Epigenetic Mechanisms of Senescence in Plants: Comparison
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Senescence is a major developmental transition in plants that requires a massive reprogramming of gene expression and includes various layers of regulations. Senescence is either an age-dependent or a stress-induced process, and is under the control of complex regulatory networks that interact with each other. It has been shown that besides genetic reprogramming, which is an important aspect of plant senescence, transcription factors and higher-level mechanisms, such as epigenetic and small RNA-mediated regulators, are also key factors of senescence-related genes. Epigenetic mechanisms are an important layer of this multilevel regulatory system that change the activity of transcription factors (TFs) and play an important role in modulating the expression of senescence-related gene. They include chromatin remodeling, DNA methylation, histone modification, and the RNA-mediated control of transcription factors and genes. 

  • plant senescence
  • aging
  • epigenetic
  • DNA methylation
  • histone modification
  • chromatin remodeling
  • miRNA

1. Overview

Senescence (from the Latin word “senescere”, meaning to grow old) is the final, main developmental phase transition in plants. It occurs at different levels, including at the level of cells, tissues, organs, and the whole plant [1]. Senescence plays an important role in photosynthesis, nutrient remobilization, the completion of the plant life cycle, successful reproduction, stress responses, adaptability, and fitness [2]. Thus, as a major developmental stage, the initiation, progress, and termination of senescence are regulated by complex regulatory pathways and multiple levels of machinery that are influenced by both internal and external factors [2,3][2][3]. Functional genetic and transcriptomic studies have reported that, upon senescence, genetic reprogramming changes the expression of many senescence-related genes [4]. For instance, time series analyses on aging Arabidopsis leaves have shown changes in the expression of up to 16% of genes during senescence [4,5][4][5]. Furthermore, the expression of the genes encoding for those transcription factors also changes during senescence, which makes the mechanisms behind senescence even more complex [3]. Genes that are upregulated during senescence (e.g., genes for the degradation and recycling of nutrients) are called senescence-associated genes (SAGs), and those downregulated (e.g., genes for photosynthesis and chloroplast development) are named senescence downregulated genes (SDGs). Transcription factors (TFs), such as NAC (NAM, ATAF and CUC) and the WRKY family, are known as key TFs that act upstream of the senescence regulatory pathways to activate the senescence genes [1,4,6][1][4][6].

2. DNA Methylation and Plant Senescence

DNA methylation in plant genomes is more extensive than in animals [11][7], and it might be either symmetric, as with CG, which is mainly modulated by DNA- METHYLTRANSFERASE-1 (MET1), or CHG (H is A, T or C), which is mainly modulated by CHROMOMETHYLASE 3 (CMT3), or asymmetric, as with CHH DNA-methylation, which is usually controlled by DOMAINS-REARRANGED METHYLTRANSFERASEs (DRMs) [11][7]. DNA methyltransferases methylate the cytosine bases that make 5-methylcytosine. The methyl groups in DNA can be removed by demethylating enzymes, such as REPRESSOR OF SILENCING 1 (ROS1), DEMETER (DME), and DEMETER-LIKE proteins (DML2/3) that contain DNA glycosylase domains [12,13][8][9]. DNA methylation can regulate gene expression by changing the methylation status of promoters or coding regions of the genes, which changes their binding ability in relation to transcriptional factors [14][10]. In addition, DNA methylation may occur at repeats, such as transposable elements (TEs), to stabilize the heterochromatic structure through silencing those repeats [15][11].
Global DNA methylation changes that occur across developmental life events are reported in plants, such as the giant redwood tree [16][12]. The effect of DNA methylation on the process of senescence is also reported in various aspects, including genes encoding methylase and demethylase enzymes, such as MET1, CMT3, ROS1, DME and DML2/3, but the specific mechanisms are not clear yet [17][13]. In a study on maize, it was suggested that DNA methylation may play a role in whole-plant senescence, as DNA methylation changes were observed at life event transitions that silenced the MuDR (Mutator-–Don Robertson) transposable elements [18][14]. Studies on MET1 transgenic Arabidopsis plants have reported that when MET1 activity is reduced, for example in met1 mutants or with the constant expression of the MET1 antisense gene, hypomethylation in genomic DNA and developmental abnormalities happen. When studying transgenic plants with a MET1 antisense gene fused to the DEMETER (DME) promoter (DME:MET1 a/s), Kim et al. [19][15] showed that when MET1 expression is suppressed, major delays in senescence and other developmental deficiencies occur [19][15].
In addition, the involvement of DNA methylation in maintaining genome integrity by silencing TEs and repetitive sequences during senescence has been reported before [20,21][16][17]. Studies on Arabidopsis and barley have shown the release of TEs during leaf senescence [22,23][18][19]. He et al. [24][20] detected a retrotransposon, called “NMR19” (naturally occurring DNA methylation variation region 19), and its location in the genome, and found that the status of its methylation varies among different Arabidopsis thaliana ecotypes. A class that they named NMR19-4 appeared to be a naturally occurring epiallele that controlled leaf senescence. They found that the DNA methylation of NMR19-4 negatively regulates the transcription of the gene “pheophytin pheophorbide hydrolase (PPH)”, which encodes an enzyme involved in chlorophyll breakdown during leaf senescence. The levels of DNA methylation and TEs were also shown to be related [24][20]. Changes in the level of DNA methylation have been shown during aging in angiosperms as well [25][21]. In another study, Trejo-Arellano et al. [26][22] investigated global methylation levels in Arabidopsis’ dark-induced senescent leaves and reported that, upon senescence, chromatin-silencing genes were downregulated, which led to the interruption of TE silencing and the reactivation of young TEs. They also found that although heterochromatin at chromocenters was decondensed, the global DNA methylation pattern was maintained, with only localized changes in CHH methylation. They concluded that senescence is associated with global chromatin reorganization but is only limited to changes in localized DNA methylation. Vatov et al. [27][23] observed faster senescence progression in two methylation mutants (ros1 and the triple dmr1/2 cmt3 knockout). They showed that as senescence progressed, wide-type plants showed a moderate decrease in DNA methylation, mostly in a CG context, and the most senescent leaf was mainly associated with CHH de novo methylation.
In some plants, aging has shown to cause the loss of morphogenic ability to the point that mature plants do not have the ability to propagate vegetatively [28][24]. It has been reported that this loss of morphogenic ability during plant senescence is related to gene expression changes modulated by DNA methylation [29][25]. Fraga et al. [30][26] investigated the differences in the extent of DNA methylation among the developmental stages of the Pinus radiata trees and found significant DNA methylation differences between the meristematic tissues of juvenile and mature trees, while they found little differences in DNA methylation between their differentiated tissues. They reported a gradual reduction in the extent of genomic DNA methylation in meristematic areas as the level of reinvigoration increased and, therefore, they suggested that the level of DNA methylation can serve as a marker of aging and reinvigoration.
The de-methylation of DNA has also been reported to be accompanied by aging. Studying A. thaliana plants as they aged, Ogneva et al. [31][27] reported the reduced expression of methyltransferase genes, CMT3 and METI, and consequently decreased the cytosine methylation of DNA regions with aging, while the transcription of demethylase genes, ROS1, DME, DML2 and DML3 increased. They concluded that plants experience the demethylation of DNA during aging through a reduction of DNA methyltransferase and an increase in levels of demethylase enzymes [31][27]. Yuan et al. [32][28] also showed that DEMETER-like DNA demethylase gene DML3 controls leaf senescence as the dml3 knockout mutants showed enriched DNA methylation in the promoters of many SAGs that suppressed their expression, resulting in delayed leaf senescence. They suggested that DML3-mediated DNA demethylation may control leaf senescence by regulating the expression of some SAGs [32][28].

3. Histone Modifications and Plant Senescence

Studies have shown that besides DNA methylation, various types of histone modifications also change the dynamic expression of genes when plants move through their developmental phases, such as senescence, or as they respond to the environmental signals. The DNA of eukaryote organisms is wrapped around eight histone molecules (a histone octamer), forming the nucleosome, which is the element of the chromatin structure [33][29]. Nucleosomes can be disassembled/reassembled at specific genome locations in response to environmental and/or developmental cues. The amino acids at the histone N-tails protruding from the histone octamer can be modified by different post-translational modifications, such as methylation, acetylation, H2B monoubiquitination, and phosphorylation, which change the structure of chromatin and, therefore, the expression of the genes, as the interaction of DNA–histone and the accessibility of transcription factors change [34][30]. Among the different histone modifications, the acetylation of lysine 9 at histone H3, (H3K9ac) and the tri-methylation of lysine 4 at histone H2 and H3 (H3K4me2/me3) are associated with inducing the transcription of the genes, while the di-methylation of lysine 9 at histone H9 (H3K9me2) and the tri-methylation of lysine 27 at histone H2 and H3 (H3K27me2/me3) marks are involved in repressing the transcription of the genes [35,36][31][32]. The main histone modifiers are histone acetyltransferases (HATs), histone deacetylases (HDAs or HDs), histone methyltransferases, and histone demethylases [7,37][33][34]. Chromatin remodeling via histone modification has been reported to be a key regulatory mechanism of plant senescence [38,39][35][36]. However, the exact mechanism of histone modification and chromatin-remodeling enzymes regulating senescence is not clear yet. The relationship between histone modification and the expression of senescence-related genes has been reported mostly for H3 histone in the forms of active marks (e.g., H3K4me2/me3 and H3K9ac) and silencing marks (e.g., H3K27me2/me3) [17][13]. The active histone H3K4me3 is more common than H3K9ac, and the expression of more senescence-related genes is associated with H3K4me3 levels [40][37].
One of the first studies that showed a direct connection between histone modification and leaf senescence regulation was when Ay et al. [39][36] reported the involvement of the SUPPRESSION(VAR)3-9 homolog2 (SUVH2) histone methyltransferase in H3 lysine methylation and its role in the delay of leaf senescence. They showed that in plants with overexpressing SUVH2 histone methyltransferase, which is involved in RNA-directed DNA methylation and transcriptional gene silencing by keeping the chromatin structure compact, leaf senescence is delayed. The delay in senescence was because of the repression of key senescence regulators, such as SIRK (senescence-induced receptor-like serine/threonine-protein kinase) or SAG101 (senescence-associated carboxylesterase 101) and was connected to the inhibition of WRKY53, a main transcription factor that promotes leaf senescence. The levels of H3K27me2 and H3K27me3 at the 5′-end region of WRKY53 was elevated and therefore caused the suppressed transcription of WRKY53 along with some SAGs [39,41][36][38]. Jing et al. [42][39] also reported that the expression of SUVH2 causes the repression of WRKY53 and some of the SAGs through H3K27me2/3 modifications. The overexpression of SUVH2 histone methyltransferase represses almost half of the senescence-related regulatory factors (SRRFs). It was reported that in plants with overexpressing SUVH2, leaf senescence is delayed by about two weeks and, therefore, SAGs are either not expressed or repressed [9][40]. Epigenetic indexing at the WRKY53 locus showed that complex epigenetic processes are involved in senescence-related gene expression reprogramming. The induced expression of WRKY53 during senescence was associated with an increasing number of active histone marks (H3K4me2 and H3K4me3) at the 5′ end and coding regions of WRKY53 [39][36], similar to many SAGs, that their upregulation during senescence is associated with increased H3K4me3 levels as well [43][41]. The level of H3K4me3 was increased during either dark-induced or developmental (age-dependent) Arabidopsis leaf senescence, mostly within WRKY53, regulating the expression of many SAGs [9][40].
Brusslan et al. [43][41] studied genome-wide changes in an active (H3K4me3) and silencing (H3K27me3) histone marks using mature and senescing Arabidopsis leaves, and found SAGs with higher H3K4me3 signals in the older leaves, while for genes that downregulate during senescence (SDGs), H3K4me3 was higher in the younger leaves. Likewise, the silencing histone mark, H3K27me3, was lost at some SAGs in the older leaves, and established at some SDGs. This again indicated the role of epigenetic regulation in the expression of senescence-related genes during leaf senescence [43][41]. Next, in a genome-wide distribution study of H3K4me3 marks at different time points during natural developmental senescence, the researchers found upregulated genes with higher H3K4me3 in older leaves, confirming the important role of H3K4me3 in senescence [40][37]. They again reported that in senescing leaves, the H3K4me3 mark increased in senescence upregulated genes and decreased in senescence downregulated genes. In addition, genes that upregulate at senescence time showed a loss of the H3K27me3 mark in older tissue, while only a few of the senescence downregulated genes gained the H3K27me3 mark [40][37].
A continuous lack of light causes changes in the expression of many genes, which leads to various developmental disruptions, including early leaf senescence [44][42]. To investigate the epigenetic mechanism behind this, Yan et al. [45][43] studied the global epigenomic profiles of H3K4me3 under dark stress in Arabidopsis. They found an increase in the number of H3K4me3 marks after three days of darkness, and the genes with dark-increased H3K4me3 were mainly involved in senescence. The upregulated genes after dark treatment were highly expressed in senescent leaves as opposed to younger leaves and, likewise, the downregulated genes after dark treatment showed lower expression in senescing leaves than in younger leaves [45][43]. They also compared the changes in H3K4me3 in dark-induced and age-associated leaf senescence, where they found that H3K4me3 changes were correlated with gene expression during age-related leaf senescence, as it had also been reported by Brusslan et al. [40][37]. GO enrichment analysis showed that some of the upregulated genes with increased H3K4me3 signals were genes, such as WRKY6, SAG113, and SAG101, that are known to promote senescence, and some were involved in dark-induced leaf senescence (e.g., Abscisic acid (ABA) Insensitive 5 (ABI5), ETHYLENE INSENSITIVE 3 (EIN3), and ORESARA 1 (ORE1)) [46][44]. Therefore, they concluded that H3K4me3 has an important impact on the regulation of SAGs and there are overlapping genes with changed H3K4me3 signals during dark-induced and natural leaf senescence. JMJ16 is an Arabidopsis JmjC-domain-containing protein and acts as an H3K4 demethylase. A decrease in JMJ16 is reported to be associated with the increase in the amount of H3K4me3 during senescence [47][45]. Liu et al. [47][45] reported that JMJ16 negatively affects age-dependent leaf senescence by repressing WRKY53 and SAG201 via its demethylase activity and reducing their level of H3K4me3. They found the overexpression of various SAGs associated with the hypermethylation of H3K4me3 in loss-of-function jmj16 mutants [47][45].
An important role of leaf senescence is known to be facilitating nutrient remobilization to younger leaves and reproductive organs to maximize fitness, and many SAGs are upregulated during the process. It is interesting to know how SAGs remain transcriptionally inactive before the onset of leaf senescence to ensure photosynthesis. Wang et al. (Wang, Gao et al. 2019), identified an epigenetic mechanism that prevents the premature expression of these genes. They reported that RELATIVE OF EARLY FLOWERING 6 (REF6) promotes H3K27me3 demethylation at the promoter and coding regions of ten target senescence genes to activate them. The number of H3K27me3 marks decreases during senescence, as they repress the expression of senescence genes. This is caused by genes, such as REF6 [48][46]. REF6 directly activates senescence regulators, such as ETHYLENE INSENSITIVE 2 (EIN2), ORE1, and NAP (NAC-like, activated by AP3/P1), and acts as a binding protein for the promoter of NYE1 (NONYELLOWING1) gene and promotes chloroplast degradation during leaf senescence by upregulating this gene [49][47].
Another histone mark that is reported to have a role in regulating leaf senescence is histone acetylation (H3K9ac). The coordinated activities of histone acetylation and deacetylation play important roles in gene expression and are organized by HATs and HDAs enzymes. While histone acetylation correlates with active transcription, histone deacetylation is often associated with the repressing and silencing of the gene by removing acetylation and inducing chromatin compaction [50,51][48][49]. The direct effect of histone acetylation on the expression of the genes that may promote senescence was first reported in a study on an acetyltransferase Elongator. Zhu et al. [52][50] studied the function of an Elongator complex protein 2-like gene in tomatoes via RNAi-mediated gene silencing and found that the silencing of this acetyltransferase Elongator gene accelerated leaf senescence and sepal senescence. Brusslan et al. [40][37] analyzed the abundance of both H3K4me3 and H3K9ac in Arabidopsis leaves at different time points during developmental senescence and reported that many upregulated senescence-related genes were also marked with H3K9ac, which activates TFs, such as WRKY53. They found that the H3K9ac levels around SAGs were high at the early stages of senescence and decreased gradually as senescence progressed. This was the opposite of what happens in the case of the H3K4me3 level, which it is usually low at the early stage of senescence and increases drastically towards the end of the senescence stage. The histone marks were highly convergent throughout aging; however, the average number of H3K4me3 marks around the SAGs covered the gene area almost two times more than what was covered by H3K9ac marks.
Histone deacetylation has been reported as a leaf senescence regulator in Arabidopsis as well. Huang et al. [53][51] found that HDA15 interacts with the single-stranded DNA-binding protein WHIRLY1 and increases H3K9ac in the promoter of WRKY53 to suppress its expression and therefore delay leaf senescence. Furthermore, histone acetyltransferase HAC1 is known to positively regulate leaf senescence [54][52], whereas various HDACs, including HDA9, HDA15, HD2C, and AtSRT1 (from SILENT INFORMATION REGULATOR2 (SIR2) family proteins), have been shown to have a negative effect on stress-triggered senescence in Arabidopsis [55,56][53][54]. Analyzing the functions of histone deacetylases (HDAs), Tian and Chen [57][55] studied transgenic plants that overexpress antisense HDA19, a histone deacetylases also known as AtHD1 that belongs to the RPD3 (reduced potassium dependency 3) class of histone deacetylases [37][34], and reported the global changes in the histone deacetylation profile that affected the regulation of senescence. Wu et al. [58][56] showed that the loss-of-function mutants of HDA6 show increases in the acetylation of histone H3 and the downregulation of SAG12 and SEN4, which delayed the senescence. However, the expression of RPS17 (ribosomal protein S17), which is normally downregulated at the time of senescence, was maintained at high level in the mutants. HDA9 is known to promote leaf senescence and regulate the genes involved in the onset of both developmental and dark-induced senescence. In HDA9 mutants, leaf senescence is reported to be delayed [51,59][49][57]. Chen et al. [51][49] reported the mechanism by which the HDA9-PWR-WRKY53 complex coordinates several signaling pathways to regulate the global transcription of genes during leaf senescence. They showed that HDA9 makes a complex with a SANT domain-containing protein POWERDRESS (PWR) and the transcription factor WRKY53. The WRKY53 then directs POWERDRESS and HDA9 to the promoters of negative senescence regulators, such as AUTOPHAGY 9 (ATG9), NUCLEAR PROTEIN X 1 (NPX1), and WRKY57 [38][35]. As mentioned before, most of these senescence studies have focused on Arabidopsis leaf senescence, which has a short life and can be easily experimentally manipulated. Future studies focusing on whole-plant senescence are necessary to obtain a better understanding of the role of histone modifications in plant senescence. One study has focused on the epigenetic and transcriptional mechanisms of fruit senescence in longan trees, which showed that histone deacetylase HD2 interacts with ethylene response factors (ERFs) and is involved in longan plant fruit senescence [60][58]. They analyzed one histone deacetylase 2-like gene, DlHD2 and two ethylene-responsive factor-like genes, DlERF1 and DlERF2, during fruit senescence, and showed that DlHD2 might cooperate with DlERF1 to regulate the transcription of fruit senescence genes [60][58].

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