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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., Competing Interests: Competing interests: The authors declare no competing interests., (© 2024. The Author(s).)

The noncoding regions throughout the genome are in large part comprised of transposable elements (TEs), some of which are functionalized with long intergenic noncoding RNAs (lincRNAs). DNA methylation is predominantly associated with TEs, but little is known about its contribution to the transcription of lincRNAs. Here, we examine the lincRNA profiles of DNA methylation-related mutants of five species, Arabidopsis, rice, tomato, maize, and mouse, to elucidate patterns in lincRNA regulation under altered DNA methylation status. Significant activation of lincRNAs was observed in the absence of CG DNA methylation rather than non-CG. Our study establishes a working model of the contribution of DNA methylation to regulation of the dynamic activity of lincRNA transcription., (© 2021 Federation of European Biochemical Societies.)

DNA methylation is essential for plant and animal development. In plants, methylation occurs at CG, CHG, and CHH (H = A, C or T) sites via distinct pathways. Cotton is an allotetraploid consisting of two progenitor genomes. Each cotton fiber is a rapidly-elongating cell derived from the ovule epidermis, but the molecular basis for this developmental transition is unknown. Here we analyzed methylome, transcriptome, and small RNAome and revealed distinct changes in CHH methylation during ovule and fiber development. In ovules, CHH hypermethylation in promoters correlated positively with siRNAs, inducing RNA-dependent DNA methylation (RdDM), and up-regulation of ovule-preferred genes. In fibers, the ovule-derived cells generated additional heterochromatic CHH hypermethylation independent of RdDM, which repressed transposable elements (TEs) and nearby genes including fiber-related genes. Furthermore, CHG and CHH methylation in genic regions contributed to homoeolog expression bias in ovules and fibers. Inhibiting DNA methylation using 5-aza-2'-deoxycytidine in cultured ovules has reduced fiber cell number and length, suggesting a potential role for DNA methylation in fiber development. Thus, RdDM-dependent methylation in promoters and RdDM-independent methylation in TEs and nearby genes could act as a double-lock feedback mechanism to mediate gene and TE expression, potentiating the transition from epidermal to fiber cells during ovule and seed development.