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Review Article
Role of Epigenetics in Modulating Phenotypic Plasticity against
Abiotic Stresses in Plants
Fayaz Ahmad Dar ,
1
Naveed Ul Mushtaq ,
2
Seerat Saleem ,
2
Reiaz Ul Rehman ,
2
Tanvir Ul Hassan Dar ,
3
and Khalid Rehman Hakeem
4,5,6
1
Department of Bioresources, Amar Singh College Campus, Cluster University, Srinagar, 190008 Jammu and Kashmir, India
2
Department of Bioresources, University of Kashmir, Srinagar, 190006 Jammu and Kashmir, India
3
School of Biosciences and Biotechnology, Baba Ghulam Shah Badshah University, Rajouri 185234, Jammu and Kashmir, India
4
Department of Biological Sciences, Faculty of Science, King Abdulaziz University, Jeddah, Saudi Arabia
5
Princess Dr Najla Bint Saud Al-Saud Center for Excellence Research in Biotechnology, King Abdulaziz University,
Jeddah, Saudi Arabia
6
Department of Public Health, Daffodil International University, Dhaka, Bangladesh
Correspondence should be addressed to Reiaz Ul Rehman; rreiazbiores@gmail.com
and Khalid Rehman Hakeem; khakim@kau.edu.sa
Received 15 January 2022; Accepted 25 May 2022; Published 14 June 2022
Academic Editor: Ertugrul Filiz
Copyright © 2022 Fayaz Ahmad Dar et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is
properly cited.
Plants being sessile are always exposed to various environmental stresses, and to overcome these stresses, modifications at the
epigenetic level can prove vital for their long-term survival. Epigenomics refers to the large-scale study of epigenetic marks on
the genome, which include covalent modifications of histone tails (acetylation, methylation, phosphorylation, ubiquitination,
and the small RNA machinery). Studies based on epigenetics have evolved over the years especially in understanding the
mechanisms at transcriptional and posttranscriptional levels in plants against various environmental stimuli. Epigenomic
changes in plants through induced methylation of specific genes that lead to changes in their expression can help to overcome
various stress conditions. Recent studies suggested that epigenomics has a significant potential for crop improvement in plants.
By the induction and modulation of various cellular processes like DNA methylation, histone modification, and biogenesis of
noncoding RNAs, the plant genome can be activated which can help in achieving a quicker response against various plant
stresses. Epigenetic modifications in plants allow them to adjust under varied environmental stresses by modulating their
phenotypic plasticity and at the same time ensure the quality and yield of crops. The plasticity of the epigenome helps to adapt
the plants during pre- and postdevelopmental processes. The variation in DNA methylation in different organisms exhibits
variable phenotypic responses. The epigenetic changes also occur sequentially in the genome. Various studies indicated that
environmentally stimulated epimutations produce variable responses especially in differentially methylated regions (DMR) that
play a major role in the management of stress conditions in plants. Besides, it has been observed that environmental stresses
cause specific changes in the epigenome that are closely associated with phenotypic modifications. However, the relationship
between epigenetic modifications and phenotypic plasticity is still debatable. In this review, we will be discussing the role of
various factors that allow epigenetic changes to modulate phenotypic plasticity against various abiotic stress in plants.
1. Introduction
The immobile lifestyle of plants exposes them to different
types of biotic and abiotic stresses. Drought, salt, severe
temperatures, nutritional deficits, heavy metal toxicity, and
UV radiation are some of the most common abiotic
stressors. Agricultural production is being threatened by
these unfavorable conditions. To adjust under such variable
conditions, plants undergo consistent changes at the physio-
logical and molecular levels. Epigenetic changes, which
Hindawi
International Journal of Genomics
Volume 2022, Article ID 1092894, 13 pages
https://doi.org/10.1155/2022/1092894
increase plant longevity by improving their tolerance to
stress, provide these productive and viable controls. Various
studies have concluded that heritable phenotypic variations
are not always due to specific DNA sequence alterations,
but the epigenetic regulation that involves certain chemical
modifications at the molecular level can alter the gene
expression [1, 2]. Among the variations induced by normal
DNA sequence variations, epigenetic changes are the
changes resulting from hereditary changes in gene function
acquired during mitotic/meiotic cell division. Nowadays,
epigenetics is defined as the changes in the genome that
occur due to heritable chemical modifications instead of
usual changes in the DNA sequence [3]. Several epigenetic
changes are observed, including modifications to DNA
bases, histones, and noncoding RNAs. In addition, tran-
scription, replication, chromosome condensation/segrega-
tion, and DNA repair mechanism are all affected by
posttranslational modifications. DNA and chromatin modi-
fications at the epigenomic level affect gene expression and
play a prominent role in unveiling phenotypic responses
against external stimuli [4] (Figure 1). This is all due to chro-
matin, a highly organized and compact complex of DNA
and associated proteins. Nucleosome consists of around
200 base pairs of DNA wrapped around octamers of core
histone proteins H2A, H2B, H3, and H4 [5, 6].
Epigenetics refers to the study of heritable phenotypic
modifications that do not involve alterations in DNA
sequence [7]. Plant phenotypic diversity under stress is often
linked to DNA sequence variations. Recently, it was shown
that epigenetic alterations can contribute to phenotypes alone
or in combination through modulating gene expression in
response to stress. When natural populations are subjected
to changes in environmental circumstances, their perfor-
mance might differ. The mechanisms behind one plant’s
stress response may differ from those underlying another [8].
Environmental factors continuously shape postembryo-
nic plant development, resulting in a high level of pheno-
typic plasticity. Although plants cannot escape their
surroundings, they adapt to the changing and unfavorable
growth conditions. The control of gene expression patterns
and epigenetic regulation work together to promote metasta-
ble changes in gene activity. All these factors help the plants
to cope to the unpredictable environments [9]. A potential
link between embryonic environmental factors and diseases
is inherent in epigenetics which suggests that gene expres-
sion is controlled by reversible, heritable changes rather than
inevitable changes to DNA sequences. Most epigenetic
mechanisms regulate gene expression through DNA methyl-
ation, histone modifications, or small noncoding RNAs.
Plants are an ideal system to study epigenetic processes.
Plant reproductive development is associated with DNA
methylation changes. Most of the studies on DNA methyla-
tion come from Arabidopsis thaliana; however, all the plant
genomes undergo methylation where some pathways are
known to predominate while some are defective. The family
of DNA methyltransferases (DNMTs) catalyzes a process
that results in a methyl group being attached to the cytosine
of DNA [10]. The covalent addition of acetyl groups to
lysine residues modifies the histones with increased tran-
scription [5]. Endogenous hormonal signaling also plays a
role in histone modification patterns. Positively charged
lysine residues when acetylated undergo neutralization of
charges. The interactions between the histone and DNA
are weakened, and the opened chromatin is more accessible
to regulators [11]. Histone acetyltransferases (HATs) cata-
lyze lysine or serine acetylation, and histone deacetylases
(HDACs) are responsible for reversing this process. Histone
acetylation is usually linked with gene expression, while
deacetylation is linked with gene repression [12]. H3 phos-
phorylation regulates gene expression and participates in
chromosome condensation/segregation [13]. Both plants
and metazoa phosphorylate conserved residues on histone
H3, such as Thr3, Ser10, Thr11, and Ser28 during interphase
or mitosis, resulting in different mechanisms for activating
transcription [14, 15]. Crop improvement strategies can be
designed using epigenetics, such as selecting the most favor-
able epigenetic states, generating novel epialleles, and
regulating the expression of transgenes. Epigenetic factors
are considered indicators of the transgenerational plasticity
in plants [10]. Epigenetics also acts as a stress memory in
plants, allowing them to cope more effectively with future
stress [1]. An example of epigenetic regulation in plant stress
response is the phenomenon of vernalization where plants
have a memory of prolonged exposure to low temperature
in the winter to flower in the spring [2].
2. Types of Epigenetic Changes in Plants
Plants and animals both rely on epigenetic mechanisms
during their life cycles. Chromatin comfirmation is vital for
the proper regulation of genes and genome activity. DNA
methylation and histone modification in plants are associ-
ated with the modulation of stress-responsive genes. Abiotic
stress can cause chromatin regulators such as acetylation,
methylation, and phosphorylation to regulate gene networks
that respond to stress [16, 17]. It has been reported that his-
tone modifications such as acetylation, phosphorylation, and
ubiquitination enhance gene transcription, while biotinyl-
ation and sumoylation suppress gene expression [4].
Plants undergo epigenetic-based programming during
growth, development, and under stress conditions, which
results in the regulation of gene expression without modifi-
cation of DNA sequences [18]. Acetylation, methylation,
phosphorylation, ubiquitination, and sumoylation are the
various posttranslational modifications of histones. It has
been reported that various environmental stimuli trigger
dynamic epigenetic modifications, which is an essential
mechanism for signal-induced transcription [11] (Figure 2).
3. Acetylation
Histone acetylation occurs when lysine residues on the
histone proteins are added with a negatively charged acetyl
group. A process initiating histone acetyltransferases
(HATs) and histone deacetylases (HDACs) is regulated by
two opposing enzymes. HATs catalyze acetyl group
addition, while HDACs catalyze its removal. A decrease in
histone acetylation results in a chromatin structure that
2 International Journal of Genomics
allows transcription to happen more freely because of its
reduced electrostatic affinity with DNA [19]. Various chro-
matin proteins and transcription factors interact with HAT
or HDAC proteins to control gene expression at specific
genomic or chromatin regions as a consequence of changes
in cellular signaling [20].
Acetylation of histones is a reversible and dynamic
process. It was proposed more than 40 years ago that tran-
scriptional activity is correlated with histone acetylation.
The highly basic nature of amino tails is attributed to the
high content of lysine and arginine amino acids. Conserved
lysine residues are acetylated which neutralizes the positive
charge of histone tails which results in reduced affinity for
negatively charged DNA that in turn promotes the accessi-
bility of chromatin to transcriptional factors [21]. Lysine
acetylation plays an important role in epigenetic processes.
It has evolved as a key posttranslational modification that
can be found at multiple places throughout the cell [22].
Lysine acetylation is one of the major protein posttransla-
tional modifications (PTMs) that is important for many
enzymes catalyzing intracellular metabolism which implies
that protein acetylation has an important role to play in
cellular functions [23]. HATs in plants are divided into four
classes: cAMP-responsive element-binding protein (CBP),
general control nondepressible 5- (GCN5-) related acetyl
transferase (GNAT), MOZ-YBF2/SAS3-SAS2/TIP60
(MYST), and TATA-binding protein associated factor 1
(TAF1). A variety of HATs are involved in acetylating spe-
cific lysine residues, for instance, HAG1 and HAG2 HATs
from the GNAT class catalyze H3K14 and H4K12 acetyla-
tion, respectively. HAM1 and HAM2 belong to MYST class
HATs acetylate H4K5. As distinct HAT molecules recognize
acetylated lysines of histone with different reader proteins,
their specific roles in gene regulation can be reflected by
enzymatic specificities [24]. Based on the subcellular distri-
bution, HATs are grouped into two categories. In the
Stress
Biotic
Abiotic
Impact during development
UBIQUITINATION
Crop improvement
PHOSPHORYLATION
Chromatin modications
HISTONE
ACETYLATION
DNA
(DE)METHYLATION
NON CODING
RNAs
BIOGENESIS
Epigenetic
states
Epigenetic
changes
Regulation of
transgene expression
Epigenetic regulation of gene
expression
Novel
epialleles
Climate smart
crop breeding
Heritable
phenotypic
changes Stress
resistance
Figure 1: Epigenetic changes in plants under stress. Plants withstand various environmental stresses throughout their developmental stages
and to overcome these challenges, epigenetic modifications play a vital role. These include covalent modifications of histone tails
(acetylation, methylation, phosphorylation, ubiquitination, and the small RNA machinery). Epigenetic changes are the heritable
phenotypic variations that are not always due to specific DNA sequence alterations, but the epigenetic regulation that involves certain
chemical modifications at the molecular level which can alter the gene expression. DNA and chromatin modifications at the epigenomic
level affect gene expression and play a prominent role in unveiling phenotypic responses against external stimuli. Epigenetic changes are
reversible and heritable to control gene expression without any change in the DNA sequence. Epigenetics holds immense potential in
crop improvement strategies, climate-smart breeding and stress resistance by choosing the favorable epigenetic states, formulation of
novel epialleles, and regulation of transgene expression.
3International Journal of Genomics
cytoplasm, type B HATs catalyze the acetylation of histone
H4 at lysine 5 and 12, which occurs before the incorporation
of the histone into newly replicated chromatin. HAT of type
B has been described in maize and functions as a heterodi-
mer. In the nucleus, type A HATs play a role in regulating
chromatin assembly and gene transcription by acetylating
nuclear histones [21]. The HDACs are divided into three
different families. The first family is identical to yeast:
reduced potassium deficiency 3 (RPD3), the most widely
studied and found throughout eukaryotes. The second
family, HD-tuins (HDT), is only present in plants and is
originally discovered in maize. The third family, sirtuins, is
structurally distinct and is homologous to the yeast silent
information regulator 2 (Sir2), which is a nicotinamide
adenine dinucleotide- (NAD-) dependent enzyme [25].
Both HDACs and HATs interact with protein complexes
as corepressors and coactivators of transcription or to
modulate DNA accessibility to various types of machinery
through associations with chromatin remodelers. Detailed
studies have been conducted on the HAT and HDAC super-
families in Arabidopsis, rice, and tomato. The HATs and
HDACs play essential roles in plants’response to abiotic and
biotic stresses. For example, they specifically increase acetyla-
tion of histone H4K5 and H3K9 in the promoter and tran-
scribed region of the maize C (4)-Pepc gene in response to
light. In addition to regulating temperature, histone acetyla-
tion is instrumental in the development of plants [26]. The
levels of acetyl-CoA and NAD
+
in the cells play an important
role in the acetylation and deacetylation processes and are
linked to the activity of HATs and HDACs [27]. Plants with
different levels of HAT gene expression display different
drought-resistant traits. HAT genes TaHAG2,TaHAG3,and
TaHAC2 were induced under drought stress in a wheat variety
called BN207, but not in other varieties with lower drought
resistance. Li et al. [28] reported that, in soybean, drought
treatment decreased expression levels of nine GmHDAC genes
(GmHDA6,GmHDA8,GmHDA13,GmHDA14,GmHDA16,
GmSRT2,GmSRT4,GmHDT2,andGmHDT4).
DEMETHYLATION
DEACETYLATION
DEPHOSPHORYLATION PHOSPHORYLATION
ACETYLATION
P
HATs
Lysine
Acetyl
group
HDACs
Kinases
Phosphatases
AC
CHROMOSOME
DNA demethylase
DNA
methyltransferase
Cytosine
N
NH2
NH2
NH2
METHYLATION
5-methylcytosine
Methyl group
N
ON
N
O
CHROMATIN
Figure 2: Various epigenetic modifications include acetylation, (de)methylation, and phosphorylation. DNA methylation involves the
addition of a methyl (-CH
3
) group to the fifth position of cytosine known as methylcytosine (5-mC). This process is carried by DNA
methyltransferases while the demethylation process is aided by DNA demethylase. Acetylation, i.e., the addition of negatively charged
acetyl group to lysine residues on histone proteins is regulated by two opposing enzymes, i.e., histone acetyltransferases (HATs) and
histone deacetylases (HDACs). Acetyl group addition is catalyzed by HATs while the removal of acetyl groups is catalyzed by HDACs.
Phosphorylation is one of the important histone modifications. Histone phosphorylation plays a role in DNA repair, synchronization of
chromosome segregation, and cell division. Histone tails can be phosphorylated by various protein kinases and dephosphorylated by
phosphatases. All the histone modifications lead to the regulation of gene expression.
4 International Journal of Genomics
4. DNA Methylation
DNA methylation is the covalent addition of a methyl (-CH
3
)
group to the fifth position of cytosine known as methylcyto-
sine (5-mC) ring in presence of enzymes DNA methyltrans-
ferases. It is a heritable and reversible process based on
genetic and cellular modification mechanisms like transposon
silencing, tissue-specific gene expression, and genome balance
after polyploidization. DNA methylation corresponds with
transcriptional silencing and typically takes place in DNA
sequences containing cytosines adjacent to a guanine base
(called a CpG site) [29]. In addition to regulating gene expres-
sion, growth, development, and protection against environ-
mental stresses, DNA methylation is important in stabilizing
genomes. Cytosine methylation in plants can occur in all con-
texts of cytosine (CG, CHG, and CHH, where H = A, C, or T).
Different methyltransferases (that function by utilizing S-ade-
nosyl-l-methionine as a methyl donor) are responsible for
DNA methylation, while enzyme-mediated base excision
repair (BER) is responsible for active DNA demethylation.
Different processes initiate, maintain, and remove cytosine
methylation in distinct genomic regions of the plant genome.
The RNA-directed DNA methylation (RdDM) pathway is
involved in de novo cytosine methylation. This pathway
utilizes small-interfering RNAs (siRNAs), scaffold RNAs,
and many accessory proteins. The maintenance of cytosine
methylation is dependent on various DNA methyltransferases.
A set of enzymes (bifunctional 5-methylcytosine DNA glyco-
sylases–apurinic/apyrimidinic lyase (APE1L)) begin the
demethylation process via the BER route during inactive
DNA demethylation [30]. In plants, DNA methylation is cru-
cial for development and to counter biotic and abiotic stresses
[31]. Reportedly, plants infected by pathogens show genome-
wide DNA methylation changes. Roots of soybean and Arabi-
dopsis thaliana infected by cyst nematodes showed widespread
DNA hypomethylation [32, 33]. Recent research has suggested
the importance of DNA methylation in mediating plant stress
responses to abiotic environmental stimuli [34]. During inor-
ganic phosphate starvation, rice plants generate more than 100
differentially methylated regions (DMRs) spanning mostly
CHH hypermethylated transposons near genes responding
to stress and referred to as Pi-starvation-induced (PSI) genes.
Salinity stress in A. thaliana changed the DNA methylation
process, which could be passed on to the next generation pri-
marily via female germlines [35]. Apart from its role in stress
resistance and development, DNA methylation suppresses
harmful DNA sequences, such as retroviral genes, which have
been incorporated into host genomes during evolution [10].
DNA methylation contributes significantly towards
modifying the genome of plants and thus increases their
adaptability and yield as these changes get inherited to the
next generation of plants. Studies have shown that there is
variable DNA methylation within and among the plant in
their natural environments. DNA methylation has been
found to influence several plant traits like flowering time,
seed dormancy, and yield of agronomically important
plants, and therefore, epigenetic changes can help in domes-
tication and evolutionary processes [36]. Modulation during
DNA methylation in plants can be of vital significance to
breeders and molecular biologists to decide the induction
of selective variations in plants through tissue culture and
transgenic approaches. An increased (hypermethylation)
and decrease (demethylation) level of DNA methylation is
seen in response to stress. In comparison to the plants grown
in normal soil conditions, rice and mangrove plants showed
hypermethylation when grown under high salinity. On the
other hand, tobacco infected with tobacco mosaic virus
(TMV) showed hypomethylation, which requires specific
expression of 31 stress-related genes. Drought conditions
led to CG hypermethylation in the pea genome [37].
5. Phosphorylation
In addition to methylation and acetylation, phosphorylation
is one of the important histone PTMs. Histone phosphoryla-
tion plays a role in DNA repair (ɣH2AX) and synchroniza-
tion of chromosome segregation and cell division [9]. The
phosphorylation of histone H2A(X) during DNA damage
cellular response is responsible for the delimitation of large
chromatin domains surrounding the DNA damage site.
Various protein kinases and phosphatases can phosphory-
late and dephosphorylate the acceptor site present at four
nucleosomal histone tails, respectively. Several residues in
histones can be phosphorylated, including serine, threonine,
and tyrosine. Many phosphorylated histone residues are
important for gene expression, e.g., phosphorylating serines
10 and 28 of H3 and serine 32 of H2B appears to be linked
to transcription of genes responding to epidermal growth
factor (EGF) [38]. Phosphorylation is also correlated to
chromosome condensation. When the cell enters mitosis,
the histone H3 is highly phosphorylated. This phosphoryla-
tion is considered to be a crucial step in chromatin conden-
sation and compaction which is an essential criterion for
chromosome congression and segregation through mitosis
and meiosis [39]. Increased salt tolerance in tobacco and
Arabidopsis is attributed to phosphorylation of histone H3,
S10, and acetylation of histone H4 [40]. In Arabidopsis,
MAP kinase MPK3, which is an important component of
stress defense signaling, phosphorylates histone deacetylase
HD2B, leading to reprogramming of defense gene expres-
sion and innate immunity with the result of intranuclear
compartmentalization of HD2B [41]. It has been reported
that abiotic stress response in Arabidopsis led to phosphoryla-
tion of decapping factors. DCP1 is phosphorylated by MAP
kinase 6 (MPK6), and this phosphorylated DCP1 promotes
dimerization and association with DCP2 and DCP5. When
drought stress is present, this interaction enhances decap-
ping activity [42]. In A. thaliana, osmotic stress increases
the phosphorylation of histone H3 threonine 3 (H3T3ph)
in pericentromeric regions where it is believed to help main-
tain heterochromatin structure. There is also evidence that
H3T3ph acts as a repressor on gene expression by antago-
nizing H3K4me3 during osmotic stress [43].
6. Ubiquitination
Ubiquitination is the process in which a ubiquitin molecule
covalently attaches itself to a target molecule. All eukaryotes
5International Journal of Genomics
contain ubiquitin, a 76-amino-acid residue that is highly
conserved among plants, with only two and three differences
between yeast and human homologs. Signaling molecules
like ubiquitin regulate cellular homeostasis and trigger a
variety of cellular processes. The monoubiquitination
process involves linking the target molecule with the C-
terminal residues of one of the eight ubiquitin residues
(Lys6, Lys11, Lys27, Lys29, Lys33, Lys48, Lys63, and
Met1). On the other hand, the attachment of multiple ubiq-
uitin molecules to other lysine residues of the same substrate
is called multiubiquitination [44]. Ubiquitin-conjugating
enzyme E1 transfers active ubiquitin to ubiquitin-
conjugating enzyme E2, and then E3 (ubiquitin ligase)
deposits the active ubiquitin onto the target protein (usually
on a lysine residue). Polyubiquitin substrates are degraded
via 26S proteasome while monoubiquitination (ub) or short
ub-chains are usually degraded via the lysosome. A group of
proteins known as ubiquitin-deconjugating enzymes are
responsible for deubiquitination. The deubiquitinase super-
family (DUB), one of the biggest superfamilies works antag-
onistically to the action of E3 ligases. The processes of
ubiquitination and deubiquitination play a vital role in many
processes such as cell homeostasis, signal transduction,
transcriptional gene regulation, protein degradation, and
endocytosis [45]. Ubiquitination can regulate transcription
by being either an active or repressive marker. Genes with
trimethylated H3K4 and H3K36 (H3K4me3 and
H3K36me3) and those with monoubiquitinated H2B
(H2Bub) are often active. A RING E3-ligase called HUB1
and HUB2 is responsible for H2B histone monoubiquitina-
tion. In addition to controlling flowering time, the cell cycle,
seed dormancy, and the circadian clock, these ligases also
protect against necrotrophic fungal pathogens [46]. Epige-
netic control is also extended by ubiquitination and deubi-
quitination of histone proteins. A plant cell’s chromatin is
turned on by monoubiquitination for downstream cellular
activation processes. Upon deubiquitination by deubiquiti-
nating proteins, ubiquitin is detached from histones and
gene expression is repressed and downstream processes are
inactivated [18]. In Arabidopsis, the transcription factor,
WRKY34, promotes the expression of the ubiquitin E3
ligase, CULLIN 3A, thereby resulting in proteasomal degra-
dation of FRIGIDA (FRI) and thereby leading to the
accumulation of long noncoding RNA (lncRNA) and cold-
induced long antisense intragenic rna (ColdAIR) in the late
phases of vernalization. High ColdAIR levels reduce
H3K4me3 in FLC (flowering locus C) facilitating flowering
after vernalization [47]. U-box E3 ubiquitin ligase TaPUB1
enhances salt stress tolerance in wheat by upregulating the
expression of genes related to ion channels and genes that
improved the antioxidant capacity of plants under salt stress
[48]. Moreover, the membrane-bound E3 ubiquitin ligase
gene BnTR1 isolated from Brassica napus contributes to
the development of thermal resistance in plants by regulat-
ing calcium channels and heat shock proteins [49].
Ubiquitin-specific protease (USP) protein families are
involved in protein deubiquitination. In Arabidopsis, these
participate in ABA signaling, drought and salt tolerance,
nutrient deficiency response, and immunity regulation [50].
7. Small RNA Machinery
The plant genome encodes an array of small RNAs that are
involved in the development, reproduction, and reprogram-
ming of the genome, besides contributing to its phenotypic
plasticity. Small RNAs play a significant role in both defense
and epigenetic responses, according to recent research.
DICER-like proteins (DCLs) help create small RNA mole-
cules by synthesizing 21–24 nucleotide RNA molecules. In
plants, small RNAs are divided into microRNA (miRNA)
and small interfering RNA (siRNA) by their origin, struc-
ture, and pathways they regulate. Endogenous siRNAs in
plants can be classified into several major groups, i.e.,
hairpin-derived siRNAs (hp-siRNAs), transacting siRNA,
natural antisense siRNAs (natsiRNAs), secondary siRNAs,
and heterochromatic siRNAs (hetsiRNAs). Plants modify
all small RNAs at the 3′end by 2′omethylation, including
microRNAs. To enhance stability and prevent degradation
following 3′uridylation, modification is essential. A miRNA
participates in posttranscriptional gene silencing in plants by
cleaving transcripts or repressing translation. Many siRNAs
are involved in PTGS, but a majority of them are involved
with RNA-directed DNA methylation (RdDM) and tran-
scriptional gene silencing (TGS) [37, 51, 52]. RdDM is the
de novo methylation caused by double-stranded RNA (ds-
RNA) molecules. The interrelation between RdDM and
RNA interference (RNAi) suggests that small RNAs guide
cytosine methylation. RdDM pathways help in adaptation
responses to various stresses, maintaining genome stability
and regulation of development [37]. Small RNAs and long
noncoding RNAs (lncRNAs) have come out as key regula-
tors of chromatin structure in eukaryotic cells. In addition
to RNA degradation, translational suppression, chromatin
modification, and RNA interference (RNAi) pathways, small
RNAs are also involved in targeted gene expression. Nuclear
RNAi pathways repress transcription through histone or
DNA methylation. Using A. thaliana as a model system,
scientists first demonstrated that DNA methylation of target
genes, as well as posttranscriptional gene silencing, was asso-
ciated with small interfering RNA (siRNA) production, link-
ing RNA-directed DNA methylation to the RNAi pathway
[53]. Researchers have reported that a 24-nt siRNA in Ara-
bidopsis is involved in downregulating P5C dehydrogenase
(P5CDH) expression via mRNA cleavage, resulting in a
decrease in proline degradation and an increase in prolines
accumulation and salt stress tolerance [4].
8. Epigenetic Modifications under Different
Stress Conditions
The persistent transmission of many DNA sequence alleles
has long been linked to the heritable foundation of complex
characteristics acquired or maintained in plants under stress
[54]. Allelic DNA variation may be altered by mutations,
influencing the genetic architecture and how these alleles
are expressed. The recent discovery that diversity in chroma-
tin states is abundant in experimental and wild populations
and may constitute an additional source of phenotypic vari-
ation has called into question the traditional idea that DNA
6 International Journal of Genomics
alleles are the only cause of phenotypic variation [55, 56]. A
plant’s chromatin state can be altered rapidly and irrevers-
ibly by DNA methyltransferases inserting methyl groups in
cytosine, acetylation and methylation of N-terminal histone
tails to promote chromatin remodeling, and small RNA
mechanisms that prevent population diversification due to
excessive rearrangements [57, 58]. Epigenetic alterations are
those that modify DNA activity without changing its underly-
ing nucleotide structure [59]. Because epigenetic alterations
may be triggered by environmental cues and passed down to
future generations, they may add another layer of complexity
to heritable phenotypic diversity and the evolutionary poten-
tial of wild populations [60]. Various epigenetic processes
and the associated genes under different stress conditions are
mentioned in Table 1. Epigenetics plays a vital role in crop
improvement. The epigenetic modifications induced in vari-
ous crop species have resulted in crop improvement. Table 2
summerises some of these modifications.
9. Epigenetic Modifications under Salt-
Induced Stress
Environmental pressures cause DNA methylation to be
either hyper or hypo. Research studies suggest that epige-
netic processes play a major role in altering genes under
adverse conditions. Under salt-induced stress, methylation
of promoters and gene bodies helps control gene expression
in a genotypically and organ-specific manner. It has been
demonstrated that salt stress manifests itself in soybean by
altering the expression of several transcription factors. In
their study, Song et al. [61] speculated that DNA methyla-
tion and histone modifications could function collectively
to affect stress-inducible genes. Furthermore, Ferreira et al.
[62] suggest that salt stress may alter the expression of
DNA demethylases leading to hypomethylation. Likewise,
the salt-resistant wheat cultivar SR3 as well as its progenitor
HBP1 showed opposing changes in cytosine methylation
patterns when exposed to salinity-induced stress. A specific
gene for demethylation was found to be effective during epi-
genetic processes in rice roots in response to salinity stress
[63]. Salt stress may cause changes in the expression levels
of high-affinity potassium transporters whose expression is
controlled by genetic and epigenetic processes in wheat [64].
Changes in chromatin structure play a key role to impart
salinity tolerance in many crop plants. According to Kaldis
et al. [65], the transcriptional adaptor ADA2b is responsible
to induce hypersensitivity in Arabidopsis thaliana under salt
stress. Consequently, salt stress impacts both genome-wide
DNA methylation and histone changes, and both these pro-
cesses are related to one another for enabling coordinated
salt stress response [66]. DNA methylation was shown to
be higher in the shoots of salt-sensitive and salt-tolerant
wheat genotypes, ranging from 30 to 40%, as compared to
that in roots [67, 68]. Under salt stress, DNA methylation
was shown to be higher in sensitive genotypes when com-
pared to intolerant genotypes in rape seeds [69].
Under abiotic stressors such as salt, DNA demethylation
in tobacco generates the NtGPDL gene (glycerophospho-
diesterase-like protein). Likewise, salt stress in rapeseed
induces cytosine methylation at CpCpGpG sites increased,
with methylation and demethylation. The enzymes involved
in the process are histone deacetylases (HDACs) and histone
acetyltransferases (HATs) [57]. Plants exhibit altered
responses to salt when HDAC activity occurs, and HDAC
toxicity inhibits the activity of HAT complexes [20, 70].
There was a discovery that sRNAs were associated with
hypermethylated areas [71].
10. Epigenetic Changes under Drought-
Induced Stress
Research on the stress biology of plants has mostly focused
on elucidating regulatory mechanisms at the complex
molecular levels in plants exposed to a variety of environ-
mental constraints. Drought-induced gene expression is
primarily regulated by histone alterations and nucleosome
density in the promoters and ORFs of the OR genes [72].
Histone changes such as H3K4me3 and H3K9ac were found
in the Rd20 and Rd29A regions under drought stress com-
pared to optimal conditions [73].
A thorough examination of the postdrought stress heal-
ing process demonstrated rapid deacetylation at the
H3K9ac sites, preceded by the ultimate clearance of RNA
polymerase II from such areas. Rd29A, Rd20, and Arabidop-
sis galactinol synthase were the genes implicated in such
substantial chromatin shifting (AtGOLS2). However,
H3K4me3 was eliminated slowly than H3K9ac with larger
rehydration dosages [1]. An elevation in H3K4 trimethyla-
tion and H3K9 acetylation on the gene promoter, as well
as H3K23 and H3K27 acetylation on the coding sections,
was shown to be crucial for drought-induced transcription
of stress-sensitive genes in A. thaliana [74]. By boosting
H3K4me3 modification, the Arabidopsis trithorax-like 1
HMT increased the overexpression of the gene encoding
the ABA biosynthesis enzyme, 9-cis-epoxy carotenoid diox-
ygenase, notably under drought stress [75].
DNA methylation demonstrates tissue selectivity during
drought stress. Drought caused a total of 12.1% methylation
changes in Oryza sativa, which were accounting across
different tissues, genotypes, and life stages. The total DNA
methylation rate in roots was lower than those in leaves at
the same developmental period, indicating that roots play a
key role in water deficiency [76]. The connection between
DNA methylation and drought stress resistance has been
demonstrated in rice cultivars IR20, a drought vulnerable
variety, exhibits hypomethylation under drought conditions,
while the resistant variants exhibit hypermethylation [77].
11. Epigenetic Modifications under Heat-
Induced Stress
Heat stress is principal to abiotic stress in plants, with dis-
tinct negative effects on plant development, physiology,
and metabolism [78]. Heat, like other stressors, causes epige-
netic changes in plants. Such adaptations enable the plants
to cope up with heat stress. Several studies have suggested
the role of these changes in plants against heat stress. Heat
stress causes greater methylation and frequent occurrence
7International Journal of Genomics
of homologous recombination in Arabidopsis plants [79]. In
response to heat stress, DRM2, nuclear RNA polymerase D1
and NRPE1 overexpression may result in enhanced genome
methylation in Arabidopsis [80]. Cork oak (Quercus suber
L.) cultivated at 55
°
C shows an increase in global methyla-
tion [81]. In Brassica napus, the heat-sensitive genotype
exhibits higher DNA methylation levels than the heat-
tolerant genotype following heat stress [82].
In developing rice seeds, mild heat stress at 34
°
C for 48
hours reduces the DNA methylation level of fertilization-
independent endosperm1 (OsFIE1), a member of polycomb
repressive complex 2 (PRC2), and represses the transcript
abundance of OsCMT3, which may contribute to OsFIE1
misregulation [83].
The expression of lysine-specific histone demethylase 1
(LSD1), which is involved in the demethylation of histone
H3 lysine 4 (H3K4) me1/2, ribosomal RNA FtsJ-like methyl-
transferase, has increased in heat stress primed second-
generation plants. This demonstrates that some epigenetic
markers stimulate genes in the offspring of primed plants
to produce tolerance. [84].
A histone variant H2A.Z induces transcriptional alter-
ations in stress-responsive genes at high temperatures [16].
In Arabidopsis thaliana, mutations in the GCN5 gene, which
encodes histone acetyltransferase, reduced transcriptional
activation of heat stress-sensitive genes including HSAF3
and MBF1c resulting in Arabidopsis thaliana thermal vul-
nerability [85]. Furthermore, brief heat stress stimulated
heat shock protein 101 (HSP101) expression in Arabidopsis,
but expression dropped after repeated brief stress treat-
ments, indicating that the plant epigenome is suited to
recover from temperature stress [86].
12. Epigenetic Modifications under Cold-
Induced Stress
Cold stress has been recognized as a major environmental
issue limiting agricultural growth and productivity especially
Table 1: Different epigenetic processes and the associated genes.
Epigenetic process Gene/enzyme Function Plant Reference
DNA methylation Asr1 and Asr2 Drought stress tolerance Tomato [99]
Demethylation and
hypomethylation Glyma11g02400 Salinity tolerance Soybean [61]
Histone modification OsHAM701 Drought stress tolerance Rice [28, 100]
Histone modification OsHAC701 Heat stress tolerance Rice [101, 102]
Histone modification AtABO1 Drought and oxidative stress
tolerance Arabidopsis [103, 104]
Histone modification AtATX1/HvTX1 Drought stress tolerance Arabidopsis and
barley [75, 105]
Hypomethylation NtGPDL Cold tolerance Tobacco [106, 107]
MicroRNA miR170, miR171 and
miR172 Drought tolerance Wheat/millet [108, 109]
Table 2: Epigenetics for crop improvement.
Species Epigenetic modification Crop improvement Reference
Arabidopsis and
tomato MicroRNA Enhanced plant vigor and phenotypes [102]
Arabidopsis, rice and
maize DNA methylation Development of new molecular markers [81]
Arabidopsis Induced expression of miR156 and miR396 Salt stress response [110]
Arabidopsis Induced expression of miR393, miR397b, and
miR402 Response to water deficiency [111]
White clover DNA methylation Stress memory phenomenon [112]
Spinach and
Arabidopsis DNA methylation Artificial induction of flowering [113]
Maize DNA methylation Defense priming to herbivores and increase
plant defense [114]
Rapeseed and barley Histone modifications Favoring acceleration of crop breeding [115]
Soybean DNA methylation Protective mechanism and seed development [116]
Rice DNA methylation Artificial crossings [117]
Rice Downregulation of miR319c, miR164c, miR319b,
and miR1861d Response to drought [118]
8 International Journal of Genomics
in steep terrain [87]. Reduced temperature impairs plant
development physiology by causing chilling ailments such
as photosynthetic apparatus damage, chlorosis, tissue death,
loss of membrane integrity, and eventually wilting [88].
Under cold stress, the expression of epigenetic regulators
fluctuates [1]. During cold acclimation, Zea mays showed
increased expression of histone deacetylases (HDACs). As
a result, the lysine residues on the histone subunits H3 and
H4 were deacetylated [89]. HOS15, a WD40-repeat protein,
functions to control gene expression through histone
deacetylation in chromatin. HOS15 interacts specifically
with and promotes deacetylation of histone H4, indicating
that chromatin remodeling plays an important role in gene
regulation in plant responses and tolerance to abiotic
stresses [90]. HOS15 interacts with histone deacetylase 2C
(HD2C) and both proteins together associate with the pro-
moters of cold-responsive COR genes, COR15A and
COR47. Cold-induced HD2C degradation is mediated by
the CULLIN4- (CUL4-) based E3 ubiquitin ligase complex
in which HOS15 acts as a substrate receptor [91].
An alternative splicing pathway involving histone
demethylase, Jumonji C domain-containing gene (JMJC5)
was discovered in Medicago truncatula [92]. When Arabi-
dopsis plants were exposed to low-temperature stress condi-
tions, they exhibited enhanced H3T3ph and H3K4me3 at
genome level but low histone H3 occupancy at the pericen-
tromeric regions [93]. Throughout the chilling and freezing
phases, rapid changes in cytosine methylation occurred
[94]. miR6445a stability was modulated by signature meth-
ylation in P. simonii subjected to cold, salt, osmotic, and heat
stressors [95]. As a result of cold treatment, Gossypium hir-
sutum exhibited a decrease in DNA methylation and an
increase in the expression of trehalose-6-phosphate
synthase-like gene, associated with plant defense [96]. The
DNA methylation of cold-response defense genes, including
HbICE1, was altered in Hevea brasiliensis following cold
treatment [97], suggesting that low-temperature response
machinery involves regulation of defense-related genes via
DNA methylation changes. Under brief cold stress, patterns
of whole-genome demethylation were also discovered in Zea
mays, allowing transposons and stress-responsive genes to
be modulated [98].
13. Conclusions
A rapidly growing population and climate change have pre-
sented several challenges to agricultural and food production
worldwide. We might be able to achieve sustainable agricul-
tural output if we understand plant stress responses and
create new tactics of protecting plants. Through epigenetic
adjustments, plants may be able to adapt under variable
biotic and abiotic stress factors. Cellular alterations, for
instance, DNA modifications, chromatin changes, small
RNA pathways, and DNA methylation, all work together
to regulate the expression of stress-responsive genes in
plants under different stress conditions. Various abiotic
stresses can now be controlled epigenetically to enable
diverse plant species to adjust under different sets of condi-
tions. Epigenetic methods have been applied in a variety of
crops. The use of epigenetics may be another method of
developing defensive mechanisms in plant species exposed
to a variety of environmental challenges. There is certainly
a need for more research in this promising field to make it
viable and widely applicable. The development of markers
to track epigenetic changes, the durability of priming, and
advances to understand multiple stresses that plants encoun-
ter in their lifetime are all essential to optimize its applica-
tion in crop protection programs in the future.
Disclosure
This is a review paper that has been collectively written.
Conflicts of Interest
The authors declare no conflict of interest among them.
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