Abstract
In plants, aerial organs originate continuously from stem cells in the center of the shoot apical meristem. Descendants of stem cells in the subepidermal layer are progenitors of germ cells, giving rise to male and female gametes. In these cells, mutations, including insertions of transposable elements or viruses, must be avoided to preserve genome integrity across generations. To investigate the molecular characteristics of stem cells in Arabidopsis, we isolated their nuclei and analyzed stage‐specific gene expression and DNA methylation in plants of different ages. Stem cell expression signatures are largely defined by developmental stage but include a core set of stem cell‐specific genes, among which are genes implicated in epigenetic silencing. Transiently increased expression of transposable elements in meristems prior to flower induction correlates with increasing CHG methylation during development and decreased CHH methylation, before stem cells enter the reproductive lineage. These results suggest that epigenetic reprogramming may occur at an early stage in this lineage and could contribute to genome protection in stem cells during germline development.
Highlights
Active transposable elements (TEs) are a severe threat to genome integrity in all organisms, especially in germline cells that form gametes and subsequent generations
We applied fluorescence-activated nuclear sorting (FANS) (Zhang et al, 2008) to nuclei isolated from manually enriched shoot apical meristem (SAM) and collected mCherry-positive and mCherry-negative nuclei, with non-transgenic plants as controls (Figs 1A and EV1A, Appendix Table S1) (Gutzat & Mittelsten Scheid, 2020)
In addition to genes involved in meristem maintenance and general regulation of gene expression, we found significant enrichment of up-regulated genes related to shoot system and flower development, even at early time points E and D7 (Table EV3, Appendix Fig S1) indicating that formation of the transcriptional signatures in SAM stem cells precedes later developmental processes
Summary
Active transposable elements (TEs) are a severe threat to genome integrity in all organisms, especially in germline cells that form gametes and subsequent generations. Strategies for suppressing TEs differ in animals and plants, based on their respective life cycles. The body plan is fixed during embryonal development, including an early specification of germ cell precursors. During an animal’s lifetime, specialized stem cell populations support tissue and organ regeneration. Many plant cells remain totipotent, and plants develop organs de novo during their life, with constant feedback from, and adjustment to the environment. As many TEs are mobilized by external triggers, the risk of insertions that affect subsequent generations is generally much higher in plants
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