Genome-wide methylation, transcriptome and characteristic metabolites reveal the balance between diosgenin and brassinosteroids in Dioscorea zingiberensis

Abstract

Diosgenin (DG) is a bioactive metabolite isolated from Dioscorea species, renowned for its medicinal properties. Brassinosteroids (BRs) are a class of crucial plant steroidal hormones. Cholesterol and campesterol are important intermediates of DG and BR biosynthesis, respectively. DG and BRs are structurally similar components; however, the regulatory network and metabolic interplays have not been fully elucidated. In an effort to decode these complex networks, we conducted a comprehensive study integrating genome-wide methylation, transcriptome and characteristic metabolite data from Dioscorea zingiberensis. Leveraging these data, we were able to construct a comprehensive regulatory network linking DG and BRs. Mass spectrometry results enabled us to clarify the alterations in cholesterol, campesterol, diosgenin, and castasterone (one of the major active BRs). The DG content decreased by 27.72% at 6 h after brassinolide treatment, whereas the content increased by 85.34% at 6 h after brassinazole treatment. Moreover, we pinpointed DG/BR-related genes, such as CASs, CYP90s, and B3-ARFs, implicated in the metabolic pathways of DG and BRs. Moreover, CASs and CYP90s exhibit hypomethylation, which is closely related to their high transcription. These findings provide robust evidence for the homeostasis between DG and BRs. In conclusion, our research revealed the existence of a balance between DG and BRs in D. zingiberensis. Furthermore, our work not only provides new insights into the relationship between the two pathways but also offers a fresh perspective on the functions of secondary metabolites.

Acknowledgements

The authors thank Prof. Feng Ren (Hubei Key Laboratory of Genetic Regulation and Integrative Biology, School of Life Sciences, Central China Normal University) for his discussion on the subject and Novogene Corporation for sequencing and preliminary analysis of RNA-seq and WGBS data. This work was supported by grants from the National Natural Science Foundation of China (31270345 and 31470388, both to J.L.).

Author contributions

J.L. conceived and supervised the project. J.L. and Z.L. designed this study. Z.L. collected, analyzed, and interpreted the data. Z.L. performed the experiments. Z.L., Y.L., L.G., and J.W. assisted with some of the experiments and data analysis. Z.L. wrote the manuscript. Y.O. and J.L. reviewed and edited the manuscript. All authors read and approved the manuscript.

Data availability

The RNA-seq raw data described in this paper have been deposited in the National Genomics Data Center, Beijing Institute of Genomics (China National Center for Bioinformation), Chinese Academy of Sciences, under the Genome Sequence Archive (GSA) accession numbers CRA010777 and CRA010789 (https://bigd.big.ac.cn/gsa).

Conflict of interest

The authors declare no competing interests.

Supplementary data

Supplementary data are available at Horticulture Research online.

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