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Kovalchuk, I. Role of Epigenetic Factors in Response to Stress. Encyclopedia. Available online: https://encyclopedia.pub/entry/51050 (accessed on 04 September 2024).
Kovalchuk I. Role of Epigenetic Factors in Response to Stress. Encyclopedia. Available at: https://encyclopedia.pub/entry/51050. Accessed September 04, 2024.
Kovalchuk, Igor. "Role of Epigenetic Factors in Response to Stress" Encyclopedia, https://encyclopedia.pub/entry/51050 (accessed September 04, 2024).
Kovalchuk, I. (2023, November 01). Role of Epigenetic Factors in Response to Stress. In Encyclopedia. https://encyclopedia.pub/entry/51050
Kovalchuk, Igor. "Role of Epigenetic Factors in Response to Stress." Encyclopedia. Web. 01 November, 2023.
Role of Epigenetic Factors in Response to Stress
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This entry is adapted from the peer-reviewed paper 10.3390/plants12213667

All species are well adapted to their environment. Stress causes a magnitude of biochemical and molecular responses in plants, leading to physiological or pathological changes. The response to various stresses is genetically predetermined, but is also controlled on the epigenetic level. Most plants are adapted to their environments through generations of exposure to all elements. Many plant species have the capacity to acclimate or adapt to certain stresses using the mechanism of priming. In most cases, priming is a somatic response allowing plants to deal with the same or similar stress more efficiently, with fewer resources diverted from growth and development. Priming likely relies on multiple mechanisms, but the differential expression of non-coding RNAs, changes in DNA methylation, histone modifications, and nucleosome repositioning play a crucial role. 

stress tolerance plants DNA methylation abiotic and biotic stresses

1. Introduction

The response to stress is genetically predetermined, since it has been honed by many years of evolution and ancestral environmental exposures. To be able to respond to the environment in a manner similar to their parental cells, each cell has to undergo faithful DNA replication [1]. In addition, all epigenetic marks need to be reproduced. In a stable environment, daughter cells look similar to parental cells in their genetic and epigenetic makeups and often in the set of various metabolites, with variations attributed typically to the developmental stage or tissue specificity. Fluctuations from a stable environment trigger different responses from plants, occurring on biochemical, molecular, and cellular levels, and including changes in primary and secondary metabolites and epigenetic marks, allowing plants to survive stress [2][3]. When stress is no longer present, most of these changes disappear [3], but some are maintained [4], allowing daughter cells to receive the information about the response to stress, allowing plants to acquire partial protection. This somatic stress memory could include various metabolites, as well as changes in DNA methylation or modifications of histone tails [4]. This was recently demonstrated in rice in response to salt—biochemical and epigenetic changes were noted, correlating with stress tolerance [4]. Similarly, the metanalysis of reports on the memory of stress applied prior and during seed germination showed that the memory was based on the changes at the level of chromatin reorganization, alternative transcript splicing, metabolite accumulation, and autophagy [5]. This memory allows the plant to perform better when stress returns. The most well-known examples of such a response to stress are acclimation and adaptation [6].

2. General Stress Response

An active metabolism, including photosynthesis, cellular respiration, and other physiological activities associated with the function of chloroplasts, peroxisomes, and lysosomes, poses a continuous challenge for any organism [7]. These internal stresses produce free radicals that are either damaging molecules such as DNA, RNA, protein, or lipid directly or trigger changes in these molecules by oxidation or via a variety of signaling pathways [8].
Avoidance is not part of a plant’s mechanism of stress response. Environmental stimuli represent external stresses that include, but are not limited to, changes in light intensity, temperature fluctuations, water and nutrient availability, wind, and other mechanical stimuli, as well as an entire realm of biotic interactions that include physical and chemical influences.
To survive these environmental stimuli, individual organisms have genetically programmed mechanisms of response. When stress persists, species also have to develop new adaptive changes in order to survive long term. Stress avoidance is a common response to stress in mobile organisms. Not being able to escape external stresses, plants are limited to mechanisms of tolerance and resistance. Adaptive metabolic changes in somatic cells [9] and heritable transgenerational changes are also part of advanced survival mechanisms. Through the process of evolution, organisms have developed various adaptive mechanisms of survival, and plants seem to be very efficient in doing that [10]. All the above-mentioned mechanisms of stress response require the rapid and efficient perception of stress and activation of signalling cascades, followed by immediate epigenetic changes, gene expression changes, changes in metabolism, and phenotypic changes, as well as short-term acclimation or long term epigenetic and phenotypic adaptation [11].
The mechanisms of general stress response also include acclimation or adaptation to stress, although to be effective, they require priming with milder stress [12]. The response to stress and the initiation of priming may be triggered by changes in plant hormonal levels; the levels of secondary messengers, such as Ca2+, free radicals, and phospholipids; and the activity of signal sensors and transducers, such protein kinases, transcription factors, and ubiquitination machinery, as well as the entire spectrum of epigenetic regulators [13][14][15][16]. Though these mechanisms are commonly functioning in somatic tissues during the growth of an organism, they may also have an intergenerational nature, and can be referred to as intergenerational acclimation [17].
The time and the level of molecular and physiological responses to stress vary for different stresses and depend on previous stress encounters [18]. Figure 1 shows several possible scenarios of priming, followed by the second stress exposure. 
Plants 12 03667 g001
Figure 1. Schematic presentation of stress tolerance with and without priming. A light blue long arrow pointing down indicates the stress exposure. Short dark blue arrow shows priming. “Lp”—latent period (shown as solid double-ended arrow), time required to mount stress tolerance; “St”—stress tolerance (shown as dashed double-ended arrow). Y axis shows arbitrary scale (from 0 to 1.5) indicating the level of stress tolerance. (A) “No priming” is characterized by long Lp and relatively low (at arbitrary level of ~0.7) and short-lasting St. (B) “Priming” is characterized by shorter Lp and higher (at arbitrary level of ~1.0) and longer lasting St. (C) “Priming with delayed stress”—likely similar in effect to “No priming” or somewhere between “Priming” and “No priming”. (D) “Double stress”—first stress response after priming is characterized by shorter Lp and stronger, longer St, similar to “Priming”, but the second stress exposure results in even stronger (arbitrary level of ~1.5) and longer lasting St. (E) “Double Priming” is characterized by shorter Lp and stronger (arbitrary level of ~1.2) and longer lasting St, which is somewhere between “Priming” and “Double stress”.

3. Epigenetic Regulation of Response to Stress

Epigenetic regulation is a critical component of the short- and long-term response to stress. Epigenetic regulation typically involves DNA methylation, histone modifications, and the activity of various non-coding RNAs [19]. Changes in nucleosome positioning, the redistribution of heterochromatin and euchromatin in the nucleus, and the differential binding of chromatin-modifying proteins (excluding histones) and methyl-CpG binding domain (MBD) proteins to DNA are also involved in the efficient response to developmental cues and environmental factors [20]. These epigenetic changes are passed from one somatic cell to another upon cell division, allowing for the effects of acclimation to occur and forming the so-called “transcriptional memory”, the epigenetic timestamp of the best possible transcriptional response to stress [21].

3.1. Changes in Chromatin Structure in Response to Stress

Chromatin is a complex structure consisting of DNA twice-wrapped around the octamer histone core, representing a nucleosome, together with the linker histone H1 and various chromatin-binding non-histone proteins. The chromatin structure is highly dynamic, representing regions of active transcription (euchromatin) or regions with poor transcriptional activity (heterochromatin), with the latter consisting of facultative and constitutive heterochromatin [22]. Various modifications of histone tails either result in the change of affinity of histones to DNA (histone acetylation) or a change in the tail structure, allowing the recruitment of a different kind of readers (histone methylation), thus regulating chromatin condensation and gene expression [23]. In addition, various non-histone proteins, including chromatin remodeling factors (CRF), also actively regulate chromatin condensation and, thus, processes such as transcription, replication, and DNA repair [24].

3.1.1. Heterochromatin Decondensation and Activation of Transposable Elements in Response to Stress

The exposure to stress leads to the removal of nucleosomes from specific genomic locations, nucleosome repositioning [25], the loss of heterochromatin, and the activation of repetitive elements [26]. These events may or may not require changes in histone modifications. A study by Pecinka et al. (2010) showed that long-term exposure to heat in Arabidopsis thaliana resulted in the activation of some repetitive elements [27]. Surprisingly, the activation occurred without the loss of DNA methylation and with only minor changes to histone modifications. Repetitive elements were primarily activated by the loss of nucleosomes and heterochromatin decondensation. The recovery from stress was characterized by nucleosome loading and transcriptional silencing. Curiously, in Chromatin Assembly Factor 1 (CAF-1) mutants impaired in the chromatin assembly, the recovery stage and nucleosome loading were considerably delayed [27]. The substantial dissociation of heterochromatin was observed beyond the recovery phase when silencing and nucleosomes had been reinstalled; the loss of heterochromatin was observed in differentiated tissues of plants exposed to heat, and it lasted in the exposed leaves until they started to show signs of senescence. These experiments demonstrated that the stress memory can persist in the form of chromatin changes long after stress is removed. It also suggests that CAF-1 may act as a negative regulator of the establishment of priming/stress memory.
An additional level of complexity is achieved by differential heterochromatin decondensation in response to heat stress in different cells; the nuclei of meristematic cells do not undergo heat-induced decondensation [27]. This makes sense; if one considers that the heat stress response is transient in nature, it should largely occur in somatic tissues only; the lack of changes in the meristem indicates a safeguarding mechanism for minimizing epigenetic and, possibly, genetic changes in the germ line. This further supports the hypothesis that decondensation is a controlled process that occurs only either during specific stages of plant development or in response to specific stresses such as heat and high-light intensity stresses. Moreover, exposure to these stresses may result in the transcriptional activation of heterochromatin-embedded genes in differentiated cells, but not in dividing cells.

3.1.2. The Role of CRFs in Response to Stress

CRFs are ATPases from the sucrose nonfermenting 2 (Snf2) family that are involved in chromatin remodeling in eukaryotes. The role of CRFs in response to stress is to regulate gene expression, replication, and genome stability by interacting with DNA methylation, histone modification, and RNA processing machineries.
BRM is an ATPase essential for many developmental processes that are both chromatin-dependent (transcription regulation and maintenance of stress memory) and independent (such as pri-miRNA processing) [28]. BRM was shown to interact with many proteins involved in abiotic and biotic stress responses, including HEAT-STRESS-ASSOCIATED 32-kDa PROTEIN (HSA32) [25][29], histone H3-binding protein FORGETTER1 (FGT1), HD2C histone deacetylase, and H3K27me3 demethylase RELATIVE OF EARLY FLOWERING6 (REF6).
BRM also appears to play a role in response to drought and salt stresses. Exposure to these stresses lead to the accumulation of the phytohormone abscisic acid (ABA) [30]. Whereas under normal conditions, BRM represses the key regulator of ABA signaling pathway ABA-INSENSITIVE 5 (ABI5), in response to stress, a high level of ABA leads to the phosphorylation of BRM, resulting in its inactivation and the de-repression of ABI5 transcription [31][32]. There is also a link between energy sensor TARGET OF RAPAMYCIN (TOR) and BRM. TOR appears to repress genes associated with bistable chromatin state, driven by H3K4me3 and H3K27me3, and, thus, actively regulates transcriptional response to stress. BRM, together with CURLEY LEAF (CLF), which deposits H3K27me3 marks, activate TOR-repressed genes, allowing a rapid response to stress [33].
Whereas BRM promotes the maintenance of heat shock-induced epigenetic memory, DDM1 eliminates it [34][35]. This is evident from the longer persistence of the heat shock-induced transcriptional activation of heterochromatic loci in ddm1 single mutant and in the ddm1 mom1 double mutant when compared to the wild-type Arabidopsis. Of note, however, is the fact that heterochromatin hyperactivation status is transmitted to the progeny specifically in the ddm1 mom1 double mutant, but not in the single ddm1 mutant [35]. DDM1 also appeared to be involved in biotic stress response; together with another CRF member, SPLAYED (SYD), it represses the transcription of plant defense genes such as SUPPRESSOR OF npr1-1 CONSTITUTIVE1 (SNC1) during a bacterial pathogen attack [36].
DDM1, together with MORPHEUS’ MOLECULE 1 (MOM1), modulates transcriptional gene silencing via DNA methylation [35][37]. The importance of ddm1 for the control of DNA methylation is reflected by the fact that the ddm1 mutant shows up to 70% reduction in global genome methylation, predominantly at heterochromatic regions [38]. 
Consequently, this triggers the activation of transposons and retrotransposons, the transcriptional activation of a previously silent disease-resistance gene array, and profound phenotypic instability amplified with every generation of self-propagation. The fact that ddm1-induced hypomethylation of various genes can be stably inherited through mitotic and meiotic cell divisions might be one of the reasons of the phenotypic instability [39].
Additional data on the DDM1 function were obtained from studies in maize [40]. ZmDDM1 is critical for CHG methylation, and less so for CG methylation in the heterochromatic regions, and is also required for the formation of mCHH islands.
The mechanism of methylation loss in ddm1 plants is not entirely clear, but it is possible that DDM1 regulates DNA methylation status via changes in histone methylation, the interaction with Arabidopsis MBD proteins (AtMBDs), or the regulation of RdDM pathway. It has been shown that ddm1 exhibited a disrupted localization of AtMBDs at chromocenters, suggesting that DDM1 may facilitate the localization of MBDs at specific nuclear domains [41]. Recent papers have shed more light on the process. DDM1 appears to aid DNA methyltransferases in displacing the nucleosomes from the chromatin. It was recently found that DDM1 promotes the replacement of histone variant H3.3 by H3.1, which allows nucleosome displacement and DNA methylation to occur [42]. In ddm1 mutants, the loss of the H3.3 chaperone HIRA allows partially restoring DNA methylation, further indicating the role of both DDM1 and H3.3 in the process [42].
One of the possible mechanisms of the involvement of DDM1 in the control of DNA methylation is the maintenance of CpG methylation at RdDM-targeted sequences after the RNA signal is removed. ddm1 plants appear to be impaired in DNA repair and are sensitive to salt and methyl methane sulfonate (MMS) stress [43], likely due to the increased activity of transposons and retrotransposons and general dysregulation of heterochromatin.
Another SWI/SNF-like protein, DRD1, represents a novel plant-specific chromatin-remodeling factor that is required for the RNA-directed de novo methylation of target promoters [44]. It is also necessary for the total loss of de novo DNA methylation after the RNA silencing trigger is withdrawn. DRD1 interacts with two other factors, NRPD1b and NRPD2a, which represent subunits of a novel, plant-specific RNA polymerase, pol IVb. DRD1 and the pol IVb complex act downstream of the ncRNA biogenesis pathway. They direct reversible silencing of euchromatic promoters in response to RNA signals possibly through the recruitment of DNA methyltransferases for the methylation of homologous DNA sequences. It is noteworthy that among putative DRD1 targets, there are DNA glycosylases, ROS1 and DME, which are involved in active DNA demethylation. The down-regulation of ROS1 in drd1 and pol IVb mutants confirms the importance of the DRD1/pol IVb pathway for the active loss of induced de novo DNA methylation [45].

3.1.3. The Role of Chromatin-modifying Proteins Lacking ATPase Domain

Another potential chromatin remodeling factor playing a role in the regulation of silencing and the inheritance of heterochromatin hyperactivation states is the nuclear protein MOM1. Despite the fact that MOM1 is evolutionarily related to chromodomain helicase DNA binding protein3 (CHD3), a chromatin remodeling protein, MOM1 does not contain the functional ATPase/helicase domain [46].
It is involved in DNA methylation- and histone methylation-independent silencing of repetitive sequences in Arabidopsis by preventing the transcription of 180-bp satellite repeats and 106B dispersed repeats [47]. This suggests the existence of two distinct epigenetic silencing pathways: one that is DNA-methylation-dependent and another one that is DNA-methylation-independent. Although MOM1 is involved in chromatin remodeling, the mutant is not hypersensitive to the DNA damaging agent MMS. Other chromatin modifiers, such as BRUSHY1 (BRU1), FASCIATA (FAS1), FAS2, and Replication protein A 2 (RPA2), are also dispensable for DNA methylation, but all of them are hypersensitive to the MMS-induced DNA damage.
One of the first proteins implicated in the appearance of heat shock memory is the HEAT SHOCK TRANSCRIPTION FACTOR A2 (HSFA2) [48]. Besides its role in inducing the expression of genes that are on for 2-3 days in response to heat, HSFA2 also establishes the hyper-methylation of histone H3K4 at the loci associated with heat shock memory formation [49]. The FGT1 gene provides another link between heat stress memory and the organization of the chromatin; FGT1 protein is essential for the sustained induction of HSA32 and several other memory genes after heat stress [25]. FGT1 interacts with several CRFs and maintains low nucleosome occupancy throughout the heat stress memory phase [25].
Other reports also indicated the link between chromatin maintenance and stress response. Mutants of a nuclear protein BRU1, encoded by the BRUSHY1 (BRU1)/TONSOKU (TSK)/MGOUN3 (MGO3) gene, involved in the maintenance of chromatin structure and epigenetic inheritance of chromatin states, were highly sensitive to genotoxic stress and were characterized by an increased frequency of intrachromosomal homologous recombination [50]. Recent report suggests that in Arabidopsis, in response to heat stress, BRU1 is required to maintain a sustained induction of heat shock-induced memory-associated genes [51]. Curiously, BRU1 was dispensable for the increase in thermotolerance. Based on the data obtained using bru1 mutants, the authors proposed a model where BRU1 mediates the faithful inheritance of chromatin states after DNA replication and cell division.

3.2. The Role of Histone Modifications in the Response to Stress

Histone modifications play an important role in the response to stress and in the establishment and propagation of somatic stress memory [52][53][54][55][56].
In plants, transcriptionally active chromatin exhibits an enhancement of H3 and H4 acetylation and the trimethylation of lysine 4 from histone H3 (H3K4me3), whereas silent chromatin contains hypoacetylated H3 and H4, methylated lysine 27 (H3K27), and lysine 9 of histone H3 (H3K9) [57]. Histone acetyltransferases (HATs) and histone deacetylases (HDACs) modulate the expression of developmental and stress-sensitive genes.
There are many reports showing histone modifications in response to various stresses, so only some, including temperature, salinity, drought, and pathogen stresses, will be covered. For example, the deposition of active histone marks H3K9Ac and H3K4me3 on heat shock protein-encoding genes HSP18, HSP22.0, APX2, and HSP70 occurs in response to heat stress. Histone H3K4 methyltransferases SET DOMAIN PROTEIN 25 (SDG25) and ARABIDOPSIS HOMOLOG OF TRITHORAX 1 (ATX1) increase H3K4me3 and decrease DNA methylation at stress response genes during heat shock stress recovery [58].
Histone acetylation is enriched in the bodies of a number of cold-responsive genes, including COR15A and COR47 [59][60]. Also, ADA2b, an interacting partner of GCN5 acetyltransferase, is stimulated by cold-responsive transcription factor CBF1, resulting in H3 hyperacetylation at COR genes [61]. The role of deacetylases is not entirely clear, as they are implemented in regulating the cold stress response and acclimation in a positive and a negative manner. During cold exposure, CULLIN4-based ubiquitin E3 ligase complex degrades HD2C deacetylase and its partner HOS15, resulting in the increased level of histone acetylation at COR genes, leading to their expression [62].
Salt stress also triggers the accumulation of H3K9/K14Ac and H3K4me3 and reduction in H3K9me2 and H3K27me3 repressive marks on salt stress-responsive genes [63][64]. H3K9/K14 acetylation in Arabidopsis in response to salt activates cell wall biosynthesis gene acetyltransferase GCN5 and stress response gene chitinase-like (CTL) [65]. The body of the Arabidopsis HKT1 gene, encoding the Na+ transporter, is normally highly enriched in H3K27me3, and salt exposure results in the removal of H3K27me3 from the HKT1 body and the activation of its expression [20].
The accumulation of permissive chromatin marks H3K4me3 and H3K9Ac in the promoter or gene body of many drought responsive genes, including NCED3, GOLS2, RD20, RD29A, RD29B, RD22, and RAP2.4, results in an increase in the expression of these genes [66][67]; an abundance of H3K4me3 and H3K9Ac positively correlates with gene expression and drought tolerance [68]. Also, the severity of drought exposure positively correlates with an abundance of these histone marks [69].
The role of histone modifications is also well documented for pathogen response. HDACs, for example, have been implicated in defense against pathogens. The HC-toxin from Cochiobolus carbonum specifically targets HDAC activity, causing histone hyperacetylation in susceptible corn cultivars [70].
Histone deacetylases can also act as negative regulators of response to pathogens: TaHDT701 was shown to be a negative regulator of wheat defence responses to Blumeria graminis f.sp. tritici [71]; HDA9 negatively regulates the Arabidopsis response to pathogens by histone deacetylation at NLR genes [72].
Changes in histone phosphorylation, sumoylation, and ubiquitination in response to stress are less well documented. It was shown that H3S10ph accumulates in response to salt and cold stresses and the H3T3ph mark accumulates in pericentromeric regions in response to drought [73]. The monoubiquitination of H2B results in the activation of stress-associated genes in response to many abiotic and biotic factors [74][75]. FGT2 encodes a TYPE-2C PROTEIN PHOSPHATASE (PP2C) and can potentially dephosphorylate histones. Plants mutated in FGT2 have normal thermotolerance, but are impaired in the establishment of heat shock memory [76].

3.3. The Role of DNA Methylation in Response to Stress

DNA methylation is the most versatile mechanism involved in the regulation of gene expression, including the inheritance of specific gene expression patterns through somatic or meiotic cell divisions. The control of DNA methylation in plants is complex, with symmetrical CpG and CpHpG and non-symmetrical CpHpH methylation established and maintained through multiple, partially redundant mechanisms. De novo symmetrical methylation is established by the DOMAINS REARRANGED METHYLTRANSFERASE 2 (DRM2) with the help of ncRNAs of the RdDM pathway, while maintained by the METHYLTRANSFERASE 1 (MET1) in the CpG context and CMT2/CMT3 proteins in CpHpG context [77]. CMT3 is recruited to the repressive histone mark H3K9me2 [78], and, in turn, CMT3 binding to DNA can facilitate the recruitment of H3K9me2 [78].
Stress may result in both hypo- and hypermethylation at specific genomic loci, and these changes may represent either a short-term change or a long-term strategy of response to stress [79]. Promoters of stress-responsive genes are often found to be hypomethylated [80][81], whereas methylation at other genomic loci may not be altered and, sometimes, may even be increased [81].
Changes in DNA methylation in response to stress may occur due to many different mechanisms, including the activity of DNA methyltransferases; DNA demethylases such as ROS1, DME1, DML2, and DML3; a passive loss of methylation via the exclusion of DNA methyltransferases from the nucleus; changes in the activity of chromatin remodelling factors and effector proteins; and many other changes in proteins regulating the chromatin structure [77].
The importance of DNA methylation for the maintenance of gene expression patterns and genome stability is reflected by the fact that plants evolved a specific enzyme to excise methylated cytosines from DNA. ROS1 is a methylated cytosine-specific glycosylase that excises methylated cytosines through the process of base excision repair [82]. This enzyme is rather unique in plants, since it combines the function of a DNA repair enzyme with that of an active demethylating process. Curiously, in the ros1 mutant, the expression of several transposons was found to be decreased due to an increase in methylation levels at CpHpG and CpHpH sites [83]. Active DNA demethylation is, thus, important in pruning methylation marks in the genome, and even previously silent transposons need dynamic control by methylation and demethylation. Such control is required for the plant epigenome to efficiently respond to developmental and environmental cues.
The immediate stress response of plant somatic tissues results in changes in methylation of various areas of the genome, with genes involved in stress response being primarily hypomethylated [84]. Under salt stress, the stress-responsive genes, including those involved in the JA pathway, undergo rapid hypomethylation, leading to increased jasmonoyl isoleucine (JA-Ile) content and JA signaling to confer salt tolerance. Also, exposure to cold causes demethylation and transcriptional activation at many different loci in different species, including transcription factors, stress-response genes, and transposons [83][85].

3.4. Role of siRNAs and RdDM in Stress Response

RdDM is a versatile mechanism implemented in development and reproduction, such as the control of flowering, TE silencing, regulation of genome stability, cell-to-cell and systemic signalling, and response to stress [86]. RdDM resembles RNA interference mechanisms and involves small non-coding RNAs, Dicers, Argonautes, and RNA-dependent RNA polymerases. siRNAs involved in RdDM are commonly produced from transposable elements, viral RNAs, transgenes, and various endogenous transcripts. RdDM occurs through a concerted function of sequence-specific siRNAs, PolIV, DCL3, RDR6, DRM2, RDM4, and several other proteins. Two polymerases, Pol IV and Pol V, are involved in the RdDM pathway. Pol IV generates 26-50 nt Pol IV-dependent RNA precursors (P4-RNAs) that are then converted into double-stranded RNA (dsRNA) by RDR2, which are then processed by DICER-LIKE protein 3 (DCL3) into 24-nt siRNAs or in the absence of DCL3, by DCL1, DCL2, and DCL4 into shorter 21- or 22-nt siRNAs [87].
RdDM plays an essential role in the suppression of transposon activity in response to stress. For example, transposon ONSEN, while activated by heat stress, can only transpose if RdDM components are intact [88]. Moreover, the heat tolerance is decreased in several RdDM mutants; plants deficient in NRPD2, the subunit of RNA polymerases IV and V, are more sensitive to heat [89].
Some direct and indirect evidence exists demonstrating the role of RdDM in somatic stress memory and the formation of epialleles. The restoration of the function of NRPD1, a polIV subunit, results in the formation of two sets of loci, those that are remethylated after restoration, and those that are not [90]. The latter ones contain higher levels of the H3K4me3 euchromatic mark, which interferes with the recruitment of the RdDM machinery, and the H3K18ac mark, which attracts ROS1 to antagonize RdDM. Those loci that can be remethylated lack H3K4me3 and H3K18ac; CG/CHG methylation at these loci serves as a memory mark that is targeted by RdDM, aiding in the formation of stable epialleles.
Prolonged heat exposure reactivates repetitive elements silenced by posttranscriptional gene silencing (PTGS). The transcriptional activation of these loci increases the level of double-stranded RNA (dsRNA), which are one of the sources of siRNAs. The formation of dsRNA requires SUPPRESSOR OF GENE SILENCING 3 (SGS3) [91]. SGS3 activity is, in turn, regulated by temperature—a shift from 22 °C to 30 °C results in a decrease in SGS3 protein levels and, thus, in a decrease in the abundance of many trans-acting siRNAs (tasiRNAs) produced from dsRNAs. Induced by heat stress, HSFA2 transcriptionally activates the H3K27me3 demethylase RELATIVE OF EARLY FLOWERING 6 (REF6), which, in turn, further derepresses HSFA2, establishing a somatically heritable feedback loop; they activate an E3 ubiquitin ligase, SGS3-INTERACTING PROTEIN 1 (SGIP1), which leads to SGS3 degradation, the inhibition of tasiRNA biogenesis, and the formation and maintenance of somatic and transgenerational memory of heat stress [34].

3.5. Potential Role of Methylated RNA in Stress Response

RNA methylation is a common process, well-described in animals, but still poorly understood in plants [92]. Methylated adenine is most common (m6A), but cytosines (m3C) can also be methylated. Plants encode all classical writers, erasers, and readers of methylation. The importance of these proteins is shown by various phenotypic abnormalities, including altered growth [93][94] and the response to pathogens [95].
Thousands of genes were reported to be affected by RNA methylation [96]; this is especially common in organelles. Almost all chloroplast transcripts and 86–90% mitochondrial transcripts are methylated, suggesting a critical role of this process in the energy metabolism [97]. The methylation of ribosomal RNA in chloroplasts is crucial for chloroplast biogenesis, photosynthesis, and for a proper abscisic acid response [98].
The methylation of mRNA may alter its mobility. m5C-modified TCTP1 (TRANSLATIONALLY CONTROLLED TUMOR PROTEIN 1) was shown to be actively transported to roots and change root growth [99]. Methylated mRNAs can move long distances and, thus, could serve as developmental and stress response signals. In Arabidopsis, the mutation of m6A writers resulted in a sensitivity to salt stress that correlated with the level of m6A [100].

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Igor Kovalchuk
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