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Significance Plant DNA methylation, which occurs in three sequence contexts (CG, CHG, and CHH, where H refers to A, T, or C), is established and maintained by different mechanisms. In this study, we present genome-wide chromatin accessibility profiles of Arabidopsis mutants that are deficient in CG, CHG, and/or CHH methylation. Through a combination of DNA methylation, chromatin accessibility, and higher-order chromosome conformation profiling of these mutants, we uncover links between DNA methylation, chromatin accessibility, and 3D genome architecture. These results reveal the interplay between CG and non-CG methylation in heterochromatin maintenance and suggest that DNA methylation can directly impact chromatin structure. DNA methylation is a major epigenetic modification found across species and has a profound impact on many biological processes. However, its influence on chromatin accessibility and higher-order genome organization remains unclear, particularly in plants. Here, we present genome-wide chromatin accessibility profiles of 18 Arabidopsis mutants that are deficient in CG, CHG, or CHH DNA methylation. We find that DNA methylation in all three sequence contexts impacts chromatin accessibility in heterochromatin. Many chromatin regions maintain inaccessibility when DNA methylation is lost in only one or two sequence contexts, and signatures of accessibility are particularly affected when DNA methylation is reduced in all contexts, suggesting an interplay between different types of DNA methylation. In addition, we found that increased chromatin accessibility was not always accompanied by increased transcription, suggesting that DNA methylation can directly impact chromatin structure by other mechanisms. We also observed that an increase in chromatin accessibility was accompanied by enhanced long-range chromatin interactions. Together, these results provide a valuable resource for chromatin architecture and DNA methylation analyses and uncover a pivotal role for methylation in the maintenance of heterochromatin inaccessibility.

DNA methylation-linked chromatin accessibility affects genomic architecture in Arabidopsis