Haplotype-resolved genome of Agastache rugosa (Huo Xiang) provides insight into monoterpenoid biosynthesis and gene cluster evolution

Abstract

Monoterpenoids are small volatile molecules produced by many plants that have applications in consumer products and healthcare. Plants from the mint family (Lamiaceae) are prodigious producers of monoterpenoids, including a chemotype of Agastache rugosa (Huo Xiang), which produces pulegone and isomenthone. We sequenced, assembled and annotated a haplotype-resolved chromosome-scale genome assembly of A. rugosa with a monoterpene chemotype. This genome assembly revealed that pulegone biosynthesis genes are in a biosynthetic gene cluster, which shares a common origin with the pulegone gene cluster in Schizonepeta tenuifolia. Using phylogenetics and synteny analysis, we describe how the clusters in these two species diverged through inversions and duplications. Using Hi-C analysis, we identified tentative evidence of contact between the pulegone gene cluster and an array of pulegone reductases, with both regions also enriched in retrotransposons. This genome and its analysis add valuable and novel insights to the organization and evolution of terpenoid biosynthesis in Lamiaceae.

Acknowledgements

We acknowledge Hans-Wilhelm Nützmann and Daniel Doerr for advice on 3D genome analysis. We thank Xiao Han and Dajiang Tian from Nanjing University of Chinese Medicine with Python language and emotional support. This research was supported by the National Natural Science Foundation of China (grant nos. 82373978, 81973435), the National Natural Science Foundation for Young Scientists of China (grant no. 81903756), the Natural Science Foundation of Jiangsu Province (grant no. BK20231307), the Open Project of Chinese Materia Medica First-Class Discipline of Nanjing University of Chinese Medicine (grant no. ZYXYL2024-002) and High-Level University 2024 Key Cultivation Project -Research Leadership Program (grant no. RC202411). B.R.L. and S.J.S were funded by the BBSRC (BB/V006452/1). B.R.L acknowledges UKRI fellowship funding (MR/S01862X/1 and MR/X010260/1) and the Royal Society (IEC\NSFC\233491).

Author contributions

C.L. designed these experiments, was responsible for the genome analysis and wrote the paper. D.S.L. conducted the Hi-C data analysis. J.D. performed the enzyme assays. J.S. performed the cultivation and sampling of the specimens. S.J.S. aided in genome analysis. Q.W. supervised the project. B.R.L. analyzed data and wrote the paper.

Data availability

The genome sequence and raw sequencing reads are available at National Genomics Data Center (BioProject PRJCA027417). The raw reads are available in the Genome Sequence Archive (PacBio and Hi-C: CRA017422; RNA-seq: CRA017425). Gene sequences for A. rugosa ISPD and IPRs can be found in accession GB0004888.

Conflict of interest statement

The authors declare no conflict of interest.

Supplementary Data

Supplementary data are available at Horticulture Research online.

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