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Single-cell RNA sequencing facilitates the elucidation of the complete biosynthesis of the antidepressant hyperforin in St. John's wort

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MOLECULAR PLANT 2024年第9期17卷 1439-1457页

作者： Wu, Song morotti, ana luisa malaco Yang, Jun Wang, Ertao Tatsis, Evangelos C. Chinese Acad Sci Shanghai Inst Plant Physiol & Ecol CAS Ctr Excellence Mol Plant Sci Natl Key Lab Plant Mol Genet Shanghai 200032 Peoples R China Univ Chinese Acad Sci Shanghai 200032 Peoples R China CEPAMS CAS JIC Ctr Excellence Plant & Microbial Sc Shanghai 200032 Peoples R China

Hyperforin is the compound responsible for the effectiveness of St. John's wort (Hypericum perforatum) as an antidepressant, but its complete biosynthetic pathway remains unknown. Gene discovery based on co- expression analysis of bulk RNA-sequencing data or genome mining failed to discover the missing steps in hyperforin biosynthesis. In this study, we sequenced the 1.54-Gb tetraploid H. perforatum genome assembled into 32 chromosomes with the scaffold N50 value of 42.44 Mb. By single-cell RNA sequencing, we identified a type of cell, "Hyper cells", wherein hyperforin biosynthesis de novo takes place in both the leaves and flowers. Through pathway reconstitution in yeast and tobacco, we identified and characterized four transmembrane prenyltransferases (HpPT1-4) that are localized at the plastid envelope and complete the hyperforin biosynthetic pathway. The hyperforin polycyclic scaffold is created by a reaction cascade involving an irregular isoprenoid coupling and a tandem cyclization. Our findings reveal how and where hyperforin is biosynthesized, enabling synthetic-biology reconstitution of the complete pathway. Thus, this study not only deepens our comprehension of specialized metabolism at the cellular level but also provides strategic guidance for elucidation of the biosynthetic pathways of other specializied metabolites in plants.

关键词： hyperforin Hypericum perforatum de novo genome sequencing single-cell RNA sequencing biosyn- thetic pathway meroterpenoids HYPERICUM-PERFORATUM AROMATIC PRENYLTRANSFERASES TRANSLUCENT GLANDS ALIGNMENT CONSTITUENTS DEPRESSION PREDICTION DIVERSITY BIOLOGY FINDER

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The genomes of medicinal skullcaps reveal the polyphyletic origins of clerodane diterpene biosynthesis in the family Lamiaceae

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Molecular Plant 2023年第3期16卷 549-570页

作者： Haixiu Li Song Wu Ruoxi Lin Yiren Xiao ana luisa malaco morotti Ya Wang Meytal Galilee Haowen Qin Tao Huang Yong Zhao Xun Zhou Jun Yang Qing Zhao Angelos K.Kanellis Cathie Martin Evangelos C.Tatsis National Key Laboratory of Plant Molecular Genetics CAS Center for Excellence in Molecular Plant SciencesShanghai Institute of Plant Physiology and EcologyChinese Academy of SciencesShanghai 200032China University of Chinese Academy of Sciences Beijing 100049China Novogene Bioinformatics Institute BeijingChina Shanghai Key Laboratory of Plant Functional Genomics and Resources Shanghai Chenshan Botanical GardenShanghai Chenshan Plant Science Research CenterChinese Academy of SciencesShanghai 201602 Group of Biotechnology of Pharmaceutical Plants Lab.of PharmacognosyDepartment of Pharmaceutical SciencesAristotle University of Thessaloniki54124 ThessalonikiGreece John Innes Centre Norwich NR47UHUK CEPAMS-CAS-JIC Centre of Excellence for Plant and Microbial Sciences Shanghai 200032China

The presence of anticancer clerodane diterpenoids is a chemotaxonomic marker for the traditional Chinese medicinal plant Scutellaria barbata,although the molecular mechanisms behind clerodane biosynthesis are ***,we report a high-quality assembly of the 414.98 Mb genome of *** into 13 *** phylogenomic and biochemical data,we mapped the plastidial metabolism of kaurene(gibberellins),abietane,and clerodane diterpenes in three species of the family Lamiaceae(Scutellaria barbata,Scutellaria baicalensis,and Salvia splendens),facilitating the identification of genes involved in the biosynthesis of the clerodanes,kolavenol,and *** show that clerodane biosynthesis evolved through recruitment and neofunctionalization of genes from gibberellin and abietane *** the assumed monophyletic origin of clerodane biosynthesis,which is widespread in species of the Lamiaceae,our data show distinct evolutionary lineages and suggest polyphyletic origins of clerodane biosynthesis in the family *** study not only provides significant insights into the evolution of clerodane biosynthetic pathways in the mint family,Lamiaceae,but also will facilitate the production of anticancer clerodanes through future metabolic engineering efforts.

关键词： Scutellaria barbata genome clerodane diterpenoids biosynthesis specialized metabolism evolution

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