Comparative genomics of the medicinal plants Lonicera macranthoides and L. japonica provides insight into genus genome evolution and hederagenin-based saponin biosynthesis

Lonicera macranthoides (LM) and L. japonica (LJ) are medicinal plants widely used in treating viral diseases, such as COVID-19. Although the two species are morphologically similar, their secondary metabolite profiles are significantly different. Here, metabolomics analysis showed that LM contained...

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Bibliographic Details
Published in:Plant biotechnology journal 2023-11, Vol.21 (11), p.2209-2223
Main Authors: Yin, Xiaojian, Xiang, Yaping, Huang, Feng-Qing, Chen, Yahui, Ding, Hengwu, Du, Jinfa, Chen, Xiaojie, Wang, Xiaoxiao, Wei, Xinru, Cai, Yuan-Yuan, Gao, Wen, Guo, Dongshu, Alolga, Raphael N, Kan, Xianzhao, Zhang, Baolong, Alejo-Jacuinde, Gerardo, Li, Ping, Tran, Lam-Son Phan, Herrera-Estrella, Luis, Lu, Xu, Qi, Lian-Wen
Format: Article
Language:English
Subjects:
Amino acids
Biosynthesis
Chinese medicine
Chromatography
Chromosomes
Coronaviruses
COVID-19
Enzymatic activity
Enzymes
Evolution
Evolutionary genetics
Flavonoids
Flowers & plants
Genes
Genomes
Genomics
Glycosyltransferase
Herbal medicine
Influenza
Lonicera macranthoides
Medicinal plants
Metabolites
Metabolomics
Oleanolic acid
Oxidation
Plant species
Saponins
Speciation
Viral diseases
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Summary:Lonicera macranthoides (LM) and L. japonica (LJ) are medicinal plants widely used in treating viral diseases, such as COVID-19. Although the two species are morphologically similar, their secondary metabolite profiles are significantly different. Here, metabolomics analysis showed that LM contained ~86.01 mg/g hederagenin-based saponins, 2000-fold higher than LJ. To gain molecular insights into its secondary metabolite production, a chromosome-level genome of LM was constructed, comprising 9 pseudo-chromosomes with 40 097 protein-encoding genes. Genome evolution analysis showed that LM and LJ were diverged 1.30-2.27 million years ago (MYA). The two plant species experienced a common whole-genome duplication event that occurred ∼53.9-55.2 MYA before speciation. Genes involved in hederagenin-based saponin biosynthesis were arranged in clusters on the chromosomes of LM and they were more highly expressed in LM than in LJ. Among them, oleanolic acid synthase (OAS) and UDP-glycosyltransferase 73 (UGT73) families were much more highly expressed in LM than in LJ. Specifically, LmOAS1 was identified to effectively catalyse the C-28 oxidation of β-Amyrin to form oleanolic acid, the precursor of hederagenin-based saponin. LmUGT73P1 was identified to catalyse cauloside A to produce α-hederin. We further identified the key amino acid residues of LmOAS1 and LmUGT73P1 for their enzymatic activities. Additionally, comparing with collinear genes in LJ, LmOAS1 and LmUGT73P1 had an interesting phenomenon of 'neighbourhood replication' in LM genome. Collectively, the genomic resource and candidate genes reported here set the foundation to fully reveal the genome evolution of the Lonicera genus and hederagenin-based saponin biosynthetic pathway.
ISSN:1467-7644
1467-7652
DOI:10.1111/pbi.14123