Many studies have reported that dynamic changes of DNA methylation occurred during cell senescence of plant. Ogneva et al. (2016) initially demonstrated the dynamic profile of DNA methylation during cell senescence of Arabidopsis shoots aging by using a methylation-sensitive DNA fragmentation (MS-AFLP) assay. They showed a global declining in DNA methylation levels during Arabidopsis shoots aging, simultaneously accompanying by a downregulation of CMT3 and MET1 methyltransferase genes, and an upregulation of demethylase genes including ROS1, DME, DML2, and DML3 (Ogneva et al., 2016). By using methylated DNA immunoprecipitation (MeDIP-Seq) assay, comparison of global DNA methylation level between young and senescent cotyledons of Gossypium hirsutum L. showed that DNA methylation levels at the promoters, regions around CpG islands, as well as transcriptional termination regions were decreased in senescent cotton cotyledons. The decreased DNA methyltransferase activity was mainly linked to secondary metabolite processes from young to senescence tissue (Dou et al., 2017). Later, by using bisulfite-sequencing analysis, Trejo-Arellano et al. (2020) addressed that local DNA methylation decreased in CHH context during dark-induced senescence, with global loosened changes in chromatin structure in the terminal stage of plant life. However, Zhang et al. (2021) presented the profiles of single-base-resolution DNA methylation of Moso bamboo leaves covering the extensive process of vegetative growth and transition to flowering. Their findings indicated that CHH methylated level gradually accumulated from vegetative growth to reproductive development, and genes with CG methylation changes were enriched in ‘vegetative to reproductive phase transition of meristem’ GO term. Integrative analysis of DNA methylation data with RNA-seq data revealed that DNA methylation in various regions of promoters, exons and introns might have different regulatory mechanism to control gene expression (Zhang et al., 2021).

Several DNA methylase and demethylase enzymes have been studied to provide mechanistic insight into global changes in DNA methylation during cell senescence of plant leaf. In Arabidopsis, neither overall nor spatial reduction of DNA methyltransferase MET1 activity by a met1 mutation or local expressed MET1 antisense gene driven by DEMETER (DME) promoter, led to global DNA hypomethylation and developmental defects including reduced fertility, failed flowering, or greatly delayed plant senescence (Kim et al., 2008). Whole-genome bisulfite sequencing (WGBS) were performed in Arabidopsis leaves of demeter-like 3 (dml3) mutant that lost the DEMETER-like DNA demethylase, relative to wild-type at three developmental stages, namely NS (non-senescent), ES (early senescence)), and LS (late senescence). While a reduction of genome-wide methylation levels at CG context was observed at stage transition from NS to LS in wild-type, loss of DML3 led to significant increase of DNA methylation at the promoters of several senescence-associated genes, thereby suppressing their expression and delaying leaf senescence. These results demonstrated that DML3 activating DNA demethylation and expression of selected senescence-associated genes modulated leaf senescence (Yuan et al., 2020) ( Figure 1A ). More recently, Vatov et al. (2022) reported that initial cytosine methylation at CG context declined moderately during progressing leaf senescence, while moderate de novo methylation of cytosines at CHH context associated with late senescence. Moreover, hypermethylated mutant ros1 and hypomethylated triple mutant dmr1/2 cmt3 (ddc) displayed a faster senescence progression and enhanced nitrogen remobilization from the leaves. Loss of methylation in CHG and CHH contexts at W-box element targeted by WRKYs as well as a core motif recognized by bZIP transcription factors (ACGTG) was observed in ddc. Differentially methylated regions at ROS1 promoter were related to down-regulation of ROS1 with the progression of senescence (Vatov et al., 2022) ( Figure 1B ). It seems that the DNA methylation during leaf senescence decrease because of cytosine methylation maintenance inhibition. Nonetheless, the linkage between moderate methylome changes and up-regulated genes during leaf senescence remains unclear.

In rice, disruption of DOMAINS REARRANGED METHYLASE 2 orthologous (OsDRM2) displayed abnormal DNA methylation and developmental tissues like delayed or absent heading or growth defects (Moritoh et al., 2012). Mutations in OsDRM2 cause near-complete CHH methylation loss and derepression of small transposable elements such as MITEs. These MITEs are commonly found at the ends of protein-coding genes. In osdrm2 plant, there is a significant reduction in CHH methylation at the ends of protein-coding genes. This finding suggests that OsDRM2-dependent CHH methylation primarily focuses gene-associated small TEs, which consequently impacts the methylation of protein-coding genes and promotes plant senescence (Tan et al., 2016) ( Figure 1C ). Silencing the elongation complex protein 2-like gene (SlELP2L) inhibited leaf growth, accelerated leaf and sepal senescence, and produced dark green fruit. Gene expression analysis revealed that the SlELP2L-deficient plants had up-regulated gene expression level of DNA methyltransferases, implying that SlELP2L may play a role in DNA methylation in tomato (Zhu et al., 2015). Meanwhile, Domains Rearranged Methyltransferase7 (SlDRM7), a regulator of leaf senescence of tomato, was activated by aging- and dark-induced senescence. Silencing of SlDRM7 causes SlLFNR1’s promoter to become hypermethylation, SlPORB’s and SlPsaK’s introns to become hypermethylation, and SlGWD’s intron to become hypomethylation, resulting in their expression repression, leads to the inhibition of photosynthesis and starch degradation, which ultimately leads to leaf senescence and chlorosis. Additionally, SlDRM7 can be induced by leaf senescence, creating a feedback regulatory loop that balances vegetative growth and leaf senescence (Wen et al., 2022) ( Figure 1D ). Further, Li et al. (2022) reported that leaf senescence of vegetable pak choi was accelerated by treatment with DNA methylation inhibitor 5-Azacytidine. Several DNA methyltransferases were down-regulated in leaves during pak choi storage. By using bisulfite-sequencing assay, it showed that DNA methylation enrichment in the promoter regions of senescence related genes BcSGR2 and BcSAG12 were decreased during storage. These results demonstrated that DNA demethylation was observed in association with the leaf senescence of pak choi.

It is important to note that DNA methylation significantly affects leaf senescence by altering chromatin structure in several ways. He et al. (2018) initially discovered a naturally occurring methylation region, NMR19-4, in Arabidopsis that was identified in the promoter region of the PHEOPHYTIN PHEOPHORBIDE HYDROLASE (PPH) gene, and the methylation status of NMR19-4 was associated with repressed PPH expression and delayed leaf senescence. Epi-allelic variations at key senescence associated genes have also been demonstrated to regulate leaf senescence in several other crop species. In maize, alterations in DNA methylation were observed during critical life event transitions when silencing the Mutator-Don Robertson transposable elements and were proposed to contribute to whole-plant senescence (Li et al., 2010). In barley, a decrease in DNA methylation was observed in senescing leaves at a specific CpG motif located within the promoter region of HvS40 (Ay et al., 2015). Similarly, tomato fruit ripening was accompanied by changes in the DNA methylome. The active DNA demethylation of promoters of fruit-ripening genes bearing a binding site for RIPENING-INHIBITOR was correlated with the transcriptional inhibition of these genes (Zhong et al., 2013; Lang et al., 2017).

The combination of chromatin immunoprecipitation sequencing (ChIP-seq) and RNA-seq methods has been employed to explore the genome-wide landscape of histone modifications and gene transcription during leaf senescence. Brusslan et al. (2015) demonstrated, in Arabidopsis, that senescence-associated genes (SAGs) correlates with elevated levels of H3K4me3 and H3K9ac, while the inhibition of senescence-downregulated genes is related to H3K27me3 (Brusslan et al., 2012; Wang et al., 2019). Zhang et al. (2022) further discovered an increase in the levels of genome-wide H3K9 acetylation during age-dependent senescence in the flag leaf of rice. The findings revealed a coordination correlation between the breadth and density of H3K9ac and both gene transcription initiation and transcript elongation. Integrative analysis revealed a landscape of H3K9ac-associated differentially expressed genes, including SAGs, metabolism-related genes, and genes related to miRNA biosynthesis. These results suggest a complex regulatory network of metabolism-mediated senescence that is associated with H3K9ac during rice flag leaf senescence.

Ay et al. (2009) provided the first evidence linking histone methylation and leaf senescence regulation. Upon activation of WRKY53, a key regulator of leaf senescence, levels of H3K4me3 and H3K4me2 were observed significantly increased at the coding regions and 5’ end of WRKY53. The overexpression of SUVH2, a histone methyltransferase, however, suppressed the transcriptional initiation of WRKY53 and additional SAGs, thereby leading to a delay of leaf senescence (Ay et al., 2009). Subsequent research indicated that overexpression of SUVH2 affected the gene expression regulation of approximately 50% of the 380 senescence-related regulatory factors (Ay et al., 2014). Therefore, SUVH2 has a significant effect on leaf senescence processes. Numerous studies have established several related enzymes controlling histone demethylation and affecting leaf senescence. For example, Liu et al. (2019) discovered that JMJ16, a particular H3K4 demethylase, negatively controlled leaf senescence, mainly by downregulating the expression of positive senescence regulators, WRKY53 and SAG201, by decreasing the H3K4me3 levels at these regions to avoid premature leaf senescence in mature leaves. Wang et al. (2019) reported that H3K27me3 methylation inhibited the transcriptional activation of key SAGs in Arabidopsis. They discovered that RELATIVE OF EARLY FLOWERING 6 (REF6), a H3K27me3 demethylase, directly accelerated the expression of ten specific SAGs, and loss-of-function of REF6 postponed leaf senescence by increasing H3K27me3 levels at all the target SAGs. Recently, in tomato plant overexpressing SlJMJ4, a histone H3K27 demethylase, resulted in premature senescence and enhanced dark-and ABA- induced leaf senescence (Ding et al., 2022). Under dark conditions, SlJMJ4- induced leaf senescence was linked to the upregulation of SlORE1, SlNAP2, SlSAG113 and SlSAG12 by removing H3K27me3. When responding to ABA, the overexpression of SlJMJ4 resulted in an increased binding ability to the loci of SlORE1, SlSAG113, SlNAP2, SlSAG12, SlNCED3 and SlABI5, while decreasing their H3K27me3 levels (Ding et al., 2022).

Histone acetylation is another extensively investigated histone modification that plays a role in leaf senescence. It is generally linked to gene activation, in contrast to histone deacetylation that is associated with gene silencing. The process of histone acetylation is a reversible and is catalyzed by the enzymes histone acetyltransferases (HATs) and deacetylases (HDACs). The earliest study exploring the relationship of histone deacetylases and leaf senescence is AtHD1 (Tian and Chen, 2001). Transgenic plants with antisense-AtHD1 had reduced AtHD1 level and increased levels of tetra acetylated histone H4 resulting in early leaf senescence and other developmental abnormalities (Tian and Chen, 2001). AtHDA6, a type of RPD3-like histone deacetylase, has been implicated in Arabidopsis leaf senescence, jasmonate response, and flowering. In comparison to the wide type (WT), the Arabidopsis HDA6 mutant exhibited higher levels of acetylated H3 and prolonged leaf lifespan (Wu et al., 2008). AtHDA9, a RPD2-like histone deacetylase, was found to play a pivotal role in promoting the onset of leaf senescence. Loss-of-function HDA9 delayed leaf senescence and increased H3K27ac levels. HDA9 formed a repressor complex with POWERDRESS and WRKY53 to suppress the expression levels of negative senescence regulators (WRKY57, NPX1and APG9) by removing H3 acetylation marks, thereby promoting aging in Arabidopsis (Chen et al., 2016). AtHDA15, another histone deacetylase, was reported that it was recruited by the single-stranded DNA-binding protein WHIRLY1 to target WRKY53 loci and reduced H3K9ac enrichment of WRKY53 promoter region, thus repressing its transcription and inhibiting leaf senescence in Arabidopsis (Huang et al., 2018; Huang et al., 2022). Further integrative analysis of the genome-wide H3K9 acetylome and transcriptome of hda15 and hda15 why1 double mutants relative to WT revealed that HDA15 had deacetylase activity and was able to remove H3K9ac at the targeted promoter region repressing the expression of senescence up-regulators, LOX2 and LARP1C and delaying leaf senescence. Additionally, AtHDA15 can be recruited by WHIRLY1 to the regions near the transcription start site (TSS) of nutrient recycling-related genes (GSTF10, DTX1, ABCC9), the D1 synthesizer attenuator PDIL1-2 of photosystem II protein, as well as WRKY53 and ELF4. This recruitment removes H3K9ac from their promoter region leading to the repressing of gene expression and the delaying both leaf senescence and flowering during the early stage of plant development (Huang et al., 2022). In rice, overexpression of OsHDA710, which encodes a histone deacetylase, delays leaf senescence, and knockdown oshda710accelerates leaf senescence. In particular, the overexpression of OsHDA710 induces up-regulation of genes related to photosynthesis and chlorophyll biosynthesis, while downregulating certain genes associated with programmed cell death and disease resistance (Zhao et al., 2020). However, up to now, only one histone acetyltransferase, AtHAC1, has been reported in Arabidopsis to play a role in promoting leaf senescence and regulating the expression of ERF022 by H3K9ac enrichment (Hinckley et al., 2019).

Numerous senescence-associated genes (SAGs) in crop plants were identified in impact of histone modification enzymes. For example, during leaf senescence, the expression of the barley gene HvS40, which encodes a potential regulator of leaf senescence, is significantly up-regulated. At the onset of leaf senescence, the regions of promoter and coding sequence of HvS40 enriched H3K9ac, but declined the enrichment of H3K9me2 (Ay et al., 2015). Under drought conditions, H3K9ac enrichment at the promoter and coding sequence regions of HvS40 in barley was affected by single strand DNA/RNA binding protein HvWHIRLY1 protein, promoting leaf senescence (Janack et al., 2016). Conversely, AtWRKY53, a leaf senescence marker regulator in Arabidopsis, its expression was repressed by AtWHIRLY1 through AtWHIRLY1 recruiting HDA15 at the TSS region of AtWRKY53 promoter to remove H3K9ac, repressing leaf senescence (Huang et al., 2018; Huang et al., 2022). In rice, OsSRT1 is an NAD+-dependent histone deacetylase. The enriched H3K9ac level at the senescence marker gene OsSAG12 in OsSRT1 RNAi line was exhibited, resulting in accelerated leaf senescence and programmed cell death (PCD) and aging (Fang et al., 2016). Zhong et al. (2013) further found that OsSRT1 played a crucial role in negatively regulating leaf senescence by repressing gene expression in the MeOH-jasmonates metabolic cascade. Notably, this effect was achieved, in part, through the deacetylation of histone H3K9 in OsPME1 (Zhong et al., 2013). In tomato, under dark conditions and response to ABA, the H3K27me3 enrichment of a series of senescence marker genes such as SlORE1, SlNAP2, SlSAG113, SlSAG12, SlNCED3, and SlABI5 loci was removed by SIJMJ14, inducing leaf senescence (Ding et al., 2022) ( Figure 2 ).

Therefore, active histone modifications such as H3K4me3 and H3K9ac positively associated with SAGs transcription via activating transcription initiation and elongation to accelerate leaf senescence, and silence marks such as H3K27me3 and H3K9me3 negatively linked to SAGs transcription and repress leaf senescence. However till now, only a few histone methyltransferase or acetyltransferase was identified, mechanism of controlling the dynamic of histone modification during cell senescence of plant maintains challenging.

Chromatin conformation is dynamically changed during cell senescence induced by age and environmental cues (Fal et al., 2021; Song et al., 2021; Miryeganeh, 2022). Ay et al. showed the global changes in chromatin organization during age-dependent leaf senescence, including the disassembly of chromatin center, the degradation and speckled distribution of euchromatin, the disappearance of nucleolus (Ay et al., 2009). The heterochromatic regions were distinguished from euchromatic regions during leaf senescence with different histone marks, influencing the accessibility of transcription factors to cis-regulatory elements. Chromatin compaction is also supposed to be involved in gene regulation in leaf senescence induced by unsuitable light intensity (van Zanten et al., 2012; Li et al., 2023). A decrease of chromatin compaction in chromocenters was observed in seedlings exposed to shade. Photoreceptor phyB was reported to inhibit dark-induced leaf senescence (Sakuraba et al., 2014) and loss of phyB leads to lower chromatin density comparing with the wild-type under normal light conditions (Tessadori et al., 2009). Another Photoreceptor CRY2, which suppresses leaf senescence in response to blue light, facilitates chromatin decompaction under low light intensity (van Zanten et al., 2010; Kozuka et al., 2023). Thus, dynamic chromatin reorganization is an important mechanism for controlling leaf senescence by altering gene expression patterns ( Figure 2 ).

Ectopic overexpression of ORE7/ESC that is a chromatin architecture-controlling protein containing an AT-hook DNA-binding motif extended leaf longevity and post-harvest storage life, suggesting a possibility that alteration of chromatin architecture may be a mechanisms to control plant senescence (Lim et al., 2007). A heterozygous line (ORE7/ore7-1D) with lower expression of the activated ORE7 genes was used in this study to analyze the senescent phenotypes. ORE7/ore7-1D mutant showed a delayed senescence phenotype as well as globally altered gene expression. Moreover, more reticular chromatin distribution and intensely nuclear bodies than wild-type plants were observed in ORE7/ore7-1D mutant. It is possible that ORE7 binds to AT-rich DNA sequences and modifies the chromatin architecture in the nucleus, then leading globally altered gene expression. In addition, a subset of hormones (jasmonic acid, abscisic acid, ethylene, and salicylic acid) related genes was down-regulated in ORE7/ore7-1D mutant, suggesting ORE7 repressed the signaling pathway of hormones during plant senescence (Lim et al., 2007).

Two SWI2/SNF2 chromatin-remodeling proteins, namely, chromatin remodeling protein 1 (DEFECTIVE IN RNA-DIRECTED DNA METHYLATION 1, DRD1) and ATP-dependent DNA helicase DDM1 (DECREASED DNA METHYLATION 1), were identified as regulators of leaf senescence (Cho et al., 2016). drd1-6 and ddm1-2 mutants, which both have the occurrence of mutations in the helicase superfamily C-terminal (HELICc) domain, showed delayed leaf senescence during dark-induced senescence and natural senescence. drd1-6 mutants exhibited higher photosynthetic parameters and lower expression levels of SAG12 and chlorophyll degradation-related genes than wile-type plants during dark-induced senescence. Moreover, the transcript levels of 180-bp centromeric (CEN) repeats and pericentromeric repeats termed transcriptionally silent information (TSI) showed slower and lesser increase in the drd1-6 mutant than in the wile-type plants. Similarly, ddm1-2 also exhibited a longer stayed green phenotype and higher photochemical efficiency than wild-type plants (Cho et al., 2016). Therefore, the authors concluded that the ATP-helicase domain might be key component of SWI2/SNF2 chromatin remodelers for regulation of leaf senescence.

Several members of the SWI2/SNF2 complex were also reported to regulate the expression of SAGs during plant senescence, but the exact function is still indistinct. BRAHMA (BRM) is one member of the two catalytic ATPase subunits of the SWI2/SNF2 complex. It directly targets to a large amount of SAGs (Archacki et al., 2013; Li et al., 2016). The H3K27me3 demethylase REF6 facilitates the recruitment of BRM and promotes leaf senescence by activating numerous senescence regulatory and functional genes (Li et al., 2016; Wang et al., 2019). Based on the data of ChIP-chip and ChIP-seq, BRM was reported to target to the promoter region of a large number of SAGs directly (Li et al., 2016; Archacki et al., 2017). Moreover, yeast two-hybrid screens showed BRM may interact with numerous leaf senescence regulators (Efroni et al., 2013), such asWRKY53, ABF3 (abscisic acid responsive elements-binding factor 3), CRF6 (cytokinin response factor 6), WRKY6, RSL1 (RHD SIX-LIKE 1), MYC2 (Basic helix-loop-helix (bHLH) DNA-binding family protein), NAC046, NAC083 (NAC domain containing protein), HB40 (homeobox protein 40), TCP1, TCP4, TCP5, TCP16 (TCP family transcription factor), etc. In addition, BRM can interact with UPL3 and UBP12 to maintain BRM polyubiquitination levels, involving in metabolic cell senescence (Lan et al., 2022). Another catalytic ATPase subunits of the SWI2/SNF2 complex, SYD (SPLAYED) plays both redundant and differential roles with BRM during plant development (Bezhani et al., 2007). It was reported to co-target to a number of senescence related genes such as NAC083, NAC032, NAC019, PIF4, WRKY6 etc. with BRM (Shu et al., 2021), suggesting that SYD and BRM may have redundant roles in regulation of leaf senescence. In addition, genome-wide analysis showed that loss of multiple chromatin remodelers upregulated SAGs (Archacki et al., 2017; Shu et al., 2021), while the genes coding chromatin remodelers such as CHR10, ALTERED SEED GERMINATION 3 (ASG3) and CHR19 (ETL1) were shown to be upregulated during senescence (Breeze et al., 2011). Further studies are necessary to uncover roles of diverse chromatin remodelers in leaf senescence and to determine how various epigenetic modifications coordinately to respond to different internal and external factors during leaf senescence in the future.

microRNAs (miRNAs) are short, non-coding RNAs that are highly conserved and typically range in length from 20 to 24 nucleotides. The discovery of lin-4, the first miRNA, in 1993 (Lee et al., 1993), in nematode Caenorhabditis elegans, marked the beginning of miRNA research, and since then, researchers have identified thousands of miRNAs in both plants and animals. These miRNAs play diverse roles in regulating a wide range of biological processes (Ameres and Zamore, 2013; Dexheimer and Cochella, 2020). miRNAs are essential in post-transcriptional gene silencing, where they suppress gene expression by either triggering the cleavage of complementary mRNAs or inhibiting their translation (Bartel, 2009). Although many factors involved in the processes of miRNA biogenesis, conversion, mobilization, and action in plants, miRNAs regulate target genes through transcript cleavage, translational repression, and enhancing transcription (Rogers and Chen, 2013; Xie et al., 2015; Yu et al., 2017). These regulatory mechanisms have been extensively reviewed (Pulido and Laufs, 2010; Woo et al., 2019; Swida-Barteczka and Szweykowska-Kulinska, 2019; Ostrowska-Mazurek et al., 2020; Guo et al., 2021; Miryeganeh, 2022). Only a few miRNAs have been functionally characterized with specific roles in the regulation of plant senescence. An example of miRNA regulation in leaf senescence and programmed cell death is miR164, which selectively targets NAC-domain containing proteins, including NAC2, KIR1, and ORE1 in Arabidopsis, Sorghum, and Populus (Kim et al., 2009; Li et al., 2013; Kim et al., 2014; Qiu et al., 2015; Fujimoto et al., 2018; Gao et al., 2018; Kim et al., 2018; Wang et al., 2021). AtORE1 is known to be post-transcriptionally regulated by miR164 in Arabidopsis leaf senescence (Kim et al., 2009); MIR164 transcription is inhibited by the direct binding of EIN3 to its promoter. The EIN2-EIN3-ORE1/MIR164-ORE1 pathway is the effector of a signaling cascade of ethylene, a hormone known to accelerate senescence (Li et al., 2013). AtKIR1, another identified NAC TF, possesses the recognition site for miR164, which induces programmed cell death in stigma and in shoots (Gao et al., 2018); and the sorghum bicolor orthologous of KIR1 (D) induces programmed cell death in pitch parenchyma of stalks, it might facilitate nutrient remobilization from source to sink tissues (Gao et al., 2018). miR396 limits growth-regulating factors (GRF) gene expression. It targets seven out of nine Arabidopsis GRFs (Jones-Rhoades and Bartel, 2004). The miR396 level positively correlates with the age of the leaves; it increases while leaf cells proliferate and after the proliferation arrest (Debernardi et al., 2014); miR319 is another miRNA that represses a group of transcription factors known as TEOSINTE BRANCHED/CYCLOIDEA/PCF (TCP). It is responsible for the biosynthesis of jasmonic acid, accelerating vessel formation that linked to the intensification of secondary cell wall biosynthesis and the initiation of programmed cell death, ultimately impacting leaf development and promoting the senescence process (Schommer et al., 2008; Seltmann et al., 2010; Koyama et al., 2017; Sun et al., 2017; Bresso et al., 2018). A recent study addressed the function of miR840–PPR/WHY3 module in Arabidopsis leaf senescence. The results demonstrated that the accumulation of short maturation products of miR840 was correlated with the progression of leaf senescence in Arabidopsis. Conversely, knockdown of miR840 resulted in delayed plant senescence, whereas overexpression of MIR840 enhanced senescence symptoms. miR840* and miR840 worked together to target the same pair of genes, PPR and WHY3, through cleavage transcripts or repressing translation, respectively, reprogramming a series of downstream SAGs (Ren et al., 2022). High-throughput small RNA sequencing techniques have been utilized to identify senescence-inducing miRNAs in Arabidopsis, rice, maize, and tomato. These miRNAs regulate several important pathways including hormone signaling, nutrients remobilization, and response to oxidative stresses during plant senescence (Xu et al., 2014; Thatcher et al., 2015; Qin et al., 2016; Wu et al., 2016; Kim et al., 2018; Ma et al., 2021).

Moreover, some miRNAs are associated with senescence induced by environmental stresses, such as flooding, darkness, extreme temperatures, and nutrition deficiencies. Under high light stress conditions, miR398 targets the CU/Zn superoxide dismutase, leading to leaf senescence (Hao et al., 2022). Authors reported that miR408 retarded dark-induced leaf senescence by repressing plastocyanin (PCY)- SAG14 module, which located on the endomembrane. However, phytochrome interacting factor 3/4/5 (PIF3/4/5) directly bound to the miR408 promoter and repressed its expression to regulate copper translocation to PCY-SAG14 during dark-induced leaf senescence. These findings suggest that the PCY-SAG14 module, which mediates intracellular copper homeostasis, plays an important regulatory role in dark-induced leaf senescence. Mishra et al. (2022) discovered a unique module, miR775-GALT9, during post-submergence recovery. They modulated the ethylene and ABA pathways to regulate the senescence of leaves in Arabidopsis. MIM775 transgenic lines exhibited accelerated senescence during post-submergence recovery, while miR775-overexpresing (Oe1) and galt9 transgenic lines showed delayed senescence. The expression of SAG29, SAG12, and ORE1 decreased in miR775-Oe1 and galt9 transgenic lines, while their expression enhanced in MIM775-1 lines, suggesting that the miR775-GALT9 module regulated the expression of SAGs to control senescence during post-submergence recovery in Arabidopsis. In crop plants, very limited miRNA was reported their detail functions related to leaf senescence. A novel tomato miRNA known as SlymiR208 was identified. When it is overexpressed, the expression of SlIPT2 and SlIPT4 was significantly reduced, and endogenous CK concentrations in leaves was declined, leading to premature leaf senescence, which was in concurrence with the phenotype of Isopentenyltransferases 4 (IPT4)-silenced lines, showing early leaf aging (Zhang et al., 2020). Another example in tomato, miR171b induced by exogenous melatonin directly bound to the α-glucan water dikinase (GWD) gene and activated it expression and increasingly catalyzed starch degradation and leaf senescence after prolonged carbon starvation. In addition, Wang et al. (2021) reported that MiR319 targeted OsGAmyb and OsTCP21 to negatively regulate rice tillering and gain yield (Wang et al., 2021) ( Figure 3 ).

Long noncoding RNA (lncRNA) is a recently discovered class of epigenetic regulator involved in regulating gene expression during plant development and in response to stresses. Dynamic landscapes of long noncoding RNAs were observed in Arabidopsis leaves and rice flag leaves during aging (Huang et al., 2021; Kim et al., 2022). Above, a conserved miR164-NAC regulatory pathway was identified as being involved in leaf senescence. In this pathway, lncRNA MSTRG.62092.1 acts as a competing endogenous RNA (ceRNA) by binding to miR164a and miR164e to regulate three downstream transcription factors. Additionally, two other lncRNAs, MSTRG.31014.21 and MSTRG.31014.36, potentially regulate the abscisic acid biosynthetic gene OsNCED4 (BGIOSGA025169) and the NAC family gene BGIOSGA016313 through osa-miR5809 (Huang et al., 2021). Further investigation was conducted on senescence-associated lncRNAs in Medicago truncatula nodules using high throughput strand specific RNA-seq. The analysis revealed that more than 60% of lncRNAs in the nodules were shown to associate with transposable elements, particularly the TIR/Mutator and Helitron DNA transposons families. It was predicted that 49 differentially expressed lncRNAs (DElncRNAs) were targeted by microRNAs. Notably, the majority of differently expressed target genes of DElncRNAs were related to the membrane component, with almost half of these genes involved in transporting organic material. These findings strongly suggest that DElncRNAs play a crucial role in substance transport across membranes during nodule senescence (Yu et al., 2022). Another example, LncRNA ASCO, a homology of GmENOD40 in Arabidopsis, competitively interacted with the RNA-binding protein NSRs in the nucleus in response to growth hormone (IAA) signals, thereby regulating alternative splicing of NSRs-targeted pre-mRNA to influence root development and senescence (Bardou et al., 2014). In addition, Pathogen effector can induce the transcription of an lncRNA named ELENA1 in Arabidopsis cells, which ELENA1 accumulates MED19a protein in the promoter region of the downstream gene PR1 through interaction, enhancing pathogen induced cell death in the innate immunity of plants (Seo et al., 2017). Up to now, the action aspect of lncRNA in leaf senescence is still limited.