A haplotype-resolved chromosome-level genome assembly of autotetraploid Chinese yam (Dioscorea polystachya) elucidates dioscin biosynthesis and regulation

Abstract

Chinese yam (Dioscorea polystachya) is extensively cultivated for nutritional and medicinal applications. However, the lack of a high-quality reference genome has hindered molecular genetic analysis and breeding advancements. Here, we present a haplotype-resolved chromosome-level assembly for this autotetraploid species, featuring a 1.56-Gb genome anchored to 80 chromosomes across four haplotypes and comprising 95 668 protein-coding genes. Following divergence from Dioscorea alata about 4.64 million years ago (Mya), D. polystachya underwent a specific whole-genome duplication ∼1.42 Mya, resulting in an autotetraploid species without subgenomic dominance. Notably, the biosynthetic pathway genes of dioscin, an important steroidal saponin primarily accumulating in tubers, were generally over-retained in D. polystachya compared to the diploid species D. alata. Of these genes, 7-dehydrocholesterol reductase (Dp7-DR) promoted the accumulation of dioscin, exhibiting tuber-specific expression and strong inducibility by abscisic acid, based on transcriptome and gene function analyses. We determined that the transcription factor DpbZIP12 activates Dp7-DR transcription, as supported by yeast one-hybrid, dual-luciferase reporter, and electrophoretic mobility shift assays. Notably, overexpressing Dp7-DR or DpbZIP12 resulted in lower cholesterol levels and elevated dioscin levels, while silencing either gene produced opposite metabolic profiles. These findings delineate promising targets for manipulating dioscin content and expand genetic resources for enhancing yam nutritional quality.

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (32460767 to Q.Z. and 32402560 to N.S.), the Jiangxi Province Key Research and Development Program (20232BBF60007 to N.S.), the Jiangxi Province Natural Science Foundation Project (20224BAB205024 to N.S.), and the Jiangxi Agriculture Research System (JXARS-02 to Q.Z.).

Author contributions

Y.H. and Q.Z. conceived and designed the experiments. N.S., Y.X., and T.L. performed most of the experiments. J.S. extracted the genomic DNA. N.S., Y.X., T.L., and S.W. conducted genome assem-blies, genome annotations, and repeat content analysis. N.S., P.W., Q.Z., and T.C. performed the RNA-seq, mapping, and data process-ing. A.A., S.L., J.L., and Z.L. commented on the manuscript. N.S., Y.X., Y.H., and Q.Z. wrote the paper with input from all authors.

Data availability

The assembled genome sequences are available under accession code PRJCA034592 at the Genome Warehouse (GWH) of the China National Center for Bioinformation (CNCB-NGDC, https://ngdc.cncb.ac.cn/gwh/), and all transcriptome raw sequence read data were uploaded to the China National GeneBank DataBase (CNGBdb, https://db.cngb.org/) website with the accession number CNP0008466. For comparative analysis, the genome of D. alata was obtained from YamBase (https://yambase.org/), and the gene, protein, and annotation files for D. rotundata were sourced from http://genome-e.ibrc.or.jp/home/bioinformatics-team/yam.

Conflicts of interest statement

The authors declare that they have no conflicts of interest.

Supplementary material

Supplementary material is available at Horticulture Research online.

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