Epigenetics, a mode for plants to respond to abiotic stresses

Abstract

Epigenetics has been becoming a hot topic in recent years. It can be mechanisms that regulate gene expression without changing DNA base sequence. In plants epigenetic regulation has been implicated to be a very important phenomenon and mechanism for the regulation of responses to environmental stresses. Environmental signals induce various epigenetic modifications in the genome, and these epigenetic modifications might likely be inherited to the next generation that behaves with enhanced ability to tolerate stresses. This review highlights recent advances in the study of epigenetics in plant stress responses.

Keywords

Epigenetics / chromatin / genome / environmental stress / histone modification

Introduction

Epigenetics had already been emerging as a new exciting branch of biology in the past 20 years, defined as mechanisms that regulate gene expression without DNA base sequence alteration. The major contents of epigenetics are DNA methylation and histone modification, which concentrate on the inheritant modifications of chromatin, and the production and action of some noncoding RNAs, especially small RNAs (Henderson and Jacobsen, 2007).

In plants epigenetic regulation has been revealed to be a very important control of plant growth and responses to environmental stresses. Environmental signals could also induce epigenetic modifications in the genome, including reversible methylation of DNA sequence, numerous histone modifications and chromatin remodeling. Stress induced epigenetic modifications might be inherited as “stress memory,” and improve the stress tolerance of plants in the next generation (Zhu, 2008).

Certain genes/proteins have been indicated to participate in epigenetic modifications and regulation of abiotic stress responses. Table 1 summarizes the genes or proteins involved in these processes.

DNA methylation

DNA methylation is one of the major mechanisms of epigenetics. DNA methylation usually means the methylation of cytosines in higher eukaryotes, this process was catalyzed by cytosine methyltransferases yielding 5-methylcytosine (m5C) after DNA replication (Henderson and Jacobsen, 2007).

Abiotic stresses can change the gene expression in plant cells through demethylation and hypermethylation of the genomic DNA. In tobacco, a glycerophosphodiesterase-like protein gene (NtGPDL) can be demethylated in the coding region when challenged by aluminum, low temperature and salt stresses, whereas the promoter sequences were totally unmethylated regardless of the stress. This demethylation correlates with NtGPDL gene expression. Grown under non-stress conditions, NtGPDL was not expressed, and its coding region was found to be heavily methylated. Upon exposure to abiotic stresses, NtGPDL transcripts were induced and its genomic locus was partially demethylated, whereas upon a biotic stress, no induction of either transcripts or genomic locus demethylation was observed (Choi and Sano, 2007).

Dyachenko et al. (2006) found that salt and drought stresses induced the CpHpG-hypermethylation of satellite DNA, in the genome of the facultative halophyte Mesembryanthemum crystallinum, that an induced switch of photosynthsis from C3 to CAM was coupled with stress-induced specific CpHpG-hypermethylation of the genome.

Drought stress could also induce DNA hypermethylation in the pea genome, specifically on the second cytosine of the CCGG target sequences (Labra et al., 2002). Salt or mild osmotic stress was observed to induce reversible DNA hypermethylation at two heterchromatic loci in tabacoo cell suspension culture (Kovarik et al., 1997). In maize, a cold stress induced ZmMI1 gene, was particularly demethylated in nucleosome cores under chilling conditions, and this demethylation cannot be reversed (Steward et al., 2002).

DNA methylation seems to be a key factor in the repression of the transposons, environmental stresses could also activate the transposable elements via DNA demethylation (Yoder et al., 1997; Martienssen, 1998). A transposon Tam3 in Antirrhinum majus udergoes a low temperature dependent transposition (LTDT), while this transposition strongly suppressed by a higher temperature (25°C). In the transposition, low temperature induced the DNA demethylation of Tam3 whereas high temperature induced the DNA hypermethylation. The Tam3 methylation level in LTDT was further demonstrated to be regulated by Tam3 activity, which is dependent on the ability of its TPase to bind DNA and impacted by growth temperature (Hashida et al., 2006).

Histone modifications

Covalent modifications of N-terminal regions of nucleosome core complex histones play a crucial role in chromatin structure and genomic stability, and thus determine the transcriptional state and expression level of genes. Histone modifications include acetylation, methylation, phosphorylation, ubiquitination, biotinylation and sumoylation. Some of them, namely acetylation, and in certain cases phosphorylation and ubiquitination (Sridhar et al., 2007; Zhang et al., 2007), enhance the transcription, while biotinylation and sumoylation repress the gene expression (Nathan et al., 2006; Camporeale et al., 2007; Chinnusamy and Zhu, 2009).

Post translational modifications

In response to environmental stresses, dynamic and reversible changes of histone H3K4 methylation and H3 acetylation of those stress-response genes usually occur in higher plants. Tsuji et al. (2006) studied the association of histone modifications with two submergence induced genes ADH1 and PDC1 in rice seedlings, and found that the Lys4 residues of histone H3 proteins (H3K4) at both the 5′ and 3′ coding regions of those two genes switched from dimethylation to trimethylation, and the acetylation of H3 increased throughout those entire genes, and that those histone modifications correlated with the increased expression of ADH1 and PDC1 under stress (Tsuji et al., 2006). In Arabidopsis and tobacoo, high salinity and cold stress induced a rapid transient upregulation of histone H3 Ser-10 phosphorylation, H3 phosphoacetylation and histone H4 acetylation, strictly correlated with the induction of stress-type specific genes (Sokol et al., 2007).

Histone H3K4 trimethylation and H3K9 acetylation usually associate with the activation of gene expression, while dimethylation of H3K9 and H3K27 represses transcription. Drought, ABA and salt stresses can induce H3K4 trimethylation and H3K9 acetylation in Arabidopsis, followed an induced expression of stress reponsive genes (Kim et al., 2008). ABA and salt stress can decrease H3K9 dimethylation, which can be considered as a repression marker for ABA and abiotic stress responsive genes (Chen et al., 2010).

Acetylation of the histones is often associated with increased gene activity, whereas deacetylation of the histones is correlated with transcriptional repression. Histone acetylases family (HDACs) mediate histone deacetylation in response to abiotic stresses in Arabidopsis and rice, the expression of different members of the HDAC families is differentially regulated by abiotic stresses like cold and salt, and hormones-like ABA, jasmonic acid (JA) (Fu et al., 2007). HDA6 and HDA19 could be induced by JA and ABA and HDA6 is invovled in transcriptional gene silencing (TGS) and RNA-directed DNA methylation in Arabidopsis (Aufsatz et al., 2002; Probst et al., 2004; Zhou et al., 2005). Stress signals enhance HDA6 and HDA19 expression, thus affecting chromatin modifications at particular gene loci, and increasing the expression levels of stress responsive genes like ERF1, PR, etc (Zhou et al. 2005). In Arabidopsishda6 mutant, the expression levels of ABA and salt stress responsive genes, such as ABI1, ABI2, KAT1, DREB2A, and RD29B, were decreased compared with those in wild type plants, and both knockout mutant and RNA-interfering plants were hypersensitive to ABA and salt stress (Chen et al., 2010).

ArabidopsisHD2C gene is downregulated by ABA signals, and the overexpression of AtHD2C results in the enhancement of LEA family genes expression and then improves salt tolerance of the transgenic Arabidopsis plants. Histone deacetylation was therefore suggested to play a key role in ABA invovled stress responses (Sridha and Wu, 2006). Histone acetyltransferases (HATs) could also activate the stress responsive gene through interacting with some stress induced transcription factors (Stockinger et al., 2001).

The histone gene expression

Each histone has variants that are encoded by different genes. Ascenzi and Gantt (1997) isolated and characterized a His1-3 gene encoding a structurally divergent linker histone from Arabidopsis. Both mRNA and protein levels of this gene could be specifically induced by drought. The His1-3 gene expression in tomato was also induced by water deficit (Scippa et al., 2000). And in rice, salt induces the H3.2 type histone H3 protein gene transcription (Qiu et al., 2006).

Small RNAs

Plants encode multiple homologs of the RNAi-machinery components, some of which are involved in RNA-directed DNA methylation and response to environmental stress signals. It is well documented that small interfering RNAs (siRNAs) and microRNAs (miRNAs) could silence genes post-transcriptionally by repressing and targeting mRNAs to degradation (Sunkar et al., 2007).

Previous studies showed that a large number of miRNAs and other small regulatory RNAs are encoded by the Arabidopsis genome, and some of them are regulated by abiotic stresses, based on an assay detecting a library of small RNAs from Arabidopsis seedlings exposed to salinity and other abiotic stresses (Sunkar and Zhu, 2004). A stress related gene, P5CDH, which determines the proline content and thus salt telorance in Arabidopsis, was downregulated by a 24-nt siRNA through the initial cleavage of its mRNA (Borsani et al., 2005). Twenty two nucleotides miRNAs regulate gene expression posttranscriptionally by directing mRNA cleavage or translational inhibition. Theoretically, stress-upregulated miRNAs target negative regulators of stress response or positive regulators of processes that are inhibited by stresses, and the stress-downregulated miRNAs could suppress the stress responsive genes or positive regulators. In Arabidopsis, miR398 targets and suppresses the expression of superoxide dismutase genes CSD1 and CSD2. Oxidative stress decreases the expression of miR398 and then induces the CSD1 and CSD2 transcription (Sunkar et al., 2006). The transcription of miR393, which inhibits TIR1 expression and downregulates seedling growth under abiotic stress conditions, was significantly increased by salinity, drought and low temperature stresses (Navarro et al. 2006). ABA-induced miR159 mediates the cleavage of MYB101 and MYB33 transcripts, as a mechanism to regulate many genes’ responses to abiotic stresses (Phillips et al., 2007).

Small interfering RNAs (siRNAs) have been demonstrated to be involved in RNA-directed DNA methylation (RdDM) which is critical for RNA interference or gene silencing. siRNAs are involved in at least one-third methylation of genomic loci (Lister et al., 2008). Some specific small RNAs have been revealed to be regulated by temperature and other abiotic stresses. Endogenous siRNAs that are regulated by abiotic stresses have been identified in Arabidopsis (Sunkar and Zhu, 2004). In Arabidopsis, 24-nt SRO5-P5CDH nat-siRNA downregulates the expression of P5CDH through mRNA cleavage, thereby decreasing proline degradation and enhancing proline accumulation and salt stress tolerance (Borsani et al., 2005). Further studies need to focus on elucidating the molecular mechanism underlying how siRNAs are involved in stress responses.

Summary

Although a lot of genes were well documented to be involved in stresses induced DNA and histone modifications, it is still unclear how much of changes may be epigenetic in nature as their mitotic and meiotic heritability is unknown. The epigenetic control over plant responses to environmental stresses is a complex process, it does not only affect the plant gene express and physiology, but also can constitute numerous change memories over couple of generations. Studies on epigenetic processes can deepen our understanding of how epigenetics-regulated gene expression controls plant development and stress tolerance. In the future, studies on how stress memory is coded by epigenetics inherited over generations should be emphasized, and it remains open for epigenetics involved plant stress response and tolerance mechanisms to be applicable in crop stress tolerance breeding.

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