Abstract
Plants are sessile organisms and, as such, their survival relies on their ability to respond quickly all along their life cycle to any kind of environmental stimuli, including abiotic and biotic stresses. In this respect, plants have developed efficient mechanisms of protection and/or adaptation to minimize deleterious effects of stress on their growth and development. In a stress type-dependent manner, external signals are firstly sensed. This step is then followed by the activation of particular signalling pathways, resulting ultimately in the rapid and specific modulation of the plant transcriptome. Currently, transcriptional regulation is considered as a central process in the build-up of plant responses to both abiotic and biotic stresses. Among mechanisms involved in transcriptional regulation, the combined effect of different histone tail post-translational modifications (PTMs; e.g. acetylation and methylation) through the activity of particular histone-modifying enzymes can lead to changes in the local chromatin structure environment and hence the underlying DNA accessibility.
Keywords
- Histone methylation and demethylation
- histone methyltransferases and demethylases
- biotic and abiotic stresses
1. Introduction
Stress, as we currently think of it, is a highly subjective phenomenon defined as a state of threatened homeostasis. Depending on their nature, external stresses are usually divided into biotic (i.e. herbivorous insects and pathogens such as fungi, bacteria and viruses) or abiotic (i.e. including, among others, high or low temperature, submergence or drought and salinity). During their lifetime, all living organisms inevitably and constantly face all sorts of environmental stresses that often occur suddenly and/or simultaneously. Classically, different strategies can be applied to minimize deleterious effects of stresses, such as resistance, tolerance, avoidance or escape. Being sessile, plants cannot escape and are therefore more prone to the deleterious effect of unfavourable environmental growth conditions. Because responses are critical to ensure their survival, plants have developed specific and efficient strategies that allow them to precisely perceive different environmental stresses and respond and/or adapt to them [1, 2]. In addition to preformed defence traits, plants have evolved inducible defence strategies. Indeed, upon perception, each stress will raise a complex and more or less specific repertoire of cellular and molecular responses implemented by the plant to minimize or prevent damage. Particularly, the stimulation of a given stress-signalling pathway after pathogen detection will be integrated into the plant cell nucleus through a set of regulatory transcription factor cascades, which prioritizes defence over growth-related cellular functions, while conserving enough valuable resources for survival and reproduction [3, 4]. Supporting the idea that the capacity of a plant to rapidly reprogramme its gene expression at the transcriptional level is an essential and common component of all plant response strategies to stress and disturbance; more than 1,000 transcription factors were found to be involved in stress responses [5, 6]. Because eukaryotic genes function in the context of chromatin, modifications and remodelling of the chromatin configuration from permissive for transcription to restrictive, and vice versa, may be an integral part of mechanisms involved in this vital transcriptional reprogramming. In this chapter, we review and discuss the current knowledge about the functional impact of chromatin changes on the transcriptional regulation of genes under different stress conditions, with particular emphasis on histone methylation/demethylation.
2. Chromatin structure and histone methylation/demethylation
In eukaryotes, genomic DNA in the cell nucleus is packaged in a complex and evolutionarily conserved structure named chromatin, with nucleosome as the basic unit. The nucleosome complex contains about 160–241 base pairs (bp) of DNA, a nucleosome core particle and the H1 linker histone. The nucleosome core particle is composed of an octamer of core histones, consisting of two H3–H4 dimers associated with two H2A–H2B dimers. About 146 bp of DNA is wrapped in ~1.65 negatively supercoiled circles around the histone octamer, while the linker DNA associated with H1 varies in length from 8 to 114 bp [7]. At first sight, the chromatin as it is described appears as a barrier, restricting the access of all kinds of enzymes that process the DNA. However, nucleosomes are not merely static but highly dynamic entities. Indeed, nucleosomes can be moved, stabilized/destabilized, disassembled/reassembled at particular genome locations in response to specific environmental signals or developmental cues [8]. This dynamic leads to a wide range of chromatin condensation states modulating the DNA accessibility, with euchromatin, being relaxed, and heterochromatin, being compacted. Therefore, in eukaryotic cells, an intimate connection exists between the structural organization of the genome and its functioning. For this reason, the level of chromatin condensation is directly related to all aspects of DNA metabolism, thus playing a major role in regulating transcription, DNA replication, DNA repair, recombination, transposition and chromosome segregation. In plants, changes in the chromatin structure were reported to affect various biological processes such as root growth, flowering, organogenesis, gametophyte or embryo formation [9–11].
In the nucleosome core particle, histones H2A, H2B, H3 and H4 possess two common regions, a histone-fold domain and a histone tail. The histone-fold domain is the most conserved region and the main element of histone dimerization [12]. The tail protrudes from the nucleosome core particle and is more variable and unstructured than the fold [13]. All four core histones have an N-terminal tail domain, but only histone H2A has an additional long C-terminal tail. Histone tails are extremely basic due to their particularly high content in basic amino acid residues, such as lysine and arginine [14]. Resulting positive charges allow them to closely associate with the negatively charged nucleosomal DNA through electrostatic interactions [15]. In addition, histone tails, especially N-terminal ones, may undergo diverse types of post-translational modifications such as acetylation or methylation. The great diversity of these modifications as well as the high number of amino acid residues that can be modified within histone tails, and the correlation between these modifications and various nuclear processes, lead to the hypothesis that the specific combination of histone modifications constitute a histone ‘code’ [16].
Technically, these histone marks can be localized by chromatin immunoprecipitation (ChIP) using specific antibodies against the modification [17]. Briefly, protein–DNA interactions are stabilized by cross-linking with formaldehyde; chromatin is sheared into small pieces to facilitate analysis and then immunoprecipitated using an antibody raised against a specific histone modification. Following enrichment, cross links are reversed to release DNA, which is then quantified by polymerase chain reaction (PCR) to measure the relative amount of the specific histone mark on selected plant genes. ChIP can also be combined with microarray hybridization (ChIP-chip) or high-throughput sequencing (ChIP-Seq), allowing the genome-wide discovery of DNA–histone modification interactions.
Methylation is the most abundant one compared with other histone PTMs. It can occur at both lysine (K) and arginine (R) residues of core histone tails. Further extending the indexing potential of this modification, mono-, di- and trimethylation of lysine and mono- and dimethylation (symmetric or asymmetric) of arginine are common at N-terminal tails of H2A, H2B, H3 and H4. Although histone acetylation is generally associated with active gene transcription, histone methylation can be associated with either active or silent gene expression, depending upon the histone, the methylated residue or the level (mono-, di- or tri-) of methylation. In
Histone methylation is relatively stable and can be established on lysine and arginine by two distinct families of enzymes, the histone lysine methyltransferases (HKMTs), all containing the evolutionary conserved catalytic SET domain in plants [24], and the protein arginine methyltransferases (PRMTs) [25], respectively. As a counterpart, methyl groups on histone can also be removed by at least two evolutionarily conserved classes of histone demethylases, the lysine-specific demethylase1 (LSD1) type and the Jumonji C (JmjC) domain-containing demethylases [26]. Histone methyltransferases and demethylases are well conserved in angiosperms and have been identified and classified on the basis of phylogenetic analyses and domain organization in several plants, including
Although histone acetylation can directly modulate the chromatin structure, arginine and lysine methylation of histone tails can promote or prevent the docking of key transcriptional effector molecules, named readers, needed to ‘translate’ the code in order to determine the functional and structural outcome of the corresponding PTMs. Just as there are a large number of PTMs on histone tails, there are also numerous protein domains that recognize and bind to particular PTMs on these tails. For example, PTM-recognition domains such as plant homeodomain (PHD) fingers, chromodomains and Tudor domains all recognize methylated lysine residues [33].
3. Histone methylation changes associated with biotic stress conditions
Biotic stress is the result of the damage done to plants by insects or pathogens, such as bacteria or fungi. Plant pathogens are generally divided into two distinct categories: biotrophs, which colonize living plant tissue and obtain nutrients from living host cells, and necrotrophs, which depend on dead host tissue for nutrients and reproduction. To fend off pathogens with different infection strategies, plants have evolved complex defence mechanisms. Classically, the pathogen-sensing machinery induces signalling cascades that promote the accumulation of hormones such as salicylic acid (SA) or jasmonic acid (JA)/ethylene (ET) [34]. These hormones then orchestrate the overall plant defence reaction locally and systemically by inducing the transcriptional activation of defence genes through an intricate signalling network. In this part, we highlight recent examples illustrating how histone methylations condition major steps leading to immunity, ranging from initial pathogen perception to hormonal homeostasis changes for antimicrobial effector expression.
3.1. Histone methylation/demethylation in the defence against biotrophic pathogens
The phytohormone SA plays an important role in plant defence, from the induction of pathogen resistance (
The ARABIDOPSIS HOMOLOG OF TRITHORAX (ATX1) is a H3K4 trimethyltransferase providing basal resistance against
Apart from
3.2. Histone methylation/demethylation in the defence against necrotrophic pathogens
While to combat biotrophic pathogens the plant activates mainly the SA signalling pathway, the activation of the JA/ET signalling pathway is prominent to mediate defences against necrotrophic pathogens and herbivorous insect attacks [50]. The involvement of histone methylation in the defence against necrotrophic pathogens is far less documented as compared with the defence against biotrophic pathogens. Besides being more susceptible to
4. Histone methylation changes associated with abiotic stress conditions
Abiotic stresses such as heat, cold, drought, salinity and nutrient deficiency are inherent to every ecosystem and essentially unavoidable. Abiotic stresses are considered the most harmful factors in terms of growth and productivity of crops worldwide [54, 55], especially when they occur in combinations [56]. Here, we summarize and discuss various studies in order to clarify the functional involvement of different histone methylation marks in setting up plant responses to adverse environmental growth conditions.
4.1. Histone methylation/demethylation and the plant stress hormone ABA
The phytohormone abscisic acid (ABA) is a crucial signalling molecule playing versatile functions in regulating many developmental processes, including seed dormancy and germination [57, 58]. ABA also plays a pivotal role in adaptive stress processes, integrating both biotic and abiotic environmental constraints in a complex network of interacting pathways with crosstalks at different levels [59–61]. Currently, ABA is considered as a global regulator of stress responses that can dominantly control the switch in priority between the responses to biotic or abiotic stress, allowing plants to respond to the most severe threat [62].
The transition from heterotrophic to autotrophic development at the post-germinative stage (i.e. embryonic state) is highly vulnerable to osmotic stress [63]. During a period of osmotic stress, ABA promotes the expression of transcription factors such as ABI3 and ABI5, which in turn delay germination and lead to osmotolerance and survival [64]. In
In adult plants, the establishment of a response and tolerance to drought stress by ABA has been extensively studied and is well discussed in several outstanding reviews [58, 66]. Briefly, under drought conditions, water stress perception triggers ABA biosynthesis and increased tissue ABA accumulation, resulting in stomatal closure and reduced transpiration. Among major enzymes involved in the ABA biosynthesis pathway, NINE-CIS-EPOXYCAROTENOID DIOXYGENASE 3 (NCED3) is thought to be the rate-limiting enzyme [67]. In
4.2. Histone methylation/demethylation in response to water stresses
Water stresses including drought or submergence are major environmental factors limiting plant growth and crop productivity worldwide [69, 70]. Consequently, plants have evolved a variety of biochemical and physiological mechanisms to respond/adapt to these stresses [71, 72]. In the following section, we distinctly address the involvement of histone methylation in responses to drought and submergence.
4.2.1. Drought stress
Using
In a similar approach but using ChIP-Seq, van Dijk et al. [76] established the whole-genome distribution patterns of H3K4me1, H3K4me2 and H3K4me3 in 4-week-old rosette
Through a genome-wide approach in rice seedling, Zong et al. [80] also uncovered a weak but positive correlation between H3K4me3 enrichment and the transcript level of some drought-responsive genes under drought stress. This correlation was extended to many genes involved in stress-related metabolite and hormone signalling pathways, further supporting the role played by H3K4me3 in the stress response [80]. However, because H3K4me3 is not the only histone mark for gene activation, this weak correlation may reflect that other active histone marks may also play important roles in regulating gene expression in response to stress in rice. Although these large data sets have provided much information on drought responses in rice, more detailed analyses will be required to elucidate whether the observed variations in H3K4 methylation are a cause or a consequence of the transcriptional changes triggered by water stress. Moreover, identifying key histone modification enzymes is indispensable to better understand the transcriptional regulatory network of the abiotic stress response.
4.2.2. Submergence
Submergence is a complex stress that encompasses many changes in environmental factors, including light intensity, pH and dissolved oxygen concentration. Alcoholic fermentation is important for the survival of plants especially under anaerobic environments [81]. In rice,
4.3. Histone methylation/demethylation in response to salt stress
Salinity is also a serious factor affecting plants in several ways (i.e. water stress, ion toxicity, nutritional disorders, oxidative stress, alteration of metabolic processes, membrane disorganization, genotoxicity, reduction of cell division and expansion), thus limiting plant growth, development and survival [84]. In
In soya bean and in response to a high NaCl concentration, these histone methylation marks were also found altered at some salinity-induced transcription factors (i.e. MYB, b-ZIP and AP2/DREB family members) that were primarily identified by microarray analysis [88]. For some genes, their transcriptional induction was correlated with an increased level of histone acetylation and H3K4me3, accompanied or not with a reduced level of DNA methylation and H3K9me2 in various parts of the promoter or coding regions. For other genes, DNA methylation had no influence on histone methylation. This work perfectly reflects the heterogeneity of the effect of salinity on histone methylation and DNA methylation, and supports the role(s) of histone methylation changes in the expression of some transcription factors important for salinity tolerance.
As mentioned above, H3K4me3 was found to be involved in the transcriptional induction of stress-responsive gene upon salt stress exposure. In plants, the JmjC-domain-containing histone demethylases JMJ14, JMJ15 and JMJ18 have been reported to display an H3K4me2/3 demethylase activity as well as to regulate diverse aspects of chromatin function and development [89–95]. Recently, the overexpression of
Besides histone lysine methylation, arginine methylation was also involved in establishing the transcriptional response to salt stress. The protein arginine methyltransferase 5 (PRMT5), also named Shk1 kinase-binding protein1 (SKB1), is a type II methyltransferase that catalyses symmetric H4R3 dimethylation, a repressive mark known to promote flowering through the repression of the floral repressor
4.4. Histone methylation/demethylation in response to temperature
In plants, temperature stresses are classically classified into different types according to temperature exposure, which may be warm, high, chilling or freezing temperature. Due to global warming and because temperature stress greatly affects plant growth and development, immunity and circadian rhythm, and poses a serious threat to the global food supply, the genetic mechanisms of plant responses to heat have been well studied. Plants exposed to temperature stresses modulate the transcription of a large number of genes involved in distinct biochemical and physiological response pathways and networks of phytohormones or secondary metabolites, ultimately leading to increased tolerance to hazardous temperature stresses [99–102]. The role played by histone methylation during the plant response to a heat or a cold stress is discussed separately hereafter.
4.4.1. Heat stress
Heat stress during seed development decreases the seed size in many cereals, resulting in severe yield losses [103, 104]. In rice, a molecular mechanism involving the putative rice polycomb repressive complex 2 (PRC2) gene
Because euchromatin is gene rich and usually transcriptionally active, investigation about the role of histone methylation in temperature stress acclimation was largely centred on euchromatin-associated coding regions. Focusing on the transcriptionally silent heterochromatin, mainly constituted of repetitive DNA sequences, some works demonstrated the transcriptional activation of normally silent transposable element embedded within heterochromatic regions under stress conditions [108]. Intriguingly, such activation under heat stress can occur without alteration of DNA methylation and with only minor changes in both H3K9me2 and H3K4me3 [109, 110]. In summary, these works suggest that temperature stress-mediated transcription of tandem-repeat elements might play a vital role in the adaptation of plants to temperature stimuli, offering an efficient mechanism by which heat or cold could promote the expression of some stress-responsive genes. Upon activation and when inserted into or very close to a gene, such transposable elements could interfere with the expression of this gene, giving rise to deleterious mutations, genetic instability or positive contribution to gene regulation and adaptation [111].
4.4.2. Cold stress
The increased tolerance of plants to cold is referred as ‘cold acclimation’. Cold acclimation differs from vernalization, as the last one requires a long-term exposure to cold temperatures, while cold acclimation can be achieved in a couple of days under non-freezing low temperatures [112]. Locally, histone methylation changes in cold-responsive genes were addressed in
In maize during cold stress, changes in histone modifications, including the heterochromatic marks H3K9me2 and DNA methylation, were assessed through a genome-wide approach [114]. The more detailed analysis of the two knob-associated tandem-repetitive sequences, the 180-bp repeat and the 350-bp repeat termed TR-1, demonstrated that their selectively and transiently cold-activated transcription was correlated with a decreased H3K9me2 and DNA methylation, together with an increased H3K9 acetylation. Such cold-induced transcriptional activation of tandem repeats is selective and transient, and the silencing state is recovered as the treatment continues.
5. Histone methylation as a memory mark of stress
In animals, the formation of memory immune cells after primary antigen recognition confers long-lasting resistance, resulting in an accelerated and a more effective immune response in case of second exposure. Despite the absence of such memory immune cells, plants often acquire a systemic immunity to further infections after a primary localized infection [115]. This requires the accumulation of the plant hormone SA in systemic tissues and is called systemic acquired resistance (reviewed in [116]. The SAR is also associated with gene priming in systemic tissues, in which defence genes will be expressed more rapidly and robustly in case of a second attack [117]. At the transcriptional level, gene expression is primarily influenced by the chromatin structure, which in turn is controlled partly by processes, often referred to as ‘epigenetic’ processes, which can be transmitted through mitosis and/or inherited through meiosis [118]. Therefore, chromatin remodelling through histone methylation offers a potential mechanism for short-/long-term stress memory within the lifespan of an individual, referred to as somatic memory, and/or across generations, referred to as transgenerational memory.
5.1. Somatic stress memory
In
Besides being involved in defence priming related to biotic stress, histone methylation was also proposed as a priming strategy against drought. To further explore the functional impact of histone methylation on biotic stress responses in
Using a large-scale approach, the distribution of H3K4me2, H3K4me3, H3K9me2 and H3K27me3 was analysed in
In contrast to H3K27me3, the higher level of H3K4me3 retained at the trainable gene
Because plant stress research has traditionally focused on single stresses, we separately described priming in response to abiotic or biotic environmental cues. However, in nature, plants are constantly exposed to mild environmental stresses during their lifetime. While testing how different environmental histories can affect the response of the plant to a subsequent biotic stress, Singh et al. [142] reported that
5.2. Transgenerational stress memory
The transgenerational stress memory refers to the transmittance of certain environmental responses from one generation to the next, thus providing the offspring of environmentally challenged plants with an adaptive advantage for better fitness (i.e. improve plant stress tolerance and impart developmental flexibility; [143]). Compared with DNA methylation and RNA interference (RNAi), very few studies suggest the involvement of histone methyltransferases and histone methylation changes in this process [144]. In
6. Discussion and perspectives
Recent advances, especially in
Nonetheless, this emerging view is facing many gaps, inaccuracies and divergences, mainly related to numerous difficulties inherent to the study of such a dynamic and acute process. In this respect, plants in nature are usually challenged simultaneously by different kinds of stresses. Responses to these stress combinations are largely controlled by different signalling pathways that can interact in a non-additive manner, producing effects that could not have been predicted from the study of either stress individually [151, 152]. The occurrence of simultaneous biotic and abiotic stresses introduces an added degree of complexity that requires stresses to be imposed simultaneously and to treat each set of environmental conditions as an entirely new stress. For this reason and to clarify the mechanism behind the regulation of stress responses by histone methylation changes, there is a strong necessity to intensify our investigations. For instance, the correlation between histone methylation/demethylation and stress responses remains elusive and clarifications will require in-depth dynamic approaches based on comparative analyses of both epigenomes and transcriptomes during stress responses. In parallel, current knowledge about the corresponding histone-modifying enzymes is still largely missing. This lack of knowledge is pending on the identification of different stress-responsive histone modifiers and will require large-scale screens and genetic analyses for the sensitivity of different histone methyltransferases/demethylases mutants to various stresses, combined or not. Among other factors governing stress-induced chromatin changes, almost nothing is known about the specific reader/effector that will recognize particular histone methylation sites in order to determine their functional and structural outcome. An effort in this direction will most likely benefit the comprehensive understanding of the fundamental mechanisms connecting histone methylation changes with the modulation of transcription of stress-responsive genes, subsequently enabling plant to withstand stress. Higher-resolution chromatin studies are undoubtedly required to reveal the targeted stress-responsive genes and the specific sites of histone methylation/demethylation. Nevertheless, investigation of the direct effects of histone methylation/demethylation in plants is difficult. One reason is that plant genomes harbour high-copy number of histone genes (e.g. the
Acknowledgments
This work was supported by the Centre National de la Recherche Scientifique, the Agence Nationale de la Recherche (ANR-12-BSV2-0013-02), the European Commission (FP7-PEOPLE-2013-ITN, grant number 607880), the National Council of Science and Technology of Mexico (CONACYT) and the Program ‘Estancias Posdoctorales y Sabaticas al Extranjero’ (Fellowship number 237557. BOBADILLA-LANDEY Roberto; CVU:162391).
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