Abstract
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.
Highlights
DNA methylation, a conserved epigenetic mark in most eukaryotes, is essential for growth and development and is associated with many epigenetic phenomena, including imprinting and transposon silencing [1,2,3,4,5]
De novo CHH (H = A, T, or C) methylation depends on RNA-directed DNA methylation (RdDM) and CHROMOMETHYLASE2 (CMT2)-mediated pathways
RNAdirected DNA methylation (RdDM)-dependent CHH methylation is linked to gene activation in ovules, and additional CMT2-dependent methylation leads to silencing of transposons and nearby genes in fibers
Summary
DNA methylation, a conserved epigenetic mark in most eukaryotes, is essential for growth and development and is associated with many epigenetic phenomena, including imprinting and transposon silencing [1,2,3,4,5]. DNA is methylated in CG, CHG and CHH (H = A, T, or C) sites through distinct pathways. Plant-specific CHROMOMETHYLASE3 (CMT3) is primarily responsible for CHG methylation, which is coupled with H3K9 dimethylation [7]. CHH methylation is established de novo by DOMAINS REARRANGED METHYLTRANSFERASE1 and 2 (DRM1 and DRM2) [8] through the RNAdirected DNA methylation (RdDM) pathway [9], involving 24-nt small interfering RNAs (siRNAs) [1, 2]. Recent studies found that CHH methylation could be established by CMT2 [10, 11], through histone H1 and DECREASE-IN-DNA-METHYLATION1 (DDM1) activities [12], which is independent of the RdDM. The role for DNA methylation in developmental regulation is poorly understood
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