Dissection of full-length transcriptome and metabolome of Dichocarpum (Ranunculaceae): implications in evolution of specialized metabolism of Ranunculales medicinal plants

Abstract

Several main families of Ranunculales are rich in alkaloids and other medicinal compounds; many species of these families are used in traditional and folk medicine. Dichocarpum is a representative medicinal genus of Ranunculaceae, but the genetic basis of its metabolic phenotype has not been investigated, which hinders its sustainable conservation and utilization. We use the third-generation high-throughput sequencing and metabolomic techniques to decipher the full-length transcriptomes and metabolomes of five Dichocarpum species endemic in China, and 71,598 non-redundant full-length transcripts were obtained, many of which are involved in defense, stress response and immunity, especially those participating in the biosynthesis of specialized metabolites such as benzylisoquinoline alkaloids (BIAs). Twenty-seven orthologs extracted from trancriptome datasets were concatenated to reconstruct the phylogenetic tree, which was verified by the clustering analysis based on the metabolomic profile and agreed with the Pearson correlation between gene expression patterns of Dichocarpum species. The phylogenomic analysis of phytometabolite biosynthesis genes, e.g., (S)-norcoclaurine synthase, methyltransferases, cytochrome p450 monooxygenases, berberine bridge enzyme and (S)-tetrahydroprotoberberine oxidase, revealed the evolutionary trajectories leading to the chemodiversity, especially that of protoberberine type, aporphine type and bis-BIA abundant in Dichocarpum and related genera. The biosynthesis pathways of these BIAs are proposed based on full-length transcriptomes and metabolomes of Dichocarpum. Within Ranunculales, the gene duplications are common, and a unique whole genome duplication is possible in Dichocarpum. The extensive correlations between metabolite content and gene expression support the co-evolution of various genes essential for the production of different specialized metabolites. Our study provides insights into the transcriptomic and metabolomic landscapes of Dichocarpum, which will assist further studies on genomics and application of Ranunculales plants.

The genus Chrysanthemum: Phylogeny, biodiversity, phytometabolites, and chemodiversity

“…However, the relative quantification using the peak area as an index cannot reflect the exact content of compounds in chrysanthemum, therefore it is necessary to establish the quantitative analysis method for the differential components of different species/varieties of Chrysanthemum . The compounds detected by UPLC-Q-TOF-MS in plant metabolomics are more comprehensive ( Hao et al, 2021 ). To find the quality control indicators of chrysanthemum from numerous compounds, it is obligatory to combine content determination and pharmacokinetics/pharmacodynamics for comprehensive evaluation, which warrant deeper studies in the pharmacologically active constituents of chrysanthemum.…”

“…The current highly intensive industrial systems of agricultural and horticultural production are counter-sustainable, as the energy consumption is particularly intensive for cultivation, and the excessive use of nitrogen fertilizer leads to the worrying emission of greenhouse gas, N 2 O ( Hao et al, 2021 ; Wang et al, 2022 ). The genetic modification (GM) is transforming the prospects of sustainable crop protection, the specialized metabolite (e.g., pyrethrins) biosynthesis genes can be integrated to the target Chrysanthemum plants to enhance the stress response and disease resistance, so as to realize the full potential of GM and offer greener crop protection.…”

Distribution of Therapeutic Efficacy of Ranunculales Plants Used by Ethnic Minorities on the Phylogenetic Tree of Chinese Species

“…Thirty-four Ranunculaceae species are used ethnomedicinally against nervous system disease (Tables S1 and S2 ). We also noted the folk medicine use of Dichocarpum auriculatum (Ranunculaceae) in Sichuan Province against sow mania (epilepsy of sow) [ 23 ], which is not recorded in the Dictionary of Chinese Ethnic Medicine [ 3 ], as this book mainly reflects the traditional medicine knowledge of Chinese ethnic minorities. Accordingly, five BIAs of D. auriculatum had the in vitro inhibitory activity against acetylcholinesterase [ 22 ].…”

“…For example, berberine extracted from Coptis of Ranunculaceae had a synergistic anticancer effect by inducing apoptosis and inhibiting cell proliferation of esophageal cancer cells [ 21 ]. Five benzylisoquinoline alkaloids (columbamine, palmatine, dauricine, jatrorrhizine, and berberine; BIAs) from Dichocarpum of Ranunculaceae had the in vitro inhibitory activity against acetylcholinesterase [ 22 , 23 ]. Therefore, taking the order Ranunculales as a representative, we aim at studying the distribution pattern of Chinese ethnomedicinal plants on the phylogenetic tree by combining the species phylogenetic tree of Chinese angiosperms and therapeutic data of ethnomedicinal plants at the species level.…”

Mining Therapeutic Efficacy from Treasure Chest of Biodiversity and Chemodiversity: Pharmacophylogeny of Ranunculales Medicinal Plants

“…The 7 families of Ranunculales are rich in medicinal species frequently utilized by traditional medical systems and ethnomedicine, (187) which represent a treasure chest of biodiversity and chemodiversity. (188) The phylogenetically related species often have similar phytometabolites, and therefore similar bioactivities. This study gives a systematic review of the molecular phylogeny, chemical components and pharmacological activities of Ranunculales within the framework of pharmacophylogeny.…”