Evolution of terpene synthases in the sesquiterpene biosynthesis pathway and analysis of their transcriptional regulatory network in Asteraceae

Abstract

The Asteraceae family, one of the largest angiosperm families, is rich in terpenoid secondary metabolites with significant medicinal value. Asteraceae plants have evolved a diverse array of terpenoid biosynthesis pathways, reflecting their adaptive significance and complex regulatory mechanisms. However, the evolutionary patterns and transcriptional regulatory mechanisms governing these biosynthetic processes remain unclear. This study investigates the evolution and transcriptional regulation of terpenoid biosynthesis genes in Asteraceae. Comparative genomic analysis of 19 Asteraceae and six out-group species revealed that Asteraceae species diverged ~74.03 million years ago and were distinctly divided into three subfamilies. A total of 1714 terpene synthase (TPS) genes were identified, predominantly in the TPS-a and TPS-b subfamilies. Caryophyllene-type sesquiterpene biosynthetic gene clusters (BGCs) were detected in 10 species, with their formation due to whole-genome duplication (WGD) and tandem duplication. By integrating weighted gene coexpression network analysis (WGCNA) and machine learning methods, key transcription factors regulating caryophyllene synthase (CPS) in Carthamus tinctorius were identified. A multilayered gene regulatory network was constructed to identify potential regulatory factors involved in TPS gene regulation under light stress. By exploring the evolutionary patterns and potential regulatory relationships involved in terpenoid biosynthesis in Asteraceae, this study provides important insights into TPS gene evolution. In addition, the findings also offer guidance for optimizing genetic engineering strategies in terpenoid-based drug development.

Acknowledgments

This work was supported by Innovation Team and Talents Cultivation Program of National Administration of Traditional Chinese Medicine (No: ZYYCXTD-D-202209) and State Key Laboratory of Southwestern Chinese Medicine Resources (SKLTCM202311).

Author contributions

W.C. and X.S. conceived the project and were responsible for the project initiation. W.C. and X.S. supervised and managed the project and research. Experiments and analyses were designed by X.Y, F.M., and Q.C. Data generation and bioinformatic analyses were performed by X.Y, F.M., and Q.C. The manuscript was organized, written, and revised by X.Y, F.M., Q.C., P.F., W.C., and X.S. All authors read and revised the manuscript.

Data availability

The genome sequence and RNA-seq data analyzed in this study are publicly available, and the corresponding links are provided in Table S26.

Conflict of interest statement

The authors declare there is no conflict of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

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