Dark-Induced Senescence Causes Localized Changes in DNA Methylation

Abstract

Senescence occurs in a programmed manner to dismantle the vegetative tissues and redirect nutrients towards metabolic pathways supporting reproductive success. External factors can trigger the senescence program as an adaptive strategy, indicating that this terminal program is controlled at different levels. It has been proposed that epigenetic factors accompany the reprogramming of the senescent genome; however, the mechanism and extent of this reprogramming remain unknown. Using bisulphite conversion followed by sequencing, we assessed changes in the methylome of senescent Arabidopsis (Arabidopsis thaliana) leaves induced by darkness and monitored their effect on gene and transposable element (TE) expression with transcriptome sequencing. Upon dark-induced senescence, genes controlling chromatin silencing were collectively down-regulated. As a consequence, the silencing of TEs was impaired, causing in particular young TEs to become preferentially reactivated. In parallel, heterochromatin at chromocenters was decondensed. Despite the disruption of the chromatin maintenance network, the global DNA methylation landscape remained highly stable, with localized changes mainly restricted to CHH methylation. Together, our data show that the terminal stage of plant life is accompanied by global changes in chromatin structure but only localized changes in DNA methylation, adding another example of the dynamics of DNA methylation during plant development.

Epigenetic Landmarks of Leaf Senescence and Crop Improvement

“…The study of leaf senescence has been complicated by the lack of coordinated development of the cells within an individual leaf, and various methods have been used to artificially induce senescence to obtain a synchronous process. For example, dark-induced senescence has been used frequently as a useful method to induce synchronous senescence as many typical senescence symptoms such as chlorophyll degradation and loss of protein occur [ 11 , 17 , 18 , 19 , 20 ]. Sobieszczuk-Nowicka et al [ 11 ] reported evident differences in gene medleys between dark-induced leaf senesce (DILS) and developmental senescence.…”

“…The high level of 5-methylcytosine is specific for the inactive state of chromatin. This mechanism is essential for silencing repetitive sequences and transposable elements (TEs), DNA sequences which can change their position within a genome, to avoid uncontrolled transposition, which allows for genome integrity maintenance [ 20 ]. In plants, it can be categorized into three types: symmetric CG or CHG (H is A, T or C) and asymmetric CHH DNA-methylation.…”

“…The latest study conducted by Trejo-Arellano et al [ 20 ] showed significant downregulation of methylation pathway elements responsible for maintaining the integrity of the chromatin during dark-induced senescence, e.g., RdDM (RNA-directed DNA methylation) and DDM1/CMT2 (nucleosome remodelers: decreased DNA methylation 1/CHH methyltransferase) correlated with CHH methylation and heterochromatin at chromocenter decondensation. However, only local changes in methylome were present.…”

Looking At the Past and Heading to the Future: Meeting Summary of the 6th European Workshop on Plant Chromatin 2019 in Cologne, Germany

“…The The yellowing of the covered-senescent leaves was accompanied by changes in the expression of transposable elements that depending on the TE family can be unaltered, up-or downregulated. Moreover, GO and pathway categories related with the maintenance of chromatin structure were enriched among the downregulated genes (for the complete analysis see Trejo-Arellano et al, 2019). Overall, the global DNA methylation landscape of the senescent leaves remained remarkably stable with only few localized DNA methylation changes detected, particularly in the CHH context (B) Working model for the UBP12/13-mediated gene repression.…”

Moderate DNA methylation changes associated with nitrogen remobilization and leaf senescence in Arabidopsis

“…Detailed whole genome bisulfite sequencing (WGBS) on leaves during dark-induced leaf senescence in Arabidopsis revealed that the methylation landscape remains largely stable, with some hypomethylation occurring in CHH contexts (Trejo-Arellano et al, 2020). By contrast, Yuan et al (2020) identified a genome wide reduction in methylation in all three cytosine contexts in age-related senescence, with the particular reduction of CG methylation in CG-rich sequences in close proximity to gene transcriptional start sites (TSS).…”