The genome of Corydalis reveals the evolution of benzylisoquinoline alkaloid biosynthesis in Ranunculales

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dc.contributor.author Xu, Zhichao
dc.contributor.author Li, Zhen
dc.contributor.author Ren, Fengming
dc.contributor.author Gao, Ranran
dc.contributor.author Wang, Zhengfan
dc.contributor.author Zhang, Jinlan
dc.contributor.author Zhao, Tao
dc.contributor.author Ma, Xiao
dc.contributor.author Pu, Xiangdong
dc.contributor.author Xin, Tianyi
dc.contributor.author Rombauts, Stephane
dc.contributor.author Sun, Wei
dc.contributor.author Van de Peer, Yves
dc.contributor.author Chen, Shilin
dc.contributor.author Song, Jingyuan
dc.date.accessioned 2023-07-17T08:52:19Z
dc.date.available 2023-07-17T08:52:19Z
dc.date.issued 2022-07
dc.description DATA AVAILABILITY STATEMENT : The assembled genome and gene structures have been deposited in the Genome Warehouse in the National Genomics Data Center under accession number GWHAORS00000000 with the BioProject ID (PRJCA003323) and the BioSample ID (SAMC231736), which is publicly accessible at https://bigd.big.ac.cn/gwh. en_US
dc.description SUPPORTING FIGURES : FIGURE S1. The morphology and genome survey of Corydalis tomentella. FIGURE S2. Hi-C intrachromosomal contact map for genome assembly (2n = 16). FIGURE S3. Dot plot of paralogous blocks in Corydalis tomentella shows the potential whole-genome duplication event. FIGURE S4. Synteny analysis between Corydalis tomentella and other eudicot genomes. FIGURE S5. Ks distributions of whole paralogs (gray bars) and anchor-pair paralogs (black bars) for Vitis vinifera and six sister lineages to core eudicots (Aquilegia coerulea, Corydalis tomentella, Eschscholzia californica, Macleaya cordata, Nelumbo nucifera and Papaver somniferum). FIGURE S6. The kernel density estimation (KDE) of the orthologous Ks distributions between Vitis vinifera and six sister lineages to core eudicots. FIGURE S7. HPLC analysis of BIAs in different tissues of Corydalis tomentella, including root, stem, leaf and flower. FIGURE S8. 1H NMR and 13C NMR spectra of dehydroapocavidine and dehydroisoapocavidine in methanol-D4 using a Bruker 600-MHz NMR spectrometer. FIGURE S9. Identification of chemical structures of dehydroapocavidine and dehydroisoapocavidine based on the 1H NMR and 13C NMR spectra. FIGURE S10. The proportion of labeled and unlabeled BIA compounds in the study of isotopic tracer. FIGURE S11. High-resolution mass spectrometry (HRMS) analysis of the BIA compounds detected in Corydalis tomentella. FIGURE S12. Gene cluster and gene expression analysis related to BIA biosynthesis in Corydalis tomentella. FIGURE S13. Evolutional analysis of NCS gene clusters among Aquilegia coerulea (AqcoeXGXXXXXX), Corydalis tomentella (contigXXXXXX), Macleaya cordata (BVC80_XXXXXXX), Nelumbo nucifera (NNU_XXXXX) and Papaver somniferum (PSXXXXXXX) genomes. FIGURE S14. Evolutional analysis of 6OMT and NMCH genes among Aquilegia coerulea (AqcoeXGXXXXXX), Corydalis tomentella (contigXXXXXX), Macleaya cordata (BVC80_XXXXXXX), Nelumbo nucifera (NNU_XXXXX) and Papaver somniferum (PSXXXXXXX) genomes. FIGURE S15. Evolutional analysis of NMT genes among Aquilegia coerulea (AqcoeXGXXXXXX), Corydalis tomentella (contigXXXXXX), Macleaya cordata (BVC80_XXXXXXX), Nelumbo nucifera (NNU_XXXXX) and Papaver somniferum (PSXXXXXXX) genomes. FIGURE S16. The classification of OMT genes identified from Aquilegia coerulea (AqcoeXGXXXXXX), Corydalis tomentella (contigXXXXXX), Macleaya cordata (BVC80_XXXXXXX), Nelumbo nucifera (NNU_XXXXX) and Papaver somniferum (PSXXXXXXX) genomes. FIGURE S17. Evolutional analysis of CYP719 genes among the Papaveraceae species, Corydalis tomentella (contigXXXXXX), Macleaya cordata (BVC80_XXXXXXX) and Papaver somniferum (PSXXXXXXX). FIGURE S18. The collinearity analysis of conserved gene cluster related to the upstream biosynthesis of BIAs between Corydalis tomentella and Macleaya cordata. FIGURE S19. The classification of CYP82N, CYP82X and CYP82Y subfamily members identified from Aquilegia coerulea (AqcoeXGXXXXXX), Corydalis tomentella (contigXXXXXX), Macleaya cordata (BVC80_XXXXXXX), Nelumbo nucifera (NNU_XXXXX) and Papaver somniferum (PSXXXXXXX) genomes. FIGURE S20. The in vivo catalytic assays of CtBBEL8 and CtBBEL31 in Sf9 insect cells using tetrahydrocolumbamin and tetrahydropalmatine as substrates, respectively. FIGURE S21. The in vivo catalytic assays of BwSTOX, CtBBEL8, CtBBEL22 and CtBBEL31 in Sf9 insect cells using cavidine, chilanthifoline and stylopine as substrates, respectively. FIGURE S22. The LC-MS analysis of the catalytic reactions of CtBBEL8, CtBBEL22 and CtBBEL31 using tetrahydrocolumbamin, tetrahydropalmatine, cheilanthifoline, cavidine and stylopine as substrates, respectively. en_US
dc.description SUPPORTING TABLES : TABLE S1. Sequencing data from Illumina short-read platform for DNA libraries. TABLE S2. Sequencing data from Illumina short-read platform for cDNA libraries. TABLE S3. Sequel sequencing data. TABLE S4. Corydalis tomentella genome assembly and annotation. TABLE S5. Statistics of eight pseudochromosome assembly of Corydalis tomentella genome. TABLE S6. Annotation of Corydalis tomentella transposable elements (TEs). TABLE S7. Identification of simple sequence repeats in the Corydalis tomentella genome. TABLE S8. The numbers of BIA biosynthetic genes in studied species from Ranunculales and Proteales. TABLE S9. Gene expression (FPKM values) analysis of BIA biosynthetic genes in Corydalis tomentella. en_US
dc.description.abstract Species belonging to the order Ranunculales have attracted much attention because of their phylogenetic position as a sister group to all other eudicot lineages and their ability to produce unique yet diverse benzylisoquinoline alkaloids (BIAs). The Papaveraceae family in Ranunculales is often used as a model system for studying BIA biosynthesis. Here, we report the chromosome-level genome assembly of Corydalis tomentella, a species of Fumarioideae, one of the two subfamilies of Papaveraceae. Based on comparisons of sequenced Ranunculalean species, we present clear evidence of a shared whole-genome duplication (WGD) event that has occurred before the divergence of Ranunculales but after its divergence from other eudicot lineages. The C. tomentella genome enabled us to integrate isotopic labeling and comparative genomics to reconstruct the BIA biosynthetic pathway for both sanguinarine biosynthesis shared by papaveraceous species and the cavidine biosynthesis that is specific to Corydalis. Also, our comparative analysis revealed that gene duplications, especially tandem gene duplications, underlie the diversification of BIA biosynthetic pathways in Ranunculales. In particular, tandemly duplicated berberine bridge enzyme-like genes appear to be involved in cavidine biosynthesis. In conclusion, our study of the C. tomentella genome provides important insights into the occurrence of WGDs during the early evolution of eudicots, as well as into the evolution of BIA biosynthesis in Ranunculales. en_US
dc.description.department Biochemistry en_US
dc.description.department Genetics en_US
dc.description.department Microbiology and Plant Pathology en_US
dc.description.librarian hj2023 en_US
dc.description.sponsorship CAMS Innovation Fund for Medical Sciences (CIFMS); European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program; National Key R&D Program of China; National Science and Technology Major Project for “Significant New Drugs Development”; postdoctoral fellowship from the Special Research Fund of Ghent University. en_US
dc.description.uri https://onlinelibrary.wiley.com/journal/1365313x en_US
dc.identifier.citation Xu, Z,, Li, Z,, Ren, F. et al. 2022, 'The genome of Corydalis reveals the evolution of benzylisoquinoline alkaloid biosynthesis in Ranunculales', Plant Journal, vol. 111, no. 1, pp. 217-230, doi : 10.1111/tpj.15788. en_US
dc.identifier.issn 0960-7412 (print)
dc.identifier.issn 1365-313X (online)
dc.identifier.other 10.1111/tpj.15788
dc.identifier.uri http://hdl.handle.net/2263/91475
dc.language.iso en en_US
dc.publisher Wiley en_US
dc.rights © 2022 Society for Experimental Biology and John Wiley & Sons Ltd. This is the pre-peer reviewed version of the following article : 'The genome of Corydalis reveals the evolution of benzylisoquinoline alkaloid biosynthesis in Ranunculales', Plant Journal, vol. 111, no. 1, pp. 217-230, 2022, doi : 10.1111/tpj.15788. The definite version is available at : https://onlinelibrary.wiley.com/journal/1365313x. en_US
dc.subject Benzylisoquinoline alkaloids en_US
dc.subject Papaveraceae en_US
dc.subject Corydalis tomentella en_US
dc.subject Whole-genome duplication en_US
dc.subject Evolution en_US
dc.title The genome of Corydalis reveals the evolution of benzylisoquinoline alkaloid biosynthesis in Ranunculales en_US
dc.type Postprint Article en_US


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