Stage-specific transcriptomes and DNA methylomes indicate an early and transient loss of transposon control in Arabidopsis shoot stem cells

Abstract

In contrast to animals, postembryonic development in plants is modular, and aerial organs originate from stem cells in the center of the shoot apical meristem (SAM) throughout life. Descendants of SAM stem cells in the subepidermal layer (L2) give also rise to male and female gametes (reviewed in 1) and are therefore considered primordial germ cells. In these cells, transmission of somatic mutations including virus and TE insertions must be avoided. Despite their essential role for plant development and intergenerational continuity, no comprehensive molecular analysis of SAM stem cells exists, due to their low number, deep embedding among non-stem cells, and difficult isolation. Here we present a comprehensive analysis of stage-specific gene expression and DNA methylation dynamics in Arabidopsis SAM stem cells. Stem cell expression signatures are mostly defined by development, but we also identified a core set of differentially expressed stemness genes. Surprisingly, vegetative SAM stem cells showed increased expression of transposable elements (TEs) relative to surrounding cells, despite high expression of genes connected to epigenetic silencing. We also find increasing methylation at CHG and a drop in CHH methylation at TEs before stem cells enter the reproductive lineage, indicating an onset of epigenetic reprogramming at an early stage. Transiently elevated TE expression is reminiscent of that in animal primordial germ cells (PGCs) 2 and demonstrates commonality of transposon biology. Our results connect SAM stem cells with germline development and transposon evolution and will allow future experiments to determine the degree of epigenetic heritability between generations.