DNA methylation and gene expression dynamics during cotton ovule and fiber development

Abstract

Cotton is the largest source of renewable textile fiber and a successful model of transgenic applications in crop production. However, improving cotton production using fiber-related transgenes is somewhat difficult. This is probably related to unique epigenetic and gene expression changes during fiber development. Here we show that inhibiting DNA methylation impairs fiber development. Genome-wide methylcytosine-, mRNA-, and small RNA-sequencing analyses reveal minor changes in CG and CHG methylation and distinct changes in CHH methylation among different tissues. In ovules CHH hypermethyaltion is associated with small RNA-directed DNA methylation (RdDM) and expression changes of nearby genes in euchromatin. Remarkably, ovule-derived fiber cells not only maintain euchromatic CHH methylation, but also generate additional heterochromatic CHH hypermethylation independent of RdDM, which represses transposable elements (TEs) and nearby genes including fiber-related genes. Furthermore, DNA methylation contributes to the expression bias of homoeologous genes in ovules and fibers. This spatiotemporal DNA methylation in promoters could act as a double-lock feedback mechanism to regulate TE and gene expression, which could be translated into genomic and biotechnological improvement of agronomic traits.