The Kyoto Encyclopedia of Genes and Genomes enrichment analysis indicated that the accumulation of steroidal alkaloid metabolites mainly occurred prior to IM02. HMGR1, DXR, CAS1, CYP 90A1, and DET2 may play a positive role in peiminine, peimine, hupehenine, korseveramine, korseveridine, hericenone N-oxide, puqiedinone, delafrine, tortifoline, pingbeinone, puqienine B, puqienine E, pingbeimine A, jervine, and ussuriedine biosynthesis, whereas the downregulation of FPS1, SQE and 17-DHCR may lead to a reduction in peimisine levels. Weighted gene correlation network analysis showed that CYP 74A2-1, CYP 74A2-2, CYP 71A26-1, CYP 71A26-2, and CYP74A were negatively correlated with peiminine and pingbeimine A, whereas CYP R and CYP707A1 were positively correlated. . CYP 74A2-1 and CYP 74A2-2 may play a negative role in peimine and korseveridine biosynthesis, whereas CYP R plays a positive role. In addition, the highly expressed C2H2, HSF, AP2/ERF, HB, GRAS, C3H, NAC, MYB-related transcription factors (TFs), GARP-G2-like TFs, and WRKY may play positive roles in the accumulation of peiminine, peimine, korseveridine, and pingbeimine A.

Discussion: These results provide new insights into scientific harvesting of F. hupehensis.

Keywords: Fritillaria hupehensis; WGCNA; bulb development; metabolic; steroidal alkaloids.

Grants and funding

This work was supported by the Key Research and Development Plan Project of Hubei (2022BBA153), the Hubei Technology Innovation Center for Agricultural Sciences - Key Research and Development Project of Science and Technology (2020-620-000-002-04), the Forestry Science and Technology Project of Central Finance (2021TG16), the Hubei Central Government Guided Local Science and Technology Development Project (2022BGE256), and the China Agriculture Research System (CARS-21).