Regulation of Leaf Longevity by DML3-Mediated DNA Demethylation

Abstract

Leaf senescence is driven by the expression of senescence-associated genes (SAGs). Developmentspecific genes often undergo DNA demethylation in their promoter and other regions, which regulates gene expression. Whether and how DNA demethylation regulates the expression of SAGs and thus leaf senescence remain elusive. Whole-genome bisulfite sequencing (WGBS) analyses of wild-type (WT) and demeter-like 3 (dml3) Arabidopsis leaves at three developmental stages revealed hypermethylation during leaf senescence in dml3 compared with WT, and 20 556 differentially methylated regions (DMRs) were identified by comparing the methylomes of dml3 and WT in the CG, CHG, and CHH contexts. Furthermore, we identified that 335 DMR-associated genes (DMGs), such as NAC016 and SEN1, are upregulated during leaf senescence, and found an inverse correlation between the DNA methylation levels (especially in the promoter regions) and the transcript abundances of the related SAGs in WT. In contrast, in dml3 the promoters of SAGs were hypermethylated and their transcript levels were remarkably reduced, and leaf senescence was significantly delayed. Collectively, our study unraveled a novel epigenetic regulatory mechanism underlying leaf senescence in which DML3 is expressed at the onset of and during senescence to demethylate promoter, gene body or 3 0 UTR regions to activate a set of SAGs.

Leaf senescence: progression, regulation, and application

“…Knockout of DML3 results in DNA hypermethylation in the promoters of many SAGs whose expression is consequently suppressed, leading to a significant delay in leaf senescence. This suggests that DML3-mediated DNA demethylation regulates leaf senescence by controlling the expression of a subset of SAGs (Yuan et al 2020). However, the detailed mechanisms of how histone modification and chromatinremodeling enzymes directly regulate SAGs expression remain exclusive.…”

A WRKY transcription factor, TaWRKY42-B, facilitates initiation of leaf senescence by promoting jasmonic acid biosynthesis

“…Generally, the initiation of leaf senescence is age-dependent and triggered by developmental cues [5]. Additionally, leaf senescence is tightly controlled by epigenetic modification, circadian clock, autophagy, chlorophyll metabolism, and transcriptional regulation [6][7][8][9][10][11][12][13][14][15][16][17]. Meanwhile, when plants encounter abiotic and biotic stresses, the initiation of senescence will be accelerated [5,18].…”

Senescence-Associated Glycine max (Gm)NAC Genes: Integration of Natural and Stress-Induced Leaf Senescence

“…Leaf senescence is a developmentally programmed or environmentally induced process by which cells activate the programmed cell death response (PCD), resulting in the relocation of nutrients towards different organs. Leaf senescence is not an unregulated cell death process initiated by aging; it is rather a sophisticated biochemical and genetic mechanism that controls cell/tissue/organism development through dynamic modulation of gene expression, metabolic reprogramming, and structural changes [ 1 , 2 , 3 , 4 , 5 , 6 ]. At the cellular level, leaf senescence can be modulated by environmental stimuli, signaling components, metabolism regulators, and phytohormones, although hormones are the major players in the different stages of leaf senescence.…”

“…This entire process is tightly regulated by gene expression control and hormone signaling. Thus, several transcription factors have been identified as modulating the expression of CCG genes upon hormone triggering and stress/environmental conditions [ 4 , 5 , 6 , 7 , 8 , 9 ].…”

“…A complex signaling network is triggered during the leaf senescence process; it is activated by aging or environmental factors, but the mechanisms and players that control the whole process are not fully understood. Nevertheless, forward and reverse genetic studies, next-generation sequencing (NGS), and omics technologies have enabled identification of components, signaling molecules, and different genes involved in several steps of the leaf senescence process [ 3 , 4 , 5 , 6 ]. To date, the leaf senescence database (LSD) has broadly listed over 5000 SAGs (senescence-associated genes) and 600 mutants from 68 species [ 7 ], and the use of these different tools has provided deep knowledge regarding the leaf senescence mechanism.…”