Volume 34, No 12, Dec 2024

ISSN: 1001-0602 
EISSN: 1748-7838 2018 
impact factor 17.848* 
(Clarivate Analytics, 2019)

Volume 34 Issue 12, December 2024: 859-872   |  Open Access

ORIGINAL ARTICLES

Population-wide DNA methylation polymorphisms at single-nucleotide resolution in 207 cotton accessions reveal epigenomic contributions to complex traits

Ting Zhao^1,† , Xueying Guan^1,† , Yan Hu^1,† , Ziqian Zhang^1,† , Han Yang^2,† , Xiaowen Shi¹ , Jin Han¹ , Huan Mei¹ , Luyao Wang³ , Lei Shao¹ , Hongyu Wu¹ , Qianqian Chen¹ , Yongyan Zhao¹ , Jiaying Pan¹ , Yupeng Hao¹ , Zeyu Dong¹ , Xuan Long¹ , Qian Deng¹ , Shengjun Zhao^1,3 , Mengke Zhang^1,3 , Yumeng Zhu^1,3 , Xiaowei Ma¹ , Zequan Chen¹ , Yayuan Deng^1,3 , Zhanfeng Si¹ , Xin Li^2,4 , Tianzhen Zhang^1,3,* , Fei Gu^2,4,* , Xiaofeng Gu^5,* , Lei Fang^1,3,*

¹Zhejiang Provincial Key Laboratory of Crop Genetic Resources, the Advance Seed Institute, Key Laboratory of Plant FactoryGeneration-adding Breeding, Ministry of Agriculture and Rural Affairs, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, Zhejiang, China
²Damo Academy, Alibaba Group, Hangzhou, Zhejiang, China
³Hainan Institute of Zhejiang University, Yazhou Bay Science and Technology City, Yazhou District, Sanya, Hainan, China
⁴Hupan Lab, Hangzhou, Zhejiang, China
⁵Biotechnology Research Institute, Chinese Academy of Agricultural Sciences, Beijing, China
^†These authors contributed equally: Ting Zhao, Xueying Guan, Yan Hu, Ziqian Zhang, Han Yang
Correspondence: Tianzhen Zhang(cotton@zju.edu.cn)Fei Gu(gufei.gf@alibaba-inc.com)Xiaofeng Gu(guxiaofeng@caas.cn)Lei Fang(fangl@zju.edu.cn)

DNA methylation plays multiple regulatory roles in crop development. However, the relationships of methylation polymorphisms with genetic polymorphisms, gene expression, and phenotypic variation in natural crop populations remain largely unknown. Here, we surveyed high-quality methylomes, transcriptomes, and genomes obtained from the 20-days-post-anthesis (DPA) cotton fibers of 207 accessions and extended the classical framework of population genetics to epigenetics. Over 287 million single methylation polymorphisms (SMPs) were identified, 100 times more than the number of single nucleotide polymorphisms (SNPs). These SMPs were significantly enriched in intragenic regions while depleted in transposable elements. Association analysis further identified a total of 5,426,782 cis-methylation quantitative trait loci (cis-meQTLs), 5078 cis-expression quantitative trait methylation (cis-eQTMs), and 9157 expression quantitative trait loci (eQTLs). Notably, 36.39% of cis-eQTM genes were not associated with genetic variation, indicating that a large number of SMPs associated with gene expression variation are independent of SNPs. In addition, out of the 1715 epigenetic loci associated with yield and fiber quality traits, only 36 (2.10%) were shared with genome-wide association study (GWAS) loci. The construction of multi-omics regulatory networks revealed 43 cis-eQTM genes potentially involved in fiber development, which cannot be identified by GWAS alone. Among these genes, the role of one encoding CBL-interacting protein kinase 10 in fiber length regulation was successfully validated through gene editing. Taken together, our findings prove that DNA methylation data can serve as an additional resource for breeding purposes and can offer opportunities to enhance and expedite the crop improvement process.

https://doi.org/10.1038/s41422-024-01027-x

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