Telomere-to-telomere genome assembly and multiomics analyses illustrate the high accumulation of quercetin glucosides in tetraploid Descurainia sophia

Abstract

Quercetin glucosides are important phytopharmaceutical metabolites in Descurainia sophia seeds, which are widely used in traditional herbal medicine. However, the key genes involved in quercetin glucoside biosynthesis in D. sophia have not been characterized. Herein, we present the telomere-to-telomere genomes of a tetraploid D. sophia, which accumulates high levels of quercetin glucoside, and a diploid D. sophia, which accumulates only trace amounts. Multiomics analyses and uridine diphosphate glucosyltransferase (UGT) enzyme assays revealed that the gene duplication and functional evolution of Dscd6AG01520, an UGT gene, led to high quercetin-3- O - β - D -glucoside and quercetin-3,7- O - β - D -diglucoside accumulation in tetraploid D. sophia seeds. Further UGT enzyme assays with the point mutations of Dscd6AG01520 showed that S213 was a critical amino acid for the enzymatic activity of Dscd6AG01520. In addition, we found that diploid D. sophia evolved from an ancestral crucifer karyotype through chromosome fusion and rearrangement. Collectively, our findings illuminate the mechanism of high quercetin glucoside accumulation in tetraploid D. sophia, clarify the origin of the diploid D. sophia genome, and provide valuable genomic resources for comparative genomics and research into polyploid evolution.

Acknowledgements

We are grateful to Prof. Hong-Qing Ling and Dr. Fengming Han for critical reading and helpful suggestions. This work was supported by Key Program of the Chinese Academy of Sciences (KJZD-SW-L13), Talents Program of Jiangxi Province (jxsq2020101020 and jxsq2020101088), the Key Research Projects of Jiangxi Province (20223BBG71003), Jiujiang Basic Research Program (S2024KXJJ0001), National Natural Science Foundation of China (32260768), and the Innovation Program of the Chinese Academy of Agricultural Sciences.

Author contributions

Conceptualization, D.K. and Y.L.; Formal Analysis, W.W., C.C., and X.S.; Investigation, J.W., H.L., T.Z., M.X., B.L., F.L., Y.W., J.Z., L.Z., and X.S.; Writing—Original Draft, W.W., C.C., J.W., X.S., and Y.L.; Writing—Review and Editing, J.W., W.L., M.H., F.C., D.K., and Y.L.; Supervision, J.Z., F.L., W.L., F.C., D.K., and Y.L.

Data availability

All the raw sequencing data generated for this project have been deposited at the Genome Sequence Archive (https://ngdc.cncb. ac.cn/gsa/) under BioProject accession No. PRJCA034923.

Conflicts of interest statement

No conflict of interest is declared.

Supplementary material

Supplementary material is available at Horticulture Research online.

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