Submitted Successfully!
To reward your contribution, here is a gift for you: A free trial for our video production service.
Thank you for your contribution! You can also upload a video entry or images related to this topic.
Version Summary Created by Modification Content Size Created at Operation
1 -- 4363 2022-11-10 09:43:09 |
2 format correct Meta information modification 4363 2022-11-11 02:03:07 |

Video Upload Options

Do you have a full video?

Confirm

Are you sure to Delete?
Cite
If you have any further questions, please contact Encyclopedia Editorial Office.
Nguyen, N.H.;  Vu, N.T.;  Cheong, J. Stress Memory and Inheritance of Drought Tolerance. Encyclopedia. Available online: https://encyclopedia.pub/entry/33902 (accessed on 20 June 2024).
Nguyen NH,  Vu NT,  Cheong J. Stress Memory and Inheritance of Drought Tolerance. Encyclopedia. Available at: https://encyclopedia.pub/entry/33902. Accessed June 20, 2024.
Nguyen, Nguyen Hoai, Nam Tuan Vu, Jong-Joo Cheong. "Stress Memory and Inheritance of Drought Tolerance" Encyclopedia, https://encyclopedia.pub/entry/33902 (accessed June 20, 2024).
Nguyen, N.H.,  Vu, N.T., & Cheong, J. (2022, November 10). Stress Memory and Inheritance of Drought Tolerance. In Encyclopedia. https://encyclopedia.pub/entry/33902
Nguyen, Nguyen Hoai, et al. "Stress Memory and Inheritance of Drought Tolerance." Encyclopedia. Web. 10 November, 2022.
Stress Memory and Inheritance of Drought Tolerance
Edit

Plants respond to drought stress by producing abscisic acid, a chemical messenger that regulates gene expression and thereby expedites various physiological and cellular processes including the stomatal operation to mitigate stress and promote tolerance. To trigger or suppress gene transcription under drought stress conditions, the surrounding chromatin architecture must be converted between a repressive and active state by epigenetic remodeling, which is achieved by the dynamic interplay among DNA methylation, histone modifications, loop formation, and non-coding RNA generation. Plants can memorize chromatin status under drought conditions to enable them to deal with recurrent stress. Furthermore, drought tolerance acquired during plant growth can be transmitted to the next generation. The epigenetically modified chromatin architectures of memory genes under stressful conditions can be transmitted to newly developed cells by mitotic cell division, and to germline cells of offspring by overcoming the restraints on meiosis.

drought tolerance chromatin remodeling chromatin loop non-coding RNA stress memory transgenerational inheritance

1. Introduction

The global climate crisis is reducing rainfall, resulting in long periods of dry weather and repeated droughts that seriously threaten crop productivity and the food supply. Plants are unable to escape from adverse environments and thus deal with stressful conditions by regulating the expression of tolerance genes to induce physiological and cellular responses [1][2][3]. Under drought conditions, plants upregulate the level of endogenous abscisic acid (ABA), which is a major plant hormone in the cellular tolerance response to osmotic stress [4]. ABA induces the closure of stomatal apertures on the leaf epidermis, to limit transpiration and thereby prevent the loss of water [5]. In addition, ABA induces the expression of numerous genes encoding enzymes that catalyze the biosynthesis of osmoprotectants, which mitigate stress and promote plant tolerance [6][7].
To initiate gene transcription, the surrounding chromatin must be converted from a repressive to an active state to enable access by transcriptional activators and RNA polymerases [8]. In the chromatin of eukaryotic cells, genomic DNA is compacted into the nucleus by wrapping around histone octamers. Chromatin architecture is epigenetically altered by remodeling through DNA (de)methylation, alterations in nucleosome density and composition, and histone modification, which take place at the promoter, the transcription start site (TSS), and gene-body regions [9][10]. In addition, in response to environmental signals or developmental cues, non-coding RNAs (ncRNAs) are generated from intergenic regions, repetitive sequences, transposons (TEs), and pseudogenes, and interact with their targets to inhibit gene expression at the transcriptional, posttranscriptional, and epigenetic levels by promoting mRNA cleavage or repressing translation [11].
Plants pre-exposed to stress often grow better under subsequent stressful conditions [12][13][14]. This phenomenon has been referred to as stress memory, priming, training, acclimation, and imprinting [15][16][17]. During and after stress, defense signaling metabolites and transcription factors accumulate in plant tissues and may play a role in transient or short-term memory. However, the most plausible mechanism involves epigenetic changes in the chromatin architecture of certain stress-responsive genes called ‘stress memory genes’ that are expressed at highly elevated or reduced levels in response to repeated stress [18][19][20][21]. Lämke and Bäurle [21] defined the sustained differential responses in gene expression (activation or repression) after an exogenous cue with the term ‘transcriptional memory’. An epigenetically modified status acquired during stress can be transmitted to newly developed cells during mitotic cell division [22][23]. Thus, the chromatin architecture constituted by epigenetic marks under initially stressful conditions may pass through the cell division process without alteration, thereby providing mitotic memory [24][25].
Stress memory whose duration is limited to one generation of organisms was termed as ‘somatic stress memory’ [21]. Furthermore, plants can transmit traits acquired during growth to their progenies (transgenerational inheritance) [21][26][27]. In mammalian cells, the acquired memory is completely erased and reset during meiosis. The mechanism by which plant cells overcome this resetting during meiosis and transmit the stress memory to progenies is unclear.
The memory and transgenerational inheritance of stress tolerance have been explored in the context of crop breeding and yield stability [28][29][30]. However, the adoption of tolerance priming (e.g., pre-treatment with stressful conditions) and inheritance technologies has been hampered by an insufficient understanding of their principles. Understanding the molecular mechanisms underlying stress memory and transgenerational inheritance would facilitate the breeding of crops to better be able to withstand adverse climatic conditions.

2. Transcription of Drought-Responsive Genes

2.1. Drought-Responsive Genes

More than half of the genes up- or downregulated under drought or high-salinity conditions are also regulated by ABA application, suggesting that the expression of osmotic stress-responsive genes is driven mainly by ABA [6][7][31]. ABA induces the expression of numerous genes encoding enzymes that catalyze the biosynthesis of osmoprotectants such as trehalose and late embryogenesis-abundant proteins. In addition, ABA-induced genes include those encoding proteins exerting either positive or negative effects on its accumulation (biosynthesis, catabolism, and glucose-conjugation), transportation, and signaling network [32]. By analyzing the promoters of ABA-responsive genes, a conserved cis-acting ABA-responsive element (ABRE; PyACGTGG/TC) was identified [33]. Subsequently, several ABRE-binding (AREB) proteins and ABRE-binding factors (ABFs) were identified by yeast one-hybrid screening [34][35].
However, a few drought-inducible genes do not respond to ABA, implying that ABA-independent pathways regulate the drought response [36]. The promoters of these genes contain the cis-acting element DRE (dehydration-responsive element)/CRT (C-repeat), which functions in ABA-independent gene expression [33]. The ERF/AP2 family transcription factors CBF/DREB1 (C-repeat-binding factor/DRE binding 1) and DREB2, which bind to DRE/CRT elements, were identified in plants [33]. Most CBF/DREB1 target genes in Arabidopsis (Arabidopsis thaliana) contain the DRE motif with a conserved (A/G)CCGACNT sequence in their promoter regions. Rice (Oryza sativa) genome sequence analyses identified 10 OsDREB1s and 4 OsDREB2s, indicating that similar transcription factors function in drought stress tolerance in dicotyledonous and monocotyledonous plants. The Arabidopsis RD29A (responsive to desiccation 29A) contains both cis-acting elements, ABRE and DRE/CRT, in the promoter region.

2.2. Regulation of ABA Signaling

The ABA de novo synthesis pathway has been unraveled [4][37]. ABA is biosynthesized in vascular tissues and transported to targets including guard cells via the export and import of transporters. In Arabidopsis, three transporter families have been identified: ATP binding cassette (ABC), detoxification efflux carriers (DTX)/multidrug and toxic compound extrusion (MATE) proteins, and nitrate transporter 1/peptide transporter family (NPF) [32][38][39][40]. For instance, ABCG25 exports ABA to the apoplastic space in vascular tissues, while ABCG40 and NPF4.6 import ABA into guard cells in response to osmotic stress.
In target cells, ABA is perceived by soluble receptors in the nucleus and cytosol. Several synonymous ABA receptors, i.e., PYR (pyrabactin resistance), PYL (PYR-related), and RCAR (regulatory component of the ABA receptor), have been identified in Arabidopsis [41][42]. In the absence of ABA under non-stressful conditions, clade A type 2C protein phosphatases (PP2Cs) in guard cells counteract a family of protein kinases, known as sucrose non-fermenting 1-related protein kinase 2s (SnRK2s) via physical interactions, thus providing negative feedback regulation of ABA signaling [43][44] (Figure 1A). Under osmotic stress, following ABA perception, PP2Cs bind to ABA receptors to capture ABA and form the PYL-ABA-PP2C complex; SnRK2s subsequently dissociate from inactivated PP2Cs to restore kinase activity [45] (Figure 1B).
Figure 1. Signaling pathway for the expression of abscisic acid (ABA)-responsive genes. (A) Repression of ABA-responsive genes. In the absence of ABA, clade A protein phosphatases (PP2Cs) physically interact with sucrose non-fermenting 1-related protein kinase 2s (SnRK2s) to reduce kinase activity via dephosphorylation. This results in the inhibition of ABRE-binding (AREB)/ABRE-binding factors (ABFs) and the suppression of ABA-responsive gene transcription. (B) The activation of ABA-responsive gene expression. Under drought stress, soluble ABA receptors (Pyrabactin resistance/PYR-related/regulatory component of the ABA receptors [PYR/PYL/RCARs]) and PP2Cs act as co-receptors to capture ABA, thereby blocking the phosphatase activity of PP2Cs. PP2Cs are released from PP2C-SnRK2 complexes, and free SnRK2s phosphorylate downstream transcription factors (AREBs/ABFs). The phosphorylated AREBs/ABFs trigger the transcription of numerous ABA-responsive genes, leading to ABA responses including stomatal closure.
Activated SnRK2s in the cytosol facilitate the functioning of slow anion channel 1 (SLAC1), K+ channel 1 (KAT1), and NADPH oxidases in the guard cell membrane to induce stomatal closure [32][46]. In the nucleus, under osmotic stress, activated SnRK2s phosphorylate and activate a family of basic-domain leucine zipper (bZIP) transcription factors, the AREB/ABFs, thereby inducing the expression of numerous ABA-responsive genes [47]. Among the nine AREB/ABFs in Arabidopsis, ABF1, AREB1/ABF2, AREB2/ABF4, and ABF3 act as master transcription factors in ABA signaling to promote osmotic stress tolerance [48].

3. Transcriptional Memory of Drought Tolerance

3.1. Drought Stress Memory

Plants memorize the tolerance induced by drought stress to respond more effectively to subsequent stresses [13][49][50]. For instance, Walter et al. [51] observed that after a late drought during the growth of perennial grass (Arrhenatherum elatius), the percentage of living biomass was increased in plants exposed to earlier drought compared to those without such exposure, even after harvest and resprouting after the first drought. Ding et al. [52] reported that Arabidopsis with experience of dehydration stress wilted more slowly than plants without such experience in response to subsequent dehydration events. Wang et al. [53] showed that wheat plants subjected to one or two drought episodes before anthesis had higher grain yields under drought conditions. Ramírez et al. [54] reported that long-term stress improved drought tolerance-related traits and tuber yield in later growth stages in potato plants. Abdallah et al. [55] showed that the pre-exposure to a drought-sensitive variety of olive plants to drought enhanced their tolerance to subsequent drought conditions, resulting in improvements in biomass production, photosynthesis, and the maintenance of water status. Tabassum et al. [56] also reported that terminal drought and seed priming improved the drought tolerance of wheat plants.
Goh et al. [57] observed that Arabidopsis exhibited memory functions related to repeated ABA stresses, i.e., the impairment of light-induced stomatal opening and the induction of the expression of drought-responsive genes. Virlouvet and Fromm [58] reported that Arabidopsis stomatal apertures closed following exposure to dehydration remained partially closed during a recovery period with access to water, thereby facilitating reduced transpiration during subsequent dehydration stress. In mutant plants defective in the ABA signaling pathway, the guard cell stomatal memory was ABA-dependent, and SnRK2s were essential for implementing stress memory during the subsequent dehydration response. Li et al. [59] performed whole-transcriptome, strand-specific RNA sequencing (ssRNA-seq) of the rice genome, and the results suggested that lncRNAs, DNA methylation, and endogenous ABA mediate drought memory by activating the drought-responsive transcription of genes in pathways such as photosynthesis and proline biosynthesis in response to subsequent drought conditions.

3.2. Drought Stress Memory Genes

In response to drought stress, plants induce or suppress the expression of many drought-responsive genes [1][2]. In most cases, up- or downregulated gene transcripts return to basal levels during recovery (watered) states. However, a subset of genes is expressed at highly elevated or reduced levels in response to repeated drought stresses, which enables the plant to respond more promptly and strongly [13][16][52]. Ding et al. [60] defined stress memory genes as those that enable responses during subsequent stress conditions that differ from the responses during the initial stress encounter, whereas genes that respond similarly to each stress are categorized as non-memory genes. However, the expression threshold for classification into one or the other category is unclear.
Numerous drought stress memory genes have been identified in plants. Ding et al. [60] used a genome-wide RNA sequencing (RNA-seq) approach to evaluate the transcriptional responses of Arabidopsis leaves detached from plants repeatedly exposed to air-drying. Genes implicated in the responses to ABA, drought, salinity, and cold/heat acclimation constituted the drought-induced memory genes, and those responsible for chloroplast and thylakoid membrane-associated functions comprised the dehydration-repressed memory genes. Kim et al. [61] performed a microarray analysis to screen drought stress memory genes in soybean. The soybean memory genes exhibiting significantly elevated transcript levels upon the second exposure to drought stress conditions include those involved in ABA-mediated tolerance responses to abiotic stresses, such as genes encoding transcription factors, trehalose biosynthesis enzymes, late embryogenesis abundant proteins, and PP2C family proteins. By contrast, memory genes with highly reduced transcript levels during the second drought included genes involved in photosynthesis and primary metabolism. Soybean drought stress memory genes included genes involved in the dehydration memory responses of Arabidopsis. However, studies of other crop plants identified species-specific drought memory genes. A genome-wide RNA-seq analysis of maize identified only 4 chloroplast- and 2 thylakoid membrane-localized genes acting as drought-repressed memory genes [62], compared to 128 Arabidopsis drought-repressed memory genes [60]. In potato, the expression levels of most photosynthesis-related genes during a second drought were higher than during the first drought [63]. In addition, most rice memory transcripts associated with photosynthesis were markedly reduced by a first drought but then recovered, remaining at a stable level during subsequent drought treatments [59].
Several memory genes encode various transcription factors in all of the plant species described above. In Arabidopsis, dehydration-induced transcriptional memory behavior was seen in members of the AP2/ERF, bHLH, homeo_ZIP, MYB, ZF, b_ZIP, CCAAT, and WRKY transcription factor families [60]. Similarly, in soybean, various transcription factor genes belonging to the AP2, NAM, MYB, bZIP_1, and WRKY families were identified as drought-induced memory genes [61]. Therefore, transcription factors with memory function may contribute to plant memory and regulate the expression of their targets upon repeated stress. This possibility should be addressed in further studies of the mechanisms of drought stress memory.

3.3. Mechanism of Transcriptional Stress Memory

3.3.1. Epigenetic Marks for Stress Memory

Epigenetic chromatin remodeling is a plausible molecular mechanism of transcriptional stress memory [12][22][23][50]. It has been proposed that chromatin architecture (DNA methylation, histone modification, and chromatin loops) maintains the altered gene expression patterns caused by an initial stressor. Transcription factors and chromatin loops may also be associated with a subset of their targets during mitosis. The role of the chromatin remodeler BRM in stress memory under heat-shock stress has been investigated. Brzezinka et al. [64] reported that Arabidopsis brm mutants were deficient in heat-shock memory and showed the reduced induction of heat-shock memory genes. BRM and the FORGETTER1 (FGT1) factor physically interact and are pre-associated with memory genes under non-stress conditions. fgt1 mutants displayed more rapid recovery of nucleosome occupancy at heat-shock memory gene loci, suggesting that the BRM-FGT1 interaction prevents nucleosome recovery at these loci and mediates heat stress-induced memory.
Changes in DNA methylation may be involved in the transcriptional memory of plant responses to abiotic stresses [65]. Wang et al. [66] observed that around 29% of drought-induced DNA (de)methylation sites remained after recovery from drought or salt stress, implying that the DNA methylation changes were recorded. Kou et al. [67] performed a genome-wide rice methylome profiling analysis under recurrent drought stresses and recovery treatments. Most drought-stress memory-related DMRs were targeted TEs and few were targeted gene bodies, which suggests that they regulate TE expression to cope with recurrent drought stress. The distances from memory DMRs to TEs were significantly shorter than those from non-memory DMRs, implicating DNA methylation in drought memory formation.
Histone modification may provide a persistent epigenetic transmission mechanism associated with transcriptional memory in response to osmotic stress [18][20][21]. For instance, H3K27me3 is a gene silencing mark related to the chromatin-induced repression of gene expression and the formation of an epigenetic memory system during development [68]. In eukaryotes, the H3K27 methylation level is regulated by the action of polycomb group (PcG) protein complexes. Polycomb-repressive complex 2 (PRC2) mediates the deposition of H3K27me2/3 by the enzymatic subunit PRC2-Ezh2 (enhancer of ZESTE 2), whereas PRC2-Ezh1 restores H3K27me2/3 via its demethylase activity or histone exchange [69]. Ezh1 and Ezh2 exhibit different expression patterns and distinct chromatin-binding properties [70]. H3K27me3 in target genes recruits an additional PcG protein complex, PRC1. PRC1 complexes are subdivided into canonical PRC1 and noncanonical (or variant) PRC1. Canonical PRC1 is recruited by H3K27me3 readers and compacts nucleosomes to repress gene expression, while noncanonical PRC1 is recruited to chromatin independently of PRC2 and H3K27me3, and ubiquitylates histone H2A (to form H2AK119ub) via its H2A E3 ubiquitin ligase activity [71][72]. Thus, PcG complexes provide the major chromatin regulatory mechanism for silencing unnecessary or unwanted gene expression in mammals and plants [73][74].
PcG genes were discovered in Drosophila (Drosophila melanogaster), and homologs of PcG components and their target genes have been identified in other eukaryotes including plants [75][76][77][78]. The role of the PRC2-mediated deposition of H3K27me3 has been studied in the context of developmental processes and environmental stress responses in plant model species including Arabidopsis [74][79][80][81]. The PRC1-like protein LHP1 (like heterochromatin protein-1) was also identified in Arabidopsis [68][82][83]. Ramirez-Prado et al. [84] showed that the loss of LHP1 induces ABA sensitivity and drought tolerance, indicating that LHP1 regulates the expression of stress-responsive genes. The H3K27me3 level was not related to H3K4me3 accumulation, suggesting that these histone modification marks function independently and do not have mutual effects on the expression of dehydration stress memory genes.
H3K4me3 deposition may play a role in the epigenetic transmission of active transcriptional states [19]. H3K4me3 deposition and the amount of Pol II stalled in memory genes were higher than in non-memory genes in Arabidopsis after multiple dehydration stresses [52][85][86]. Kim et al. [87] observed H3K4me3 and H3K9ac deposition in drought-inducible genes (RD20, RD29A, and AtGOLS2) in response to drought. During recovery by rehydration, H3K9ac was rapidly removed, whereas H3K4me3 was maintained at a low level, implying that H3K4me3 functions as an epigenetic mark of stress. Ding et al. [52] observed that H3K4me3 deposition in trainable genes (RD29B and RAB18) was maintained during recovery from stress-induced transcription but decreased to a basal level in non-trainable genes (RD29A and COR15A). Thus, H3K4me3 and Pol II were induced in several dehydration stress memory genes in response to the first dehydration stress event, persisted during the recovery period, and increased greatly due to a second stress event.
As identified in Drosophila, the epigenetic transmission of active transcriptional states is supposed to be mediated by TrxG (trithorax group) complexes: the SWI/SNF complex and the COMPASS (complex of proteins associated with Set1) family [88][89]. Antagonistic links were identified between PcG genes and SWI/SNF, and COMPASS was associated with histone methyltransferase activity leading to the H3K4me3 deposition. In Arabidopsis, multiple TrxG factors have been identified, based on their ability to suppress PcG mutant phenotypes [90]. Plant TrxG factors regulate gene transcription in seedling growth, anther and ovule formation, gametophyte development, and reprogramming during developmental transitions [91][92][93][94].
However, it is not clear whether H3K4me3 in chromatin contributes to transcriptional activation under subsequent stress conditions. Genome-wide transcript profiling revealed that the transcription of most genes is unaffected by the loss of the histone methyltransferase activity of ATX1 (Arabidopsis homolog of TRITHORAX 1) and that H3K4me3 is required for efficient elongation of the transcription, but not the initiation, of ATX1-regulated genes [95][96]. Howe et al. [97] proposed that H3K4me3 deposition in chromatin is a consequence of transcription, influencing splicing, transcription termination, the memory of previous states, and transcriptional consistency, rather than inducing gene transcription in response to repeated stresses. Moreover, the mechanism of TrxG recruitment to the chromatin during mitosis is not clearly elucidated.

4. Transgenerational Inheritance of Memory

4.1. Transgenerational Transmission of Drought Tolerance

Traits acquired under stressful conditions can be transmitted to plant progeny [29][30][98]. The progeny of parents exposed to stress exhibits a higher yield than the progeny of non-stressed parents. Lämke and Bäurle [21] use the term ‘intergenerational memory’ when only the first stress-free generation has a detectable memory effect. As the progeny develops on the mother plant, intergenerational memory may be mediated by the conditions in which the seed grows and by cues introduced into the seed or embryo by the mother plant. In ‘transgenerational memory’, by contrast, memory is detectable after at least two stress-free generations. Verkest et al. [99] improved drought tolerance in canola (Brassica napus) by repeatedly selecting lines exhibiting increased drought tolerance for three generations. Tabassum et al. [100] reported that the hydro- and osmo-priming of bread wheat seeds caused the transgenerational transmission of improved tolerance to drought and salt stresses. Raju et al. [101] applied RNAi suppression to modulate abiotic stress-response pathways in soybean and developed an epigenetic breeding system for increased yield and stability.
Transgenerational memory may have an epigenetic basis [21]. Based on invertebrate developmental processes, it has been suggested that histones and other core chromatin components survive the passage of replication forks during meiosis [102][103][104]. Zenk et al. [105] showed that H3K27me3 was transgenerationally inherited from the maternal germline and resisted reprogramming events, thereby regulating the activation of enhancers and lineage-specific genes during early embryogenesis in Drosophila. Molla-Herman et al. [106] proposed that chromatin modifiers and Piwi-interacting small RNAs (piRNAs) function in adaptive and inheritable epigenetic memory events that occur in Drosophila during embryogenesis. Weiser and Kim [107] revealed an important role of endogenous siRNAs and piRNAs in transgenerational epigenetic inheritance in Caenorhabditis elegans. Those sRNAs may regulate heritable chromatin marks conveying epigenetic memory and thereby repress deleterious transcripts, such as TEs and repetitive elements. However, the relevance of these mechanisms to plant transgenerational inheritance of drought stress tolerance is unclear.

4.2. DNA Methylation for Transgenerational Inheritance

DNA methylation may contribute to transgenerational memory in plants [65]. Zheng et al. [108] reported that a high proportion of multigenerational drought-induced alterations in DNA methylation status are maintained in subsequent generations, possibly improving drought adaptability in rice. Drought stress-induced non-random epimutations over 11 successive generations improved the drought adaptability of rice epimutation lines. A large proportion (~45%) of the altered DNA methylation states were transmitted to unstressed progeny in subsequent generations. The epimutated genes participated in stress-responsive pathways, suggesting that they promote progeny adaptation to drought stress. Mathieu et al. [109] observed that the Arabidopsis mutant methyltransferase 1-3 (met 1-3), which is deficient in terms of maintaining CG methylation, formed progressively more aberrant epigenetic patterns over several generations, suggesting that CG methylation is a central coordinator of epigenetic memory that secures stable transgenerational inheritance. Zhang et al. [110] reported that many epigenetic recombinant inbred lines of Arabidopsis were nearly isogenic as a result of drought but were highly variable at the level of DNA methylation. Cortijo et al. [111] identified several DMRs that act as epigenetic quantitative trait loci and account for 60–90% of the heritability related to flowering time and primary root length in Arabidopsis. However, the contributions of locus-specific methylation changes to the maintenance of stress memory and whether the inheritance of drought stress tolerance is mediated only by DMRs require further investigation.
Matzke and Mosher [112] proposed that RdDM contributes to the transmission of DNA methylation patterns in parental cells to their offspring by affecting germ-cell specification and parent-specific gene expression. Morgado et al. [113] observed that the composition of sRNAs in apomictic dandelion (Taraxacum officinale) lineages indicated a footprint of drought stress experienced two generations prior. Kuhlmann et al. [114] reported that the methylation of the reporter gene ProNOS was not completely erased in DRM-2 (domains rearranged methyltransferase 2) mutants but persisted in the context of symmetric CG. ProNOS DNA methylation maintenance was evident after two generations of ongoing RdDM and increased in subsequent generations. They suggested that the methylation of a particular genomic region can be consolidated by RdDM and maintained over generations in Arabidopsis, thereby establishing epigenetic transgenerational memory. Wibowo et al. [115] suggested that epigenetic inheritance relies on DNA methylation changes at sequences that function as distantly acting control elements of key stress-response regulators, including antisense lncRNAs. Some of these changes are associated with conditionally heritable adaptive phenotypic stress responses and transmitted to the offspring, where they affect the transcriptional regulation of a small group of genes associated with enhanced tolerance to environmental stresses.
By contrast, two studies of Arabidopsis yielded conflicting results. In Arabidopsis subjected to slow-onset water deprivation treatment, Ganguly et al. [116] observed far fewer conserved DMRs in drought-exposed lineages compared to non-exposed lineages. Most of the variation was attributed to preexisting differences in the epigenome at repetitive regions of the genome. Thus, transgenerational memory may not be associated with changes in the DNA methylome. Van Dooren et al. [117] found that descendants of stressed and non-stressed Arabidopsis plants were phenotypically indistinguishable after an intervening generation without stress, irrespective of whether they were grown under normal or water-deficit conditions. In addition, although mild drought induced changes in the DNA methylome of exposed plants, these were not inherited by the next generation. Therefore, whether stress-induced DNA methylation variation transmits drought stress memory to the next generation is unclear.

4.3. Overcoming Meiosis

In mammals, paternal chromatin is extensively reprogrammed via the global erasure of DNA methylation achieved through extensive DNA demethylation and the packaging by exchange of histones with protamines [118][119]; this hampers the inheritance of stress-induced changes in chromatin architecture. Thus, epigenetic marks are reprogrammed in the gametes and the genomic potential is thus reset in the next generation. In contrast to mammals, DNA methylation in flowering plants is not completely erased from the germlines and is thus maintained during reproduction [120][121][122]. Wibowo et al. [115] reported that hyperosmotic stress memory in Arabidopsis restricts DME activity in the male germline. Moreover, protamine exchange does not occur in Arabidopsis, enabling the retention of histone-based chromatin in sperm [123]. However, Borg et al. [124] found that H3K27me3 is completely lost from histone-based sperm chromatin in Arabidopsis by the concerted action of three mechanisms; (1) the loss of histone methyltransferase activity in PRC2 to write H3K27me3, (2) the erasing activity of H3K27 demethylases, and (3) the deposition of the sperm-specific histone variant H3.10 which may be resistant to H3K27 methylation. The loss of H3K27me3 facilitates the transcription of genes essential for spermatogenesis but resets epigenetic memory in plant paternal chromatin.
Based on the above observations, newly acquired stress tolerance and associated epigenetic marks might be preferentially transmitted through the female germline. In Arabidopsis, Borg et al. [124] detected H3K27me3 in the microspore and in the daughter nuclei following microspore division, suggesting inheritance via meiosis. Inoue et al. [125] identified maternal H3K27me3 as a DNA methylation-independent imprinting mechanism in mouse (Mus musculus) embryonic cell lineage. Grossniklaus and Paro [126] reported that no major loss of H3K27me3 is expected on maternal alleles because PRC2 is active in the central cell. PcG complexes deposit or bind to certain histone modifications (e.g., H3K27me3 and H2AK119ub1) to prevent gene activation and maintain the repression of chromatin domains, which are implicated in plant vernalization and seed development. The relevance to plant drought stress tolerance mechanisms identified in flowering warrants further investigation.

References

  1. Shinozaki, K.; Yamaguchi-Shinozaki, K. Molecular responses to drought and cold stress. Curr. Opin. Biotechnol. 1996, 7, 161–167.
  2. Shanker, A.K.; Maheswari, M.; Yadav, S.K.; Desai, S.; Bhanu, D.; Attal, N.B.; Venkateswarlu, B. Drought stress responses in crops. Funct. Integr. Genom. 2014, 14, 11–22.
  3. Gupta, A.; Rico-Medina, A.; Caño-Delgado, A.I. The physiology of plant responses to drought. Science 2020, 368, 266–269.
  4. Nambara, E.; Marion-Poll, A. Abscisic acid biosynthesis and catabolism. Annu. Rev. Plant Biol. 2005, 56, 165–185.
  5. Bharath, P.; Gahir, S.; Raghavendra, A.S. Abscisic acid-induced stomatal closure: An important component of plant defense against abiotic and biotic stress. Front. Plant Sci. 2021, 12, 615114.
  6. Seki, M.; Ishida, J.; Narusaka, M.; Fujita, M.; Nanjo, T.; Umezawa, T.; Kamiya, A.; Nakajima, M.; Enju, A.; Sakurai, T.; et al. Monitoring the expression pattern of around 7000 Arabidopsis genes under ABA treatments using a full-length cDNA microarray. Funct. Integr. Genom. 2002, 2, 282–291.
  7. Hoth, S.; Morgante, M.; Sanchez, J.-P.; Hanafey, M.K.; Tingey, S.V.; Chua, N.H. Genome-wide gene expression profiling in Arabidopsis thaliana reveals new targets of abscisic acid and largely impaired gene regulation in the abi1-1 mutant. J. Cell Sci. 2002, 115, 4891–4900.
  8. Cairns, B.R. The logic of chromatin architecture and remodeling at promoters. Nature 2009, 461, 193–198.
  9. Yamamuro, C.; Zhu, J.-K.; Yang, Z. Epigenetic modifications and plant hormone action. Mol. Plant 2016, 9, 57–70.
  10. Kim, J.-H. Multifaceted chromatin structure and transcription changes in plant stress response. Int. J. Mol. Sci. 2021, 22, 2013.
  11. Ma, X.; Zhao, F.; Zhou, B. The characters of non-coding RNAs and their biological roles in plant development and abiotic stress response. Int. J. Mol. Sci. 2022, 23, 4124.
  12. Bruce, T.J.A.; Matthes, M.C.; Napier, J.A.; Pickett, J.A. Stressful “memories” of plants: Evidence and possible mechanisms. Plant Sci. 2007, 173, 603–608.
  13. Godwin, J.; Farrona, S. Plant epigenetic stress memory induced by drought: A physiological and molecular perspective. Methods Mol. Biol. 2020, 2093, 243–259.
  14. Choudhary, M.; Singh, A.; Rakshit, S. Coping with low moisture stress: Remembering and responding. Physiol. Plant. 2021, 172, 1162–1169.
  15. Conrath, U. Molecular aspects of defence priming. Trends Plant Sci. 2011, 16, 524–531.
  16. Kinoshita, T.; Seki, M. Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol. 2014, 55, 1859–1863.
  17. Marthandan, V.; Geetha, R.; Kumutha, K.; Renganathan, V.G.; Karthikeyan, A.; Ramalingam, J. Seed priming: A feasible strategy to enhance drought tolerance in crop plants. Int. J. Mol. Sci. 2020, 21, 8258.
  18. Luo, M.; Liu, X.; Singh, P.; Cui, Y.; Zimmerli, L.; Wu, K. Chromatin modifications and remodeling in plant abiotic stress responses. Biochim. Biophys. Acta 2012, 1819, 129–136.
  19. Kim, J.-M.; Sasaki, T.; Ueda, M.; Sako, K.; Seki, M. Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Front. Plant Sci. 2015, 8, 114.
  20. Avramova, Z. Transcriptional ‘memory’ of a stress: Transient chromatin and memory (epigenetic) marks at stress-response genes. Plant J. 2015, 83, 149–159.
  21. Lämke, J.; Bäurle, I. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol. 2017, 18, 124.
  22. Crisp, P.; Ganguly, D.; Eichten, S.R.; Borevitz, J.O.; Pogson, B.J. Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics. Sci. Adv. 2016, 2, e1501340.
  23. Sharma, M.; Kumar, P.; Verma, V.; Sharma, R.; Bhargava, B.; Irfan, M. Understanding plant stress memory response for abiotic stress resilience: Molecular insights and prospects. Plant Physiol. Biochem. 2022, 179, 10–24.
  24. Naumova, N.; Imakaev, M.; Fudenberg, G.; Zhan, Y.; Lajoie, B.R.; Mirny, L.A.; Dekker, J. Organization of the mitotic chromosome. Science 2013, 342, 948–953.
  25. Wang, F.; Higgins, J.M. Histone modifications and mitosis: Countermarks, landmarks, and bookmarks. Trends Cell Biol. 2013, 23, 175–184.
  26. Molinier, J.; Ries, G.; Zipfel, C.; Hohn, B. Transgeneration memory of stress in plants. Nature 2006, 442, 1046–1049.
  27. Quadrana, L.; Colot, V. Plant transgenerational epigenetics. Annu. Rev. Genet. 2016, 50, 467–491.
  28. Springer, N.M. Epigenetics and crop improvement. Trends Genet. 2013, 29, 241–247.
  29. Mickelbart, M.V.; Hasegawa, P.M.; Bailey-Serres, J. Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nat. Rev. Genet. 2015, 16, 237–251.
  30. Bilichak, A.; Kovalchuk, I. Transgenerational response to stress in plants and its application for breeding. J. Exp. Bot. 2016, 67, 2081–2092.
  31. Todaka, D.; Takahashi, F.; Yamaguchi-Shinozaki, K.; Shinozaki, K. ABA-responsive gene expression in response to drought stress: Cellular regulation and long-distance signaling. Adv. Bot. Res. 2019, 92, 83–113.
  32. Cheong, J.-J. Modulation of abscisic acid signaling for stomatal operation under salt stress conditions. Adv. Bot. Res. 2022, 103, 89–121.
  33. Yamaguchi-Shinozaki, K.; Shinozaki, K. Organization of cis-acting regulatory elements in osmotic- and cold-stress-responsive promoters. Trends Plant Sci. 2005, 10, 88–94.
  34. Choi, H.; Hong, J.; Ha, J.; Kang, J.; Kim, S.Y. ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 2000, 275, 1723–1730.
  35. Uno, Y.; Furihata, T.; Abe, H.; Yoshida, R.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl Acad. Sci. USA 2000, 97, 11632–11637.
  36. Shinozaki, K.; Yamaguchi-Shinozaki, K. Gene networks involved in drought stress response and tolerance. J. Exp. Bot. 2007, 58, 221–227.
  37. Cutler, A.; Krochko, J. Formation and breakdown of ABA. Trends Plant Sci. 1999, 4, 472–478.
  38. Merilo, E.; Jalakas, P.; Laanemets, K.; Mohammadi, O.; Hõrak, H.; Kollist, H.; Brosché, M. Abscisic acid transport and homeostasis in the context of stomatal regulation. Mol. Plant 2015, 8, 1321–1333.
  39. Kuromori, T.; Seo, M.; Shinozaki, K. ABA transport and plant water stress responses. Trends Plant Sci. 2018, 23, 513–522.
  40. Seo, M.; Marion-Poll, A. Abscisic acid metabolism and transport. Adv. Bot. Res. 2019, 92, 1–49.
  41. Gonzalez-Guzman, M.; Pizzio, G.A.; Antoni, R.; Vera-Sirera, F.; Merilo, E.; Bassel, G.W.; Fernández, M.A.; Holdsworth, M.J.; Perez-Amador, M.A.; Kollist, H.; et al. Arabidopsis PYR/PYL/RCAR receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid. Plant Cell 2012, 24, 2483–2496.
  42. Dittrich, M.; Mueller, H.M.; Bauer, H.; Peirats-Llobet, M.; Rodriguez, P.L.; Geilfus, C.M.; Carpentier, S.C.; Al Rasheid, K.A.S.; Kollist, H.; Merilo, E.; et al. The role of Arabidopsis ABA receptors from the PYR/PYL/RCAR family in stomatal acclimation and closure signal integration. Nat. Plants 2019, 5, 1002–1011.
  43. Umezawa, T.; Sugiyama, N.; Mizoguchi, M.; Hayashi, S.; Myouga, F.; Yamaguchi-Shinozaki, K.; Ishihama, Y.; Hirayama, T.; Shinozaki, K. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis. Proc. Natl. Acad. Sci. USA 2009, 106, 17588–17593.
  44. Jung, C.; Nguyen, N.H.; Cheong, J.-J. Transcriptional regulation of protein phosphatase 2C genes to modulate abscisic acid signaling. Int. J. Mol. Sci. 2020, 21, 9517.
  45. Umezawa, T.; Nakashima, K.; Miyakawa, T.; Kuromori, T.; Tanokura, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Molecular basis of the core regulatory network in ABA responses: Sensing, signaling and transport. Plant Cell Physiol. 2010, 51, 1821–1839.
  46. Dong, T.; Park, Y.; Hwang, I. Abscisic acid: Biosynthesis, inactivation, homoeostasis and signaling. Essays Biochem. 2015, 58, 29–48.
  47. Yoshida, T.; Fujita, Y.; Maruyama, K.; Mogami, J.; Todaka, D.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant Cell Environ. 2015, 38, 35–49.
  48. Yoshida, T.; Fujita, Y.; Sayama, H.; Kidokoro, S.; Maruyama, K.; Mizoi, J.; Shinozaki, K.; Yamaguchi-Shinozaki, K. AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 2010, 61, 672–685.
  49. Liu, H.; Able, A.J.; Able, J.A. Priming crops for the future: Rewiring stress memory. Trends Plant Sci. 2022, 27, 699–716.
  50. Sadhukhan, A.; Prasad, S.S.; Mitra, J.; Siddiqui, N.; Sahoo, L.; Kobayashi, Y.; Koyama, H. How do plants remember drought? Planta 2022, 256, 7.
  51. Walter, J.; Nagy, L.; Hein, R.; Rascher, U.; Beierkuhnlein, C.; Willner, E.; Jentsch, A. Do plants remember drought? Hints towards a drought-memory in grasses. Environ. Exp. Bot. 2011, 71, 34–40.
  52. Ding, Y.; Fromm, M.; Avramova, Z. Multiple exposures to drought ‘train’ transcriptional responses in Arabidopsis. Nat. Commun. 2012, 3, 740.
  53. Wang, X.; Vignjevic, M.; Jiang, D.; Jacobsen, S.; Wollenweber, B. Improved tolerance to drought stress after anthesis due to priming before anthesis in wheat (Triticum aestivum L.) var. Vinjett. J. Exp. Bot. 2014, 65, 6441–6456.
  54. Ramírez, D.A.; Rolando, J.L.; Yactayo, W.; Monneveux, P.; Mares, V.; Quiroz, R. Improving potato drought tolerance through the induction of long-term water stress memory. Plant Sci. 2015, 238, 26–32.
  55. Abdallah, M.B.; Methenni, K.; Nouairi, I.; Zarrouk, M.; Youssef, N.B. Drought priming improves subsequent more severe drought in a drought-sensitive cultivar of olive cv. Chétoui. Sci. Hortic. 2017, 221, 43–52.
  56. Tabassum, T.; Farooq, M.; Ahmad, R.; Zohaib, A.; Wahid, A.; Shahid, M. Terminal drought and seed priming improves drought tolerance in wheat. Physiol. Mol. Biol. Plants 2018, 24, 845–856.
  57. Goh, C.-H.; Nam, H.G.; Park, Y.S. Stress memory in plants: A negative regulation of stomatal response and transient induction of rd22 gene to light in abscisic acid-entrained Arabidopsis plants. Plant J. 2003, 36, 240–255.
  58. Virlouvet, L.; Fromm, M. Physiological and transcriptional memory in guard cells during repetitive dehydration stress. New Phytol. 2015, 205, 596–607.
  59. Li, P.; Yang, H.; Wang, L.; Liu, H.; Huo, H.; Zhang, C.; Liu, A.; Zhu, A.; Hu, J.; Lin, Y.; et al. Physiological and transcriptome analyses reveal short-term responses and formation of memory under drought stress in rice. Front. Genet. 2019, 10, 55.
  60. Ding, Y.; Liu, N.; Virlouvet, L.; Riethoven, J.-J.; Fromm, M.; Avramova, Z. Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biol. 2013, 13, 229.
  61. Kim, Y.-K.; Chae, S.; Oh, N.-I.; Nguyen, N.H.; Cheong, J.-J. Recurrent drought conditions enhance the induction of drought stress memory genes in Glycine max L. Front. Genet. 2020, 11, 576086.
  62. Ding, Y.; Virlouvet, L.; Liu, N.; Riethoven, J.-J.; Fromm, M.; Avramova, Z. Dehydration stress memory genes of Zea mays; comparison with Arabidopsis thaliana. BMC Plant Biol. 2014, 14, 141.
  63. Chen, Y.; Li, C.; Yi, J.; Yang, Y.; Lei, C.; Gong, M. Transcriptome response to drought, rehydration and re-dehydration in potato. Int. J. Mol. Sci. 2020, 21, 159.
  64. Brzezinka, K.; Altmann, S.; Czesnick, H.; Nicolas, P.; Gorka, M.; Benke, E.; Kabelitz, T.; Jähne, F.; Graf, A.; Kappel, C.; et al. Arabidopsis FORGETTER1 mediates stress-induced chromatin memory through nucleosome remodeling. eLife 2016, 5, e17061.
  65. Liu, J.; He, Z. Small DNA methylation, big player in plant abiotic stress responses and memory. Front. Plant Sci. 2020, 11, 595603.
  66. Wang, W.-S.; Pan, Y.-J.; Zhao, X.-Q.; Dwivedi, D.; Zhu, L.-H.; Ali, J.; Fu, B.-Y.; Li, Z.-K. Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). J. Exp. Bot. 2011, 62, 1951–1960.
  67. Kou, S.Y.; Gu, Q.Y.; Duan, L.; Liu, G.J.; Yuan, P.R.; Li, H.H.; Wu, Z.G.; Liu, W.H.; Huang, P.; Liu, L. Genome-wide bisulphite sequencing uncovered the contribution of DNA methylation to rice short-term drought memory formation. J. Plant Growth Regul. 2021, 1–15.
  68. Hennig, L.; Derkacheva, M. Diversity of Polycomb group complexes in plants: Same rules, different players? Trends Genet. 2009, 25, 414–423.
  69. Margueron, R.; Reinberg, D. The Polycomb complex PRC2 and its mark in life. Nature 2011, 469, 343–349.
  70. Margueron, R.; Li, G.; Sarma, K.; Blais, A.; Zavadil, J.; Woodcock, C.L.; Dynlacht, B.D.; Reinberg, D. Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol. Cell 2008, 32, 503–518.
  71. Gao, Z.; Zhang, J.; Bonasio, R.; Strino, F.; Sawai, A.; Parisi, F.; Kluger, Y.; Reinberg, D. PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes. Mol. Cell 2012, 45, 344–356.
  72. Tavares, L.; Dimitrova, E.; Oxley, D.; Webster, J.; Poot, R.; Demmers, J.; Bezstarosti, K.; Taylor, S.; Ura, H.; Koide, H.; et al. RYBP-PRC1 complexes mediate H2A ubiquitylation at Polycomb target sites independently of PRC2 and H3K27me3. Cell 2012, 148, 664–678.
  73. Blackledge, N.P.; Klose, R.J. The molecular principles of gene regulation by Polycomb repressive complexes. Nat. Rev. Mol. Cell Biol. 2021, 22, 815–833.
  74. Baile, F.; Gómez-Zambrano, Á.; Calonje, M. Roles of Polycomb complexes in regulating gene expression and chromatin structure in plants. Plant Commun. 2022, 3, 100267.
  75. Bratzel, F.; López-Torrejón, G.; Koch, M.; Del Pozo, J.C.; Calonje, M. Keeping cell identity in Arabidopsis requires PRC1 RING-finger homologs that catalyze H2A monoubiquitination. Curr. Biol. 2010, 20, 1853–1859.
  76. Yang, C.; Bratzel, F.; Hohmann, N.; Koch, M.; Turck, F.; Calonje, M. VAL- and AtBMI1-mediated H2Aub initiate the switch from embryonic to postgerminative growth in Arabidopsis. Curr. Biol. 2013, 23, 1324–1329.
  77. Wang, Q.; Shen, W.-H. Chromatin modulation and gene regulation in plants: Insight about PRC1 function. Biochem. Soc. Trans. 2018, 46, 957–966.
  78. Vijayanathan, M.; Trejo-Arellano, M.G.; Mozgová, I. Polycomb repressive complex 2 in eukaryotes-An evolutionary perspective. Epigenomes 2022, 6, 3.
  79. Mozgova, I.; Hennig, L. The Polycomb group protein regulatory network. Annu. Rev. Plant Biol. 2015, 66, 269–296.
  80. Bieluszewski, T.; Xiao, J.; Yang, Y.; Wagner, D. PRC2 activity, recruitment, and silencing: A comparative perspective. Trends Plant Sci. 2021, 26, 1186–1198.
  81. Godwin, J.; Farrona, S. The importance of networking: Plant Polycomb Repressive Complex 2 and its interactors. Epigenomes 2022, 6, 8.
  82. Mylne, J.S.; Barrett, L.; Tessadori, F.; Mesnage, S.; Johnson, L.; Bernatavichute, Y.V.; Jacobsen, S.E.; Fransz, P.; Dean, C. LHP1, the Arabidopsis homologue of HETEROCHROMATIN PROTEIN1, is required for epigenetic silencing of FLC. Proc. Natl. Acad. Sci. USA 2006, 103, 5012–5017.
  83. Hecker, A.; Brand, L.H.; Peter, S.; Simoncello, N.; Kilian, J.; Harter, K.; Gaudin, V.; Wanke, D. The Arabidopsis GAGA-binding factor basic pentacysteine6 recruits the polycomb-repressive complex1 component like heterochromatin protein1 to GAGA DNA motifs. Plant Physiol. 2015, 168, 1013–1024.
  84. Ramirez-Prado, J.S.; Latrasse, D.; Rodriguez-Granados, N.Y.; Huang, Y.; Manza-Mianza, D.; Brik-Chaouche, R.; Jaouannet, M.; Citerne, S.; Bendahmane, A.; Hirt, H.; et al. The Polycomb protein LHP1 regulates Arabidopsis thaliana stress responses through the repression of the MYC2-dependent branch of immunity. Plant J. 2019, 100, 1118–1131.
  85. Liu, N.; Ding, Y.; Fromm, M.; Avramova, Z. Different gene-specific mechanisms determine the ‘revised-response’ memory transcription patterns of a subset of A. thaliana dehydration stress responding genes. Nucleic Acids Res. 2014, 42, 5556–5566.
  86. Liu, N.; Fromm, M.; Avramova, Z. H3K27me3 and H3K4me3 chromatin environment at super-induced dehydration stress memory genes of Arabidopsis thaliana. Mol. Plant 2014, 7, 502–513.
  87. Kim, J.-M.; To, T.K.; Ishida, J.; Matsui, A.; Kimura, H.; Seki, M. Transition of chromatin status during the process of recovery from drought stress in Arabidopsis thaliana. Plant Cell Physiol. 2012, 53, 847–856.
  88. Piunti, A.; Shilatifard, A. Epigenetic balance of gene expression by Polycomb and COMPASS families. Science 2016, 352, aad9780.
  89. Schuettengruber, B.; Bourbon, H.-M.; Croce, L.D.; Cavalli, G. Genome regulation by Polycomb and Trithorax: 70 years and counting. Cell 2017, 171, 34–57.
  90. Fletcher, J.C. State of the art: TrxG factor regulation of post-embryonic plant development. Front. Plant Sci. 2017, 8, 1925.
  91. Grini, P.E.; Thorstensen, T.; Alm, V.; Vizcay-Barrena, G.; Windju, S.S.; Jørstad, T.S.; Wilson, Z.A.; Aalen, R.B. The ASH1 HOMOLOG 2 (ASHH2) histone H3 methyltransferase is required for ovule and anther development in Arabidopsis. PLoS ONE 2009, 4, e7817.
  92. Guo, L.; Yu, Y.; Law, J.A.; Zhang, X. SET DOMAIN GROUP2 is the major histone H3 lysine 4 trimethyltransferase in Arabidopsis. Proc. Natl. Acad. Sci. USA 2010, 107, 18557–18562.
  93. Carter, B.; Henderson, J.T.; Svedin, E.; Fiers, M.; McCarthy, K.; Smith, A.; Guo, C.; Bishop, B.; Zhang, H.; Riksen, T.; et al. Cross-talk between sporophyte and gametophyte generations is promoted by CHD3 chromatin remodelers in Arabidopsis thaliana. Genetics 2016, 203, 817–829.
  94. Chen, L.-Q.; Luo, J.-H.; Cui, Z.-H.; Xue, M.; Wang, L.; Zhang, X.-Y.; Pawlowski, W.P.; He, Y. ATX3, ATX4, and ATX5 encode putative H3K4 methyltransferases and are critical for plant development. Plant Physiol. 2017, 174, 1795–1806.
  95. Ding, Y.; Ndamukong, I.; Xu, Z.; Lapko, H.; Fromm, M.; Avramova, Z. ATX1-generated H3K4me3 is required for efficient elongation of transcription, not initiation, at ATX1-regulated genes. PLoS Genet. 2012, 8, e1003111.
  96. Fromm, M.; Avramova, Z. ATX1/AtCOMPASS and the H3K4me3 marks: How do they activate Arabidopsis genes? Curr. Opin. Plant Biol. 2014, 21, 75–82.
  97. Howe, F.S.; Fischl, H.; Murray, S.C.; Mellor, J. Is H3K4me3 instructive for transcription activation? Bioessays 2017, 39, 1–12.
  98. Boyko, A.; Kovalchuk, I. Genome instability and epigenetic modification--heritable responses to environmental stress? Curr. Opin. Plant Biol. 2011, 14, 260–266.
  99. Verkest, A.; Byzova, M.; Martens, C.; Willems, P.; Verwulgen, T.; Slabbinck, B.; Rombaut, D.; Van de Velde, J.; Vandepoele, K.; Standaert, E.; et al. Selection for improved energy use efficiency and drought tolerance in canola results in distinct transcriptome and epigenome changes. Plant Physiol. 2015, 168, 1338–1350.
  100. Tabassum, T.; Farooq, M.; Ahmad, R.; Zohaib, A.; Wahid, A. Seed priming and transgenerational drought memory improves tolerance against salt stress in bread wheat. Plant Physiol. Biochem. 2017, 118, 362–369.
  101. Raju, S.K.K.; Shao, M.R.; Sanchez, R.; Xu, Y.Z.; Sandhu, A.; Graef, G.; Mackenzie, S. An epigenetic breeding system in soybean for increased yield and stability. Plant Biotechnol. J. 2018, 16, 1836–1847.
  102. Campos, E.I.; Stafford, J.M.; Reinberg, D. Epigenetic inheritance: Histone bookmarks across generations. Trends Cell Biol. 2014, 24, 664–674.
  103. Fabrizio, P.; Garvis, S.; Palladino, F. Histone methylation and memory of environmental stress. Cells 2019, 8, 339.
  104. Šrut, M. Ecotoxicological epigenetics in invertebrates: Emerging tool for the evaluation of present and past pollution burden. Chemosphere 2021, 282, 131026.
  105. Zenk, F.; Loeser, E.; Schiavo, R.; Kilpert, F.; Bogdanović, O.; Iovino, N. Germ line-inherited H3K27me3 restricts enhancer function during maternal-to-zygotic transition. Science 2017, 357, 212–216.
  106. Molla-Herman, A.; Matias, N.R.; Huynh, J.R. Chromatin modifications regulate germ cell development and transgenerational information relay. Curr. Opin. Insect Sci. 2014, 1, 10–18.
  107. Weiser, N.E.; Kim, J.K. Multigenerational regulation of the Caenorhabditis elegans chromatin landscape by germline small RNAs. Annu. Rev. Genet. 2019, 53, 289–311.
  108. Zheng, X.; Chen, L.; Xia, H.; Wei, H.; Lou, Q.; Li, M.; Li, T.; Luo, L. Transgenerational epimutations induced by multi-generation drought imposition mediate rice plant’s adaptation to drought condition. Sci. Rep. 2017, 7, 39843.
  109. Mathieu, O.; Reinders, J.; Caikovski, M.; Smathajitt, C.; Paszkowski, J. Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 2007, 130, 851–862.
  110. Zhang, Y.Y.; Fischer, M.; Colot, V.; Bossdorf, O. Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol. 2013, 197, 314–322.
  111. Cortijo, S.; Wardenaar, R.; Colomé-Tatché, M.; Gilly, A.; Etcheverry, M.; Labadie, K.; Caillieux, E.; Hospital, F.; Aury, J.M.; Wincker, P.; et al. Mapping the epigenetic basis of complex traits. Science 2014, 343, 1145–1148.
  112. Matzke, M.A.; Mosher, R.A. RNA-directed DNA methylation: An epigenetic pathway of increasing complexity. Nat. Rev. Genet. 2014, 15, 394–408.
  113. Morgado, L.; Preite, V.; Oplaat, C.; Anava, S.; de Carvalho, J.F.; Rechavi, O.; Johannes, F.; Verhoeven, K.J.F. Small RNAs reflect grandparental environments in apomictic dandelion. Mol. Biol. Evol. 2017, 34, 2035–2040.
  114. Kuhlmann, M.; Finke, A.; Mascher, M.; Mette, M.F. DNA methylation maintenance consolidates RNA-directed DNA methylation and transcriptional gene silencing over generations in Arabidopsis thaliana. Plant J. 2014, 80, 269–281.
  115. Wibowo, A.; Becker, C.; Marconi, G.; Durr, J.; Price, J.; Hagmann, J.; Papareddy, R.; Putra, H.; Kageyama, J.; Becker, J.; et al. Hyperosmotic stress memory in Arabidopsis is mediated by distinct epigenetically labile sites in the genome and is restricted in the male germline by DNA glycosylase activity. eLife 2016, 5, e13546.
  116. Ganguly, D.R.; Crisp, P.A.; Eichten, S.R.; Pogson, B.J. The Arabidopsis DNA methylome is stable under transgenerational drought stress. Plant Physiol. 2017, 175, 1893–1912.
  117. Van Dooren, T.J.M.; Silveira, A.B.; Gilbault, E.; Jiménez-Gómez, J.M.; Martin, A.; Bach, L.; Tisné, S.; Quadrana, L.; Loudet, O.; Colot, V. Mild drought in the vegetative stage induces phenotypic, gene expression and DNA methylation plasticity in Arabidopsis but no transgenerational effects. J. Exp. Bot. 2020, 71, 3588–3602.
  118. Braun, R.E. Packaging paternal chromosomes with protamine. Nat. Genet. 2001, 28, 10–12.
  119. Reik, W.; Dean, W.; Walter, J. Epigenetic reprogramming in mammalian development. Science 2001, 293, 1089–1093.
  120. Feng, X.J.; Li, J.R.; Qi, S.L.; Lin, Q.F.; Jin, J.B.; Hua, X.J. Light affects salt stress-induced transcriptional memory of P5CS1 in Arabidopsis. Proc. Natl. Acad. Sci. USA 2016, 113, E8335–E8343.
  121. Calarco, J.P.; Borges, F.; Donoghue, M.T.; Van Ex, F.; Jullien, P.E.; Lopes, T.; Gardner, R.; Berger, F.; Feijó, J.A.; Becker, J.D.; et al. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 2012, 151, 194–205.
  122. Heard, E.; Martienssen, R.A. Transgenerational epigenetic inheritance: Myths and mechanisms. Cell 2014, 157, 95–109.
  123. Borg, M.; Berger, F. Chromatin remodelling during male gametophyte development. Plant J. 2015, 83, 177–188.
  124. Borg, M.; Jacob, Y.; Susaki, D.; LeBlanc, C.; Buendía, D.; Axelsson, E.; Kawashima, T.; Voigt, P.; Boavida, L.; Becker, J.; et al. Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin. Nat. Cell Biol. 2020, 22, 621–629.
  125. Inoue, A.; Jiang, L.; Lu, F.; Suzuki, T.; Zhang, Y. Maternal H3K27me3 controls DNA methylation-independent imprinting. Nature 2017, 547, 419–424.
  126. Grossniklaus, U.; Paro, R. Transcriptional silencing by polycomb-group proteins. Cold Spring Harb. Perspect. Biol. 2014, 6, a019331.
More
Information
Subjects: Plant Sciences
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register : , ,
View Times: 596
Revisions: 2 times (View History)
Update Date: 15 Nov 2022
1000/1000
Video Production Service