Review Article Epigenetic Dynamics: Role of Epimarks and ...downloads.hindawi.com/journals/ijg/2014/187146.pdf · Review Article Epigenetic Dynamics: Role of Epimarks and Underlying

Review ArticleEpigenetic Dynamics Role of Epimarks and UnderlyingMachinery in Plants Exposed to Abiotic Stress

Manoj Kumar Dhar1 Parivartan Vishal1 Rahul Sharma1 and Sanjana Kaul2

1 Plant Genomics Laboratory School of Biotechnology University of Jammu Jammu 180006 India2 School of Biotechnology University of Jammu Jammu 180006 India

Correspondence should be addressed to Manoj Kumar Dhar manojkdharrediffmailcom

Received 16 May 2014 Revised 28 July 2014 Accepted 7 August 2014 Published 18 September 2014

Academic Editor Henry Heng

Copyright copy 2014 Manoj Kumar Dhar et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Abiotic stress induces several changes in plants at physiological and molecular level Plants have evolved regulatory mechanismsguided towards establishment of stress tolerance in which epigenetic modifications play a pivotal roleWe provide examples of geneexpression changes that are brought about by conversion of active chromatin to silent heterochromatin and vice versa Methylationof CG sites and specific modification of histone tail determine whether a particular locus is transcriptionally active or silent Wepresent a lucid review of epigenetic machinery and epigenetic alterations involving DNA methylation histone tail modificationschromatin remodeling and RNA directed epigenetic changes

1 Introduction

Stress is inevitable in the life cycle of living organisms Beingsessile plants are more prone to the deleterious effects of en-vironmental stress Depending upon whether the factorsinvolved are living or nonliving environmental stress can becategorized as biotic (plant pathogens etc) or abiotic stress(drought salinity chilling etc) Stressful conditions gener-ally do not occur as isolated events but as crosstalk ofmultiplestresses Therefore plants have developed complex mecha-nisms to survive under these challenging conditions Tol-erance avoidance and resistance are three major strategiesfollowed by plants to counter the recurring biotic and abioticstresses These mechanisms involve genes associated withseveral interconnected pathways which lead them towardsbetter stress tolerance [1] Plants resort to various modifica-tions in their morphological traits physiology and so forthin response to stress

Depending uponwhether the stress is permanent or tran-sitory plants respond through various short term as well aslong term strategies Short term strategies include alterationin the plant homeostasis Restoration of cellular homeostasisreduces stress injury by eliminating consequences of stresswhich leads to development of stress tolerance Long-term

strategies include transgenerational changes involving devel-opment of heritable gene expression changes This comprisescreation of new epigenetic marks while erasing old ones andincreasing the expression of some genes while silencing someother genes Severe and prolonged stress can lead to genomealterations which may sometimes contribute towards betteradaptation [2] The basic information guiding the behaviorof plant lies in the DNA sequence and alterations in DNAsequence by mutation or genetic recombination lead to newalleles which may confer enhanced stress tolerance to theplant However the rate of formation of new gene combina-tions is too slow in comparison to the occurrence of differentstresses in the environment [3] Therefore the survival ofplant in these conditions depends largely on the regulationof various stress responsive genes that is epigenetic mech-anisms Epigenetic changes include any heritable change inan organism which does not involve change in the DNAsequence Rather it involves addition or deletion of epimarks(methylation etc) on DNA posttranslational modificationson histone tails (acetylation methylation sumoylation etc)and RNA interference

Histone modifications and alterations in DNA methy-lation are together referred to as epigenetic regulation butonly those changes which are either mitotically ormeiotically

Hindawi Publishing CorporationInternational Journal of GenomicsVolume 2014 Article ID 187146 10 pageshttpdxdoiorg1011552014187146

2 International Journal of Genomics

heritable are truly epigenetic [4]These alterations affect geneexpression by chromatin remodeling which involves changein chromatin state of the chromosome that is euchromatinor heterochromatin For instance in order to increase theexpression of a particular gene its promoter sequence mustbe exposed so that transcription factor and RNA polymerasecould bind to the underlying upstream DNA and carryouttranscription of the gene In order to expose the DNA forefficient transcription nucleosome complex must be untan-gled Conversely for shutting off gene expressionDNAmeth-ylation has to be reestablished followed by packaging of theDNA stretch covering that particular gene by the histonecomponents of the nucleosome complex

2 Epigenetic Alterations andRequisite Machinery

21 DNAMethylation Methylation is the only covalentmod-ification that has been identified on DNA till date [5] Itinvolves addition of methyl group (minusCH

3) at fifth carbon in

the cytosine ring of theDNAmolecule at CpG CpNpG (sym-metric) or CpNpN (asymmetric) sites (whereN isA C or T)

MechanismofDNAmethylation is governed by two typesof enzymes

(i) methyltransferases(ii) demethylases

Two major enzymatic activities regulate cytosine methy-lation in plants which involve de novo establishment of meth-ylation on DNA and maintenance of the already methylatedDNA The de novo methylation is a process by which pre-viously unmethylated cytosine residues are methylated lead-ing to the formation of new methylation patterns Mainte-nance methylation is the process of maintenance of preex-isting methylation patterns after DNA replication [6] MET1(DNAmethyltransferase 1) and CMT (chromomethylase) areresponsible for maintenance of CG and CNG methylationrespectively [7]De novomethylation is established by DRM2(domains rearranged methyltransferase 2) in the new DNAsequences generated after DNA replication DNA gycosylases(ROS1 DML2 DML3 and DME) catalyze the removal ofmethyl group from cytosine residue [8]

Genome-wide analysis of DNAmethylation in Arabidop-sis thaliana revealed the methylation status of its genome as24CG 67 CNG and 17 CNNmethylation [9] CpNpGand CpNpN methylation changes mediated by CMT3 andDRM2 have been reported to regulate transposons and repeatregions through chromatin remodelling during exposure tostress [10 11]

DNA methylation is distributed in the plant genomeincluding heterochromatic and euchromatic regions [12]Theheterochromatic regions densely packed with transposableelements and other repetitive sequences are highly methy-lated whereas euchromatic regions containing genes andnonrepetitive intergenic regions show comparatively lessercytosine methylation Interestingly transposons are methy-lated along their entire length in contrast to genes which areoften methylated away from the start and termination sites

Within the euchromatic region pseudogenes and transcrip-tionally inactive genes show higher levels of methylation thanactively expressing genes [13] Expressed genes are methy-lated in the transcribed region (gene-body methylation) [14]Gene bodymethylation exhibits a parabolic relationship withtranscription level in rice and Arabidopsis Both the leastexpressed and the highly expressed genes are least prone tomethylation whereas moderately expressed genes are mostlikely to be methylated at gene body [15 16] Genic regionsdo not contain non-CG methylation while transposons andrepeats abundantly possess CpNpG or CpNpN methylationMethylation at 51015840 portion (promoter plus some transcribedregion) and 31015840 portion inhibits gene expression

Stress can cause hypermethylation or hypomethylationof DNA In maize roots cold induced expression of ZmMI1was accompanied with a decrease in DNAmethylation whichdid not revert to basal level even after 7 days of recoveryIn tobacco aluminium salt cold and paraquat stresses in-duced DNA demethylation at CG nucleotides in the codingsequence of NtGPDL gene (glycerophosphodiesterase-likeprotein) [17] Heavy metal stress is known to induce hypo-methylation at specific sites in the genome of both the metal-sensitive Trifolium repens L and metal-tolerant Cannabissativa L [18] DNA hypermethylation at CG but not CNGat two heterochromatic loci was induced in cell suspensionculture of tobacco by osmotic stress [19] Drought-inducedhypermethylation has been proposed to play a primary anddirect role in reducing the metabolic activity in pea root tipsafter 72-hour water deficit [20 21] Suji and Joel [22] reporteddrought induced hypermethylation and hypomethylation indrought tolerant and drought susceptible varieties of ricerespectively Stress induced hypermethylation of satelliteDNA was associated with a switch in photosynthesis modefrom C3 to CAM in Mesembryanthemum crystallinum L afacultative halophyte [23]

Promoter demethylation is known to abolish constitutivegene silencing established because of hypermethylation ofXa21G gene thereby conferring disease resistance in rice [24]Changed methylation level in maize exposed to osmotic andsalt stress helps in stress acclimation [25] Stressful environ-ment produces transgenerational epigenetic modificationsleading to enhanced stress adaptability in future progenies[26] Nonstressed progenies of stressed rice plants carryingmodified methylation patterns acquired from the parentexhibit enhanced stress tolerance [27]

Transposons and other repeats constitute large part of theplant genome and cytosine methylation is chiefly targetedtowards transposon silencing [28 29] CG and non-CGmethylation contribute towards transposon immobilizationIn plants non-CG methylation is proposed to have evolvedas an epigenetic tag committed to transposon control [30]A close relationship between methylation and low temper-ature dependent transposition (LTDT) has been reportedwhere low temperature caused reduction inmethylation levelopposed to hypermethylation resulting from higher temper-ature in Antirrhinum majus [31] Transposon methylationchanges which control transposition activity of transposonsare also reported to spread silencing signal to neighboring

International Journal of Genomics 3

H3H4 H2B

H2A

RNA Pol

mRNA

Active chromatin

UMUM

UM

UM

UM UM

UM

Unmethylated CpGs

A AA

M3

M2

M1

4 9 23 27

ARTKQTARKSTGGKAPRKQLATKAARKSA

Figure 1 Epigenetic marks associated with transcriptionally active chromatin Trimethylation at K4 and acetylation at K9 K23 and K27 ofH3 and unmethylated CGs signify active chromatin

genes Tos17 methylation spreads to upstream ABC-trans-porter-like gene [32]

22 Histone Code Histones are very crucial for packagingof DNA DNA folds around histone octamer (H2A H2BH3 and H4) to form nucleosome which is the basic unitof chromatin The organization of chromatin is critical fortranscription and many other cellular processes like replica-tion repair recombination and so forthThis organization isdirectly influenced by posttranslational modifications in thehistone tails protruding out of their amino terminal The his-tone tails are reported to interact with negative charge on theDNA and other associated proteins [33] These interactionsare altered by certain posttranslationalmodifications targetedtowards specific amino acid residues and depending upon theposttranslational modification on histone tail the integrity ofnucleosome in that region is determinedThesemodificationsinclude methylation acetylation phosphorylation ubiquiti-nation biotinylation and sumoylation at specific amino acidresidues [34] A combination of site-specific posttranslationalmodifications on different residues of histone tail consti-tutes ldquohistone coderdquo Each modification signifies a particularchromatin state and regulates transcriptional activity incombination with different external and internal signals

23 Modifying Enzymes Histone acetyltransferases (HATs)carry out acetylation of histone tails and are associated withgene activation HATs transfer acetyl group to 120576-amino groupof lysine residues in the N-terminal extensions of nucleoso-mal core histones

Lysine (K) bears positive charge and the transfer of acetylgroup neutralizes this positive chargeThis reduces the affini-ty of nucleosome complex for DNA leading to relaxed chro-matin state and subsequent transcriptional activation About

15 HATs have been reported in Arabidopsis which belong tothree families GNATMYST CBP and TF II250 [35] HATsinteract with TFs and activate stress responsive genes whichregulate stress tolerance SAGA (HAT) interacts with ADA1(TF) and the SAGAADA1 complex interacts with CBF1which recruits this complex to activate downstream genes forbetter cold tolerance [36]

Histone deacetylases (HDACs) are responsible for deacet-ylation that is removal of acetyl group fromhistones leadingto condensed chromatin state and thereby causing genesilencing [37] HDACs are further divided into three families[38] namely (a) RPD3 family (b) SIR2 family and (c) HD2family Both HATs andHDACs affect the expression of devel-opmental and stress responsive genes

HMTs (histone methyl transferases) and HDMs (histonedemethylases) are responsible for methylation and demethy-lation of histone tails respectively

Histone methylation occurs at lysine and arginine aminoacids All lysine methylations are carried out by HKMTs(histone lysine methyltransferases) containing SET domain[39] They are classified in to five classes Class I to Class V(Table 1)

Histone Demethylases (HDMs) There are two types of de-methylases which carry out oxidative demethylation of his-tones (Table 2)

24 Histone Modifications

241 H3K Acetylation Acetylation of lysine residues is veryflexible and plays a vital role in the life cycle of plants [7]Active chromatin is marked by H3 acetylation resulting inrelaxation of chromatin state which facilitates the transit ofRNA polymerase [42] (Figure 1) Histone lysine acetylation


Table1Differentclasses

ofhisto

nemethyltransferases(HMTs)

ClassI

ClassII

ClassIII

ClassIV

ClassV

SUVH

SUVR

Mem

bers

Thesea

reho

mologueso

fE(Z)

(enh

ancero

fzeste

from

Drosophila

)three

E(Z)-like

proteins

are

encodedby

Arabidopsis

geno

me

CURL

YLE

AF(C

LF)

MED

EA(M

EA)

SWIN

GER

(SWN)

Thiscla

ssis

constituted

bySD

G8

SDG4

Thiscla

sscontains

homologueso

fTritho

rax

thereforemem

bersare

calledAT

X(Arabidopsis

Trith

orax-like)p

roteins1ndash5

Five

genese

ncod

eTrithorax

homologuesAT

X1ndash5

Arabidopsis

has

twomem

bers

belong

ingto

this

classA

TXR5

and

ATXR

6

SUVH(SU(VAR3-9))

Tenplantspecific

mem

bers

[SU(VAR)

3-9related]

Dom

ains

Con

tainsS

ET(sup

pressor

ofvarie

gatio

nenhancer

ofzeste

andTrith

orax)

domain

E(Z)

domain

SANTdo

main(SW13

ADA2NCO

Rand

TFIIIB-binding

)and

CXC(cysteiner

ichregion

)

Con

tain

SETdo

main

andAW

Smotif

(associatedwith

SET)

Con

tain

SETpo

st-SE

Tdo

main

PHD(plant

homeodo

main)

PWWP

(prolin

e-tryptoph

an-

tryptoph

an-prolin

e)

FYRN

(FY

rich

N-te

rminus)and

FYRC

(FY

rich

C-term

inus)

Con

tain

SET

domainandPH

Ddo

main

Con

tain

SETdo

main

pre-SE

Tdo

main

post-

SETdo

main

and

SRA(SET

andRING

fingera

ssociated

domain)

Con

tain

allother

domains

except

SRA

domain

somem

embersare

repo

rted

topo

ssessa

novelW

IYLD

domainsim

ilarto

DNA-

bind

ingprotein

Role

CLFhelpsinflo

weringtim

eregu

latio

nMEA

isinvolved

inseed

developm

ent

SWNisrequ

iredforfl

ower

developm

ent

SDG8isinvolved

inFL

Cexpressio

nwhich

regu

lates

flowering

time

SDG4isinvolved

inprop

erpo

llenand

stam

endevelopm

ent

Involved

indrou

ghtstre

ssrespon

seatx1m

utantis

hypo

sensitive

todehydration

Play

rolein

cell

cycle

regu

lation

Markinactiv

echromatingene

silencing

Potentialrolein

heterochromatic

siRNAprod

uctio

nmachinery

EpigeneticRo

leTh

eyhave

H3K

27methyltransfe

rase

activ

ity

They

carryou

tdi-or

trim

ethylatio

nof

H3K

36

ATX1

andAT

X2are

involved

inH3K

4me3

and

H3K

4me2

Functio

nof

ATX345is

stillno

tkno

wn

They

carryou

tmon

omethylatio

nof

H3K

27

H3K

9methylatio

ndifferent

SRAdo

mains

have

preferentia

laffinity

ford

ifferentcytosine

methylatio

ncontext

(sym

metric

orasym

metric

)

Functio

nun

clear

yet

howeveritresem

bles

proteins

involved

inheterochromatin

form

ation


Table 2 Types of Histone demethylases (HDMs)

Lysine specific demethylase 1 (KDMLSD1) Jumonji C domain containing proteins (JmjC)Require flavin as cofactor Require Fe(II) and 120572-ketoglutarate as cofactorsRemove methyl group from mono- and dimethylatedlysines on histone tails Remove methylation from mono- di- and trimethylated lysines

Four KDMLSD1 demethylases in ArabidopsisFlowering locus D (FLD)LSD1 like (LDL1)LDL2LDL3

Twenty one JmjC-domain proteins are reported in Arabidopsis which areclassified into 5 subfamiliesKDM5JARID1 groupKDM4JHDM3 groupKDM3JHDM2 groupJMJD6 groupJmjC-domain only

FLD LDL1 and LDL2 are involved in flower inductionin Arabidopsis through flc repression

KDM4JHDM3 proteins along with ELF6JMJ11 (early flowering 6) andREFJMJ12 (relative of early flowering) control flowering time (Yu et al2008) [40]whereas KDM3JHDM2 protein for instance IBM1JMJ25 (increase inbonsai methylation) protects active genes from ectopic H3K9me2 andCNG DNAmethylation [41]

rearrangement has been reported to be associated with flow-ering [43] and cold stress tolerance [44] HDA6 and HDA19expression is induced by stress and affects local chromatinstructure HDA6 has been reported to be responsible fordeacetylation of histones in response to biotic and abioticstress induced by jasmonic acid and ethylene in ArabidopsisOverexpression of AtHD2C in transgenic Arabidopsis resultsin increased expression of ABA-responsive genes (LEA) lead-ing to improved salt and drought stress tolerance [45] Hos15protein interacts with H4 and carries out H4 deacetylationthereby regulating stress tolerance in Arabidopsis [44]

H3K4me3 and H3K9 acetylation on promoter regionand H3K23 acetylation and H3K27 acetylation on codingregion affect gene expression of stress responsive genes [35]Four drought responsive genes (RD29A RD29B RD20and RAP24) have been reported to exhibit enrichment ofH3K4me3 and H3K9 acetylation and activation in responseto drought stress Moreover there is a gradual decreaseof nucleosomal density on RD20 and RAP24 genes underdrought stress [35]

242 H3K Methylation H3 lysine methylation is the mostabundant histone modification Lysine can be mono- di- ortrimethylatedH3K9methylation is a characteristic of hetero-chromatin and signifies silencing of the locus [46] (Figure 2)Despite this the loss of this mark does not always representthe activation of the region suggesting the involvement ofother important factors also [47] H3K27me3 is a majorchromatin silencing modification found associated with 51015840region of thousands of genes inArabidopsis [48] On the otherhand H3K9me3 is a repressive chromatin modification asso-ciated with gene coding region [49] H3K9me2 is localizedin heterochromatic region transposons pseudogenes andrepeats [50] All H3K4me marks are associated with activechromatin H3K4me3 and H3K4me2 are associated withpromoter and 51015840 part of the transcribed gene while H3K4me1covers terminal part (31015840) of the gene [51] Silent chromatin

(heterochromatin) bears H3K9me which recruits other pro-teins such as heterochromatin protein 1 (LHP1)These bind tomethylated H3K9 and help in the propagation of heterochro-matin to adjacent region of the chromosome [52]

Drought-inducible linker histone variant (H1S) in tomatois responsible for negative regulation of stomatal closure [53]H3K4me3 and H3 acetylation was found to be induced inalcohol dehydrogenase 1 (ADH1) and pyruvate decarboxylase1 (PDC1) genes These changes were reverted back on with-drawal of submergence stress [54]

H3K4memarks on nucleosomes of stress-inducible geneshave been reported to be associated with the activation ofchromatin in response to dehydration [55] H3Kmemarks arereported to be present in 90 of annotated Arabidopsis geneswherein abundance of H3K4me3 mark is directly relatedto level of transcriptional activity of the drought responsivegenes Increase in H3 phosphorylation and H3 and H4acetylation in response to abiotic stresses have been found intobacco and Arabidopsis [56]

243 Other Histone Modifications In Arabidopsis an argi-nine methyltransferase SKB1 (also known as protein argininemethyl transferase5 PRMT5) is involved in abiotic stressresponse SKB1 is normally associated with chromatin andincreases level of arginine trimethylation on H4 (H4Rme2)so as to repress gene expression With the onset of salt stressSKB1 dissociates from chromatin and results in induction ofstress responsive genes skb1 mutant is hypersensitive to saltstress [57]

25 RNA Directed DNA Methylation (RdDM) Abiotic stresshas been reported to modulate the expression of several hun-dred genes and depending upon their roles they are eitherupregulated or downregulated Apart from the regulatorycontrol at the level of transcription the posttranscriptionalregulation is also important for regulation of gene expressionThis is achieved by RNA binding proteins (RBPs) which bind


MM

M

H3H2A

H4H2B

M

Heterochromatin

Methylated CpGs

Inactive chromatin

M3

M2

M1 M1

M3

M2

M1

4 9 23 27


Figure 2 Epigenetic marks associated with transcriptionally inactive chromatin Methylation at K4 K9 and K27 of H3 and methylated CGsindicate silent chromatin

to UTRs of mRNAs and control their stability localization ortranslation In addition to this small RNAs (microRNAs andsmall interfering RNAs) play a vital role in gene regulation[58] RNAi machinery is necessary for the maintenance ofheterochromatin and silencing of repetitive DNA trans-posons and so forth [59] RNA directed DNA methylation(RdDM) is known to be regulated by temperature Virus-induced gene silencing is promoted at low temperature anddelayed by high temperature [60]Though promoters are alsomethylated de novo TEs and other repetitive DNA elementsare effectively silenced by this mechanism [61]

251 miRNA MicroRNAs are short (20ndash24 nucleotide) en-dogenous RNAs processed byDicer-like enzyme from longertranscripts which are not translated into proteins [58] PlantmiRNAs genes have been found away from protein codingregions of the genome and are expressed by their own tran-scription unit [62]

Role of miRNAs in gene regulation vis-a-vis abiotic stresshas been best studied by Sunkar et al [58] Genes which arenegative regulators of stress tolerance (ie repress stress re-sponsive genes) are downregulated during stress by upregula-tion of microRNAs targeting these genes On the other handmiRNA downregulation under stress results in accumulationof mRNAs of those genes which act as positive regulators ofstress tolerance [58]

Overexpression of miR396 in Arabidopsis and rice plantsresulted in reduced tolerance to salt and alkali stress [63]Sequence analysis of small RNA library of stress treatedArabidopsis thaliana showed that miR393 was the mostabundantly expressed miRNA and its level increased by avariety of stresses like cold salt ABA and dehydration Somestress-specific expression of miRNAs was also observed forinstance miR319c is upregulated by cold but not by ABA

salt or dehydration [64] Cold stress resulted in differentialexpression of a number of miRNAs including miR319 inrice and Brachypodium [65 66] On oxidative stress miR398is transcriptionally downregulated therefore leading to theaccumulation of CSD1 and CSD2 mRNAs which are crucialfor plant stress resistance mRNAs of these two genes donot accumulate under normal conditions because ofmiR398-guided cleavage [67] miR160 and miR164 along with theirtarget genes have been reported to play an important role inthe regulation of root growth in Arabidopsis during droughtstress Overexpression ofmiR160 led to agravitropic roots andincrease in the number of lateral roots [68] Manipulationof miRNA-guided gene regulation can help development ofstress-resistant plants [69]

252 siRNA Small interfering RNAs (siRNAs) 20ndash24 nucle-otides in length are known to play an important role in arange of processes such as heterochromatin formation trans-poson silencing transgene silencing posttranscriptional reg-ulation of mRNAs and defense against viruses Processingof long dsRNAs generated from natural cis-antisense genepairs repetitive DNA or noncoding transcripts by Dicer-likeenzymes generate small interfering RNAs [58]

After processing one of the strands of the duplex servesas guide strand and is loaded onto RITS (RNA-inducedtranscriptional silencing complex) The complex binds tosiRNA by PAZ domain of AGO4 protein and is directed tothe homologous DNA sequence for gene silencing at tran-scriptional level (TGS) AGO4 is associated with Pol V whichsynthesizes transcripts that interact with siRNAs to induceDNA methylation at the targeted site by DRM2 (de novomethyltransferase) [10] Nascent RNAs bind to the targetDNA sequences and recruit histonemethylases to addmethylgroup to lysine residues at 9 or 27 position of H3 histone


tails This leads to recruitment of DNA methylases whichtransfer methyl group to DNA ultimately leading to genesilencing and heterochromatin formation [70 71] The meth-ylated DNA serves as template for Pol IV Pol IV transcribesthe methylated DNA and its downstream sequence to pro-duce aberrant RNA transcripts which subsequently generatesdsRNA by the activity RDR2 (RNA-dependant RNA poly-merase 2) These RDR2 synthesized dsRNAs act as precursorfor secondary siRNA which help in spreading methylation toadjacent sequences [10]

One of the possible mechanisms of regulation of plantstress response is the inhibition of siRNA biogenesis Dcl2and Dcl3 mutants having weakened transactivation activityof siRNA biogenesis were more sensitive to MMS (methyl-methane sulfonate) which causes genotoxic stress [72]

An excellent example of regulation of stress tolerance isthat of genes involved in proline catabolism in ArabidopsisSR05 is induced by salt stress SR05mRNA is complementaryto P5CDH mRNA (P5CDH protein is an important enzymefor proline breakdown) and they together generate a dsRNAwhich is acted upon by siRNA biogenesis pathway factors(DCL2 RDR6 SGS3 and NRPD1A) to produce 24nt-siRNAThis nat-siRNA guides the cleavage of P5CDH mRNAsleading to proline accumulation and better salt toleranceSR05 mutants exhibit hypersensitivity to salt stress [73]

26 Chromatin Remodelling Factors (CRMs) Chromatin re-modeling factors are multisubunit protein complexes whichmodify chromatin structure by influencing histone-DNA in-teractions in order to assemble destabilize or displace nucle-osomes using ATP derived energy [74] High CRM concen-tration results in histone octamer transfer to another DNAmolecule Atmoderate concentration they facilitate sliding ofthe octamer position leading to altered gap between adjacentnucleosomes to facilitate access of TFs restriction enzymesand so forth

ATP dependent chromatin remodeling factors can begrouped into three categories

(1) SWFSNF ATPases(2) ISWI (Imitation Switch) ATPases(3) CHD (chromodomain and helicase-like domain)

ATPases

SWF1SNF complex was originally identified for defectsin mating type switching (SW1) and sucrose fermentation(sucrose nonfermenting) [75] ATCHR12 a SNF2Brahma-type chromatin-remodelling protein plays an importantrole in temporary growth arrest of normally active primarybuds in Arabidopsis thaliana exposed to stress [76] SW13subunit of SW1SNF complex has been recently reported toact as a positive regulator in ABA-mediated inhibition ofseed germination and growth by interacting with a negativeregulator HAB1 (Hypersensitive to ABA1) to increase theexpression of RAB18 and RD29B [77] Another chromatinremodeling factor PICKLE (PKL) helps in maintaining AB13and AB15 chromatin in a repressed state during germinationindicated by reduced H3K9 and H3K27 methylation level inpklmutant seeds when treated with ABA [78]

Histone chaperons are known to carry out nucleosomeassembly and disassembly by deposition or expulsion ofhistones respectively NAP1 (nucleosome assembly protein1) is known to function as chaperon for H2A and H2Bhistones in Arabidopsis [79] AtNAPs are reported to bepositive regulators of ABA signaling pathway [80] MSI1 aWD40 repeat protein acting as a subunit for many proteincomplexes (like chromatin assembly factor 1 and Polycombgroup protein complexes) is involved in chromatin assemblyand plays the role of a negative regulator in drought stressresponse in Arabidopsis [81] Plants with highly reducedMSI1 levels exhibit enhanced level of ABA-responsive genetranscripts [82] COR (Cold regulated) genes containingCDRE (C-repeatdehydration responsive element) are alsoregulated negatively by MSI1-like protein MSI4FVE [83]

3 Conclusion

Stress-induced epigenetic changes in the form of DNAmeth-ylation histone tail modifications and RNA directed DNAmethylation are governed by a complex phenomenon involv-ing myriad factors interacting among themselves Thesechanges in epigeneticmarksmodulate transcription of stress-responsive genes leading to the formation of heritable epialle-les which subsequently enable plant to withstand stressThereis a need for the identification of such epialleles along withcomprehensive understanding of the fundamental epigeneticmechanisms Importantly it is necessary to study epigeneticheterogeneity (a key aspect of epigenetic dynamics) bothat epialleles level and whole genome level [84] Completeknowledge of these mechanisms would lay a platform for theresearchers to devise better strategies for crop improvementlike exploitation of small RNAs for the manipulation ofepialleles

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors are grateful to the Department of BiotechnologyGovernment of India for the financial support Thanks arealso due to the Bioinformatics Centre at School of Biotech-nology University of Jammu

References

[1] S Mahajan and N Tuteja ldquoCold salinity and drought stressesan overviewrdquo Archives of Biochemistry and Biophysics vol 444no 2 pp 139ndash158 2005

[2] S D Horne S K Chowdhury and H H Q Heng ldquoStressgenomic adaptation and the evolutionary trade-offrdquo Frontiersin Genetics vol 5 article 92 2014

[3] H Peng and J Zhang ldquoPlant genomic DNA methylation inresponse to stresses potential applications and challenges inplant breedingrdquo Progress in Natural Science vol 19 no 9 pp1037ndash1045 2009


[4] V Chinnusamy and J K Zhu ldquoEpigenetic regulation of stressresponses in plantsrdquo Current Opinion in Plant Biology vol 12no 2 pp 133ndash139 2009

[5] M Tariq and J Paszkowski ldquoDNA and histone methylation inplantsrdquo Trends in Genetics vol 20 no 6 pp 244ndash251 2004

[6] T Chen and E Li ldquoStructure and function of eukaryotic DNAmethyltransferasesrdquo Current Topics in Developmental Biologyvol 60 pp 55ndash89 2004

[7] M Chen S Lv and Y Meng ldquoEpigenetic performers in plantsrdquoDevelopment Growth and Differentiation vol 52 no 6 pp 555ndash566 2010

[8] X Cao N M Springer M G Muszynski R L Phillips SKaeppler and S E Jacobsen ldquoConserved plant genes withsimilarity to mammalian de novo DNA methyltransferasesrdquoProceedings of the National Academy of Sciences of the UnitedStates of America vol 97 no 9 pp 4979ndash4984 2000

[9] J A Law and S E Jacobsen ldquoEstablishing maintaining andmodifying DNA methylation patterns in plants and animalsrdquoNature Reviews Genetics vol 11 no 3 pp 204ndash220 2010

[10] M Matzke T Kanno L Daxinger B Huettel and A J MMatzke ldquoRNA-mediated chromatin-based silencing in plantsrdquoCurrent Opinion in Cell Biology vol 21 no 3 pp 367ndash376 2009

[11] I J Furner and M Matzke ldquoMethylation and demethylation ofthe Arabidopsis genomerdquo Current Opinion in Plant Biology vol14 no 2 pp 137ndash141 2011

[12] M Gehring and S Henikoff ldquoDNA methylation dynamics inplant genomesrdquo Biochimica et Biophysica ActamdashGene Structureand Expression vol 1769 no 5-6 pp 276ndash286 2007

[13] I Ahmed A Sarazin C Bowler V Colot and H QuesnevilleldquoGenome-wide evidence for local DNA methylation spreadingfrom small RNA-targeted sequences in Arabidopsisrdquo NucleicAcids Research vol 39 no 16 pp 6919ndash6931 2011

[14] S J Cokus S Feng X Zhang et al ldquoShotgun bisulphitesequencing of the Arabidopsis genome reveals DNA methyla-tion patterningrdquo Nature vol 452 no 7184 pp 215ndash219 2008

[15] D Zilberman M Gehring R K Tran T Ballinger and SHenikoff ldquoGenome-wide analysis of Arabidopsis thalianaDNAmethylation uncovers an interdependence betweenmethylationand transcriptionrdquo Nature Genetics vol 39 no 1 pp 61ndash692007

[16] A Zemach I E McDaniel P Silva and D Zilberman ldquoGe-nome-wide evolutionary analysis of eukaryotic DNA methyl-ationrdquo Science vol 328 no 5980 pp 916ndash919 2010

[17] C-S Choi and H Sano ldquoAbiotic-stress induces demethylationand transcriptional activation of a gene encoding a glycerophos-phodiesteraselike protein in tobacco plantsrdquoMolecular Geneticsand Genomics vol 277 no 5 pp 589ndash600 2007

[18] R Aina S Sgorbati A Santagostino M Labra A Ghiani andS Citterio ldquoSpecific hypomethylation of DNA is induced byheavy metals in white clover and industrial hemprdquo PhysiologiaPlantarum vol 121 no 3 pp 472ndash480 2004

[19] A Kovarik B Koukalova M Bezdek and Z Opatrny ldquoHyper-methylation of tobacco heterochromatic loci in response toosmotic stressrdquoTheoretical and Applied Genetics vol 95 no 1-2pp 301ndash306 1997

[20] M Bracale M Levi C Savini W Dicorato and M G GallildquoWater deficit in pea root tips effects on the cell cycle and onthe production of dehydrin-like proteinsrdquoAnnals of Botany vol79 no 6 pp 593ndash600 1997

[21] M Labra A Ghiani S Citterio et al ldquoAnalysis of cytosinemethylation pattern in response towater deficit in pea root tipsrdquoPlant Biology vol 4 no 6 pp 694ndash699 2002

[22] K K Suji and A J Joel ldquoAn epigenetic change in rice cultivarsunder water stress conditionsrdquo Electronic Journal of PlantBreeding vol 1 no 4 pp 1142ndash1143 2010

[23] O V Dyachenko N S Zakharchenko T V Shevchuk H JBohnert J C Cushman and Y I Buryanov ldquoEffect of hyper-methylation of CCWGG sequences in DNA of Mesembryan-themum crystallinum plants on their adaptation to salt stressrdquoBiochemistry (Moscow) vol 71 no 4 pp 461ndash465 2006

[24] K Akimoto H Katakami H J Kim et al ldquoEpigenetic inheri-tance in rice plantsrdquo Annals of Botany vol 100 no 2 pp 205ndash217 2007

[25] M Tan ldquoAnalysis of DNA methylation of maize in response toosmotic and salt stress based onmethylation-sensitive amplifiedpolymorphismrdquo Plant Physiology and Biochemistry vol 48 no1 pp 21ndash26 2010

[26] X Ou Y Zhang C Xu et al ldquoTransgenerational inheritanceof modified DNAmethylation patterns and enhanced toleranceinduced by heavy metal stress in rice (Oryza sativa L)rdquo PLoSONE vol 7 no 9 Article ID e41143 2012

[27] H P Kou Y Li X X Song et al ldquoHeritable alteration in DNAmethylation induced by nitrogen-deficiency stress accompaniesenhanced tolerance by progenies to the stress in rice (Oryzasativa L)rdquo Journal of Plant Physiology vol 168 no 14 pp 1685ndash1693 2011

[28] M M Suzuki and A Bird ldquoDNA methylation landscapesprovocative insights from epigenomicsrdquo Nature Reviews Genet-ics vol 9 no 6 pp 465ndash476 2008

[29] R S Sekhon and S Chopra ldquoProgressive loss of DNAmethyla-tion releases epigenetic gene silencing froma tandemly repeatedmaize Myb generdquo Genetics vol 181 no 1 pp 81ndash91 2009

[30] M Kato A Miura J Bender S E Jacobsen and T KakutanildquoRole of CG and non-CG methylation in immobilization oftransposons in Arabidopsisrdquo Current Biology vol 13 no 5 pp421ndash426 2003

[31] S Hashida K Kitamura TMikami and Y Kishima ldquoTempera-ture shift coordinately changes the activity and the methylationstate of transposon Tam3 in Antirrhinum majusrdquo Plant Physiol-ogy vol 132 no 3 pp 1207ndash1216 2003

[32] C Cheng M Daigen and H Hirochika ldquoEpigenetic regulationof the rice retrotransposon Tos17rdquo Molecular Genetics andGenomics vol 276 no 4 pp 378ndash390 2006

[33] J C Rice and C D Allis ldquoHistone methylation versus histoneacetylation new insights into epigenetic regulationrdquo CurrentOpinion in Cell Biology vol 13 no 3 pp 263ndash273 2001

[34] S L Berger ldquoThe complex language of chromatin regulationduring transcriptionrdquo Nature vol 447 no 7143 pp 407ndash4122007

[35] J-M Kim T K To J Ishida et al ldquoAlterations of lysinemodifications on the histone H3 N-tail under drought stressconditions inArabidopsis thalianardquo Plant amp Cell Physiology vol49 no 10 pp 1580ndash1588 2008

[36] E J Stockinger Y Mao M K Regier S J Triezenberg andM FThomashow ldquoTranscriptional adaptor and histone acetyl-transferase proteins in Arabidopsis and their interactions withCBF1 a transcriptional activator involved in cold-regulatedgene expressionrdquoNucleic Acids Research vol 29 no 7 pp 1524ndash1533 2001

[37] Z J Chen and L Tian ldquoRoles of dynamic and reversible histoneacetylation in plant development and polyploidyrdquo Biochimica etBiophysica Acta vol 1769 no 5-6 pp 295ndash307 2007


[38] C Hollender and Z Liu ldquoHistone deacetylase genes in Ara-bidopsis developmentrdquo Journal of Integrative Plant Biology vol50 no 7 pp 875ndash885 2008

[39] F Pontvianne T Blevins andC S Pikaard ldquoArabidopsishistonelysine methyltransferasesrdquo Advances in Botanical Research vol53 pp 1ndash22 2010

[40] X Yu L Li M Guo J Chory and Y Yin ldquoModulation ofbrassinosteroid-regulated gene expression by jumonji domain-containing proteins ELF6 and REF6 in Arabidopsisrdquo PNAS vol105 no 21 pp 7618ndash7623 2008

[41] A Miura M Nakamura S Inagaki A Kobayashi H Sazeand T Kakutani ldquoAn Arabidopsis jmjC domain protein protectstranscribed genes fromDNAmethylation at CHG sitesrdquo EMBOJournal vol 28 no 8 pp 1078ndash1086 2009

[42] D Vermaak K Ahmad and S Henikoff ldquoMaintenance ofchromatin states an open-and-shut caserdquo Current Opinion inCell Biology vol 15 no 3 pp 266ndash274 2003

[43] D M Bond E S Dennis B J Pogson and E J Finnegan ldquoHis-tone acetylation vernalization insensitive 3 flowering locus Cand the vernalization responserdquo Molecular Plant vol 2 no 4pp 724ndash737 2009

[44] J Zhu J C Jae Y Zhu et al ldquoInvolvement ofArabidopsisHOS15in histone deacetylation and cold tolerancerdquo Proceedings of theNational Academy of Sciences of the United States of Americavol 105 no 12 pp 4945ndash4950 2008

[45] S Sridha and K Wu ldquoIdentification of AtHD2C as a novelregulator of abscisic acid responses in Arabidopsisrdquo PlantJournal vol 46 no 1 pp 124ndash133 2006

[46] A Gendrel Z Lippman C Yordan V Colot and R AMartienssen ldquoDependence of heterochromatic histone H3methylation patterns on the Arabidopsis gene DDM1rdquo Sciencevol 297 no 5588 pp 1871ndash1873 2002

[47] L M Johnson X Cao and S E Jacobsen ldquoInterplay betweentwo epigenetic marks DNA methylation and histone H3 lysine9 methylationrdquo Current Biology vol 12 no 16 pp 1360ndash13672002

[48] K Zhang V V Sridhar J Zhu and A Kapoor ldquoDistinctive corehistone post-translational modification patterns in Arabidopsisthalianardquo PLoS ONE vol 2 no 11 Article ID e1210 2007

[49] F Turck F Roudier S Farrona et al ldquoArabidopsis TFL2LHP1specifically associates with genes marked by trimethylation ofhistone H3 lysine 27rdquo PLoS Genetics vol 3 article e86 2007

[50] Y V Bernatavichute X Zhang S Cokus M Pellegrini andS E Jacobsen ldquoGenome-wide association of histone H3 lysinenine methylation with CHG DNA methylation in Arabidopsisthalianardquo PLoS ONE vol 3 no 9 Article ID e3156 2008

[51] X Zhang Y V Bernatavichute S Cokus M Pellegrini andS E Jacobsen ldquoGenome-wide analysis of mono- di- andtrimethylation of histone H3 lysine 4 in Arabidopsis thalianardquoGenome Biology vol 10 no 6 article R62 2009

[52] A Boyko P Kathiria F J Zemp Y Yao I Pogribny and IKovalchuk ldquoTransgenerational changes in the genome stabilityand methylation in pathogen-infected plants (Virus-inducedplant genome instability)rdquo Nucleic Acids Research vol 35 no5 pp 1714ndash1725 2007

[53] G S Scippa M di Michele E Onelli G Patrignani DChiatante and E A Bray ldquoThe histone-like protein H1-S andthe response of tomato leaves to water deficitrdquo Journal ofExperimental Botany vol 55 no 394 pp 99ndash109 2004

[54] H Tsuji H Saika N Tsutsumi A Hirai and M NakazonoldquoDynamic and reversible changes in histone H3-Lys4 methy-lation and H3 acetylation occurring at submergence-inducible

genes in ricerdquo Plant and Cell Physiology vol 47 no 7 pp 995ndash1003 2006

[55] K van Dijk Y Ding S Malkaram et al ldquoDynamic changesin genome-wide histone H3 lysine 4 methylation patterns inresponse to dehydration stress in Arabidopsis thalianardquo BMCPlant Biology vol 10 article 238 2010

[56] A Sokol A Kwiatkowska A Jerzmanowski and MPrymakowska-Bosak ldquoUp-regulation of stress-induciblegenes in tobacco and Arabidopsis cells in response to abioticstresses and ABA treatment correlates with dynamic changesin histone H3 and H4 modificationsrdquo Planta vol 227 no 1 pp245ndash254 2007

[57] Z Zhang S Zhang Y Zhang et al ldquoArabidopsis floral initiatorSKB1 confers high salt tolerance by regulating transcription andpre-mRNA splicing through altering histone H4R3 and smallnuclear ribonucleoprotein LSM4 methylationrdquo Plant Cell vol23 no 1 pp 396ndash411 2011

[58] R Sunkar V Chinnusamy J Zhu and J Zhu ldquoSmall RNAsas big players in plant abiotic stress responses and nutrientdeprivationrdquo Trends in Plant Science vol 12 no 7 pp 301ndash3092007

[59] T A Volpe C Kidner I M Hall G Teng S I S Grewal and RA Martienssen ldquoRegulation of heterochromatic silencing andhistone H3 lysine-9 methylation by RNAirdquo Science vol 297 no5588 pp 1833ndash1837 2002

[60] J R Tuttle A M Idris J K Brown C H Haigler and DRobertson ldquoGeminivirus-mediated gene silencing from cottonleaf crumple virus is enhanced by low temperature in cottonrdquoPlant Physiology vol 148 no 1 pp 41ndash50 2008

[61] Y Okano D Miki and K Shimamoto ldquoSmall interferingRNA (siRNA) targeting of endogenous promoters inducesDNAmethylation but not necessarily gene silencing in ricerdquo PlantJournal vol 53 no 1 pp 65ndash77 2008

[62] B J Reinhart E GWeinstein MW Rhoades B Bartel and DP Bartel ldquoMicroRNAs in plantsrdquo Genes and Development vol16 no 13 pp 1616ndash1626 2002

[63] P Gao X Bai L Yang et al ldquoOver-expression of osa-MIR396cdecreases salt and alkali stress tolerancerdquo Planta vol 231 no 5pp 991ndash1001 2010

[64] R Sunkar and J K Zhu ldquoNovel and stress regulatedmicroRNAsand other small RNAs from Arabidopsisrdquo Plant Cell vol 16 no8 pp 2001ndash2019 2004

[65] J Zhang Y Xu Q Huan and K Chong ldquoDeep sequencing ofBrachypodium small RNAs at the global genome level identifiesmicroRNAs involved in cold stress responserdquo BMC Genomicsvol 10 article 1471 p 449 2009

[66] D K Lv X Bai Y Li et al ldquoProfiling of cold-stress-responsivemiRNAs in rice by microarraysrdquo Gene vol 459 no 1-2 pp 39ndash47 2010

[67] R Sunkar A Kapoor and J Zhu ldquoPosttranscriptional inductionof two CuZn superoxide dismutase genes in Arabidopsis ismediated by downregulation of miR398 and important foroxidative stress tolerancerdquo Plant Cell vol 18 no 8 pp 2051ndash2065 2006

[68] H S Guo Q Xie J F Fei and N H Chua ldquoMicroRNA directsmRNA cleavage of the transcription factor NAC1 to downreg-ulate auxin signals for Arabidopsis lateral root developmentrdquoPlant Cell vol 17 no 5 pp 1376ndash1386 2005

[69] L Navarro P Dunoyer F Jay et al ldquoA plant miRNA contributesto antibacterial resistance by repressing auxin signalingrdquo Sci-ence vol 312 no 5772 pp 436ndash439 2006


[70] A Verdel S Jia S Gerber et al ldquoRNAi-mediated targeting ofheterochromatin by the RITS complexrdquo Science vol 303 no5658 pp 672ndash676 2004

[71] S I S Grewal andDMoazed ldquoHeterochromatin and epigeneticcontrol of gene expressionrdquo Science vol 301 no 5634 pp 798ndash802 2003

[72] Y Yao A Bilichak A Golubov T Blevins and I KovalchukldquoDifferential sensitivity of Arabidopsis siRNA biogenesismutants to genotoxic stressrdquo Plant Cell Reports vol 29 no 12pp 1401ndash1410 2010

[73] O Borsani J Zhu P E Verslues and R Sunkar ldquoEndogenoussiRNAs derived from a pair of natural cis-antisense transcriptsregulate salt tolerance in Arabidopsisrdquo Cell vol 123 no 7 pp1279ndash1291 2005

[74] M E Alvarez F Nota and D A Cambiagno ldquoEpigeneticcontrol of plant immunityrdquo Molecular Plant Pathology vol 11no 4 pp 563ndash576 2010

[75] P Sudarsanam and F Winston ldquoThe SwiSnf family nu-cleosome-remodeling complexes and transcriptional controlrdquoTrends in Genetics vol 16 no 8 pp 345ndash351 2000

[76] L Mlynarova J Nap and T Bisseling ldquoThe SWISNF chro-matin-remodeling gene AtCHR12 mediates temporary growtharrest in Arabidopsis thaliana upon perceiving environmentalstressrdquo Plant Journal vol 51 no 5 pp 874ndash885 2007

[77] A Saez A Rodrigues J Santiago S Rubio and P L RodriguezldquoHAB1-SWI3B interaction reveals a link between abscisic acidsignaling and putative SWISNF chromatin-remodeling com-plexes in Arabidopsisrdquo Plant Cell vol 20 no 11 pp 2972ndash29882008

[78] E Perruc N Kinoshita and L Lopez-Molina ldquoThe role ofchromatin-remodeling factor PKL in balancing osmotic stressresponses during Arabidopsis seed germinationrdquo Plant Journalvol 52 no 5 pp 927ndash936 2007

[79] A Dong Z Liu Y Zhu et al ldquoInteracting proteins anddifferences in nuclear transport reveal specific functions for theNAP1 family proteins in plantsrdquo Plant Physiology vol 138 no 3pp 1446ndash1456 2005

[80] Z Q Liu J Gao A W Dong and W H Shen ldquoA truncatedArabidopsis nucleosome assembly protein 1 AtNAP1 3T altersplant growth responses to abscisic acid and salt in the Atnap1 3-2 mutantrdquoMolecular Plant vol 2 no 4 pp 688ndash699 2009

[81] L Hennig R Bouveret and W Gruissem ldquoMSI1-like proteinsan escort service for chromatin assembly and remodelingcomplexesrdquo Trends in Cell Biology vol 15 no 6 pp 295ndash3022005

[82] C Alexandre YMoller-Steinbach N SchonrockW Gruissemand L Hennig ldquoArabidopsis MSI1 is required for negativeregulation of the response to drought stressrdquo Molecular Plantvol 2 no 4 pp 675ndash687 2009

[83] H Kim Y Hyun J Park et al ldquoA genetic link between coldresponses and flowering time through FVE in Arabidopsisthalianardquo Nature Genetics vol 36 no 2 pp 167ndash171 2004

[84] H H Q Heng S W Bremer J B Stevens K J Ye G Liuand C J Ye ldquoGenetic and epigenetic heterogeneity in cancer agenome-centric perspectiverdquo Journal of Cellular Physiology vol220 no 3 pp 538ndash547 2009

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of


Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology


Molecular Biology International

GenomicsInternational Journal of


The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014


BioinformaticsAdvances in

Marine BiologyJournal of



Signal TransductionJournal of


BioMed Research International

Evolutionary BiologyInternational Journal of



Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014


Genetics Research International


Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational



Enzyme Research



Microbiology


heritable are truly epigenetic [4]These alterations affect geneexpression by chromatin remodeling which involves changein chromatin state of the chromosome that is euchromatinor heterochromatin For instance in order to increase theexpression of a particular gene its promoter sequence mustbe exposed so that transcription factor and RNA polymerasecould bind to the underlying upstream DNA and carryouttranscription of the gene In order to expose the DNA forefficient transcription nucleosome complex must be untan-gled Conversely for shutting off gene expressionDNAmeth-ylation has to be reestablished followed by packaging of theDNA stretch covering that particular gene by the histonecomponents of the nucleosome complex

2 Epigenetic Alterations andRequisite Machinery

21 DNAMethylation Methylation is the only covalentmod-ification that has been identified on DNA till date [5] Itinvolves addition of methyl group (minusCH

3) at fifth carbon in

the cytosine ring of theDNAmolecule at CpG CpNpG (sym-metric) or CpNpN (asymmetric) sites (whereN isA C or T)

MechanismofDNAmethylation is governed by two typesof enzymes

(i) methyltransferases(ii) demethylases

Two major enzymatic activities regulate cytosine methy-lation in plants which involve de novo establishment of meth-ylation on DNA and maintenance of the already methylatedDNA The de novo methylation is a process by which pre-viously unmethylated cytosine residues are methylated lead-ing to the formation of new methylation patterns Mainte-nance methylation is the process of maintenance of preex-isting methylation patterns after DNA replication [6] MET1(DNAmethyltransferase 1) and CMT (chromomethylase) areresponsible for maintenance of CG and CNG methylationrespectively [7]De novomethylation is established by DRM2(domains rearranged methyltransferase 2) in the new DNAsequences generated after DNA replication DNA gycosylases(ROS1 DML2 DML3 and DME) catalyze the removal ofmethyl group from cytosine residue [8]

Genome-wide analysis of DNAmethylation in Arabidop-sis thaliana revealed the methylation status of its genome as24CG 67 CNG and 17 CNNmethylation [9] CpNpGand CpNpN methylation changes mediated by CMT3 andDRM2 have been reported to regulate transposons and repeatregions through chromatin remodelling during exposure tostress [10 11]

DNA methylation is distributed in the plant genomeincluding heterochromatic and euchromatic regions [12]Theheterochromatic regions densely packed with transposableelements and other repetitive sequences are highly methy-lated whereas euchromatic regions containing genes andnonrepetitive intergenic regions show comparatively lessercytosine methylation Interestingly transposons are methy-lated along their entire length in contrast to genes which areoften methylated away from the start and termination sites

Within the euchromatic region pseudogenes and transcrip-tionally inactive genes show higher levels of methylation thanactively expressing genes [13] Expressed genes are methy-lated in the transcribed region (gene-body methylation) [14]Gene bodymethylation exhibits a parabolic relationship withtranscription level in rice and Arabidopsis Both the leastexpressed and the highly expressed genes are least prone tomethylation whereas moderately expressed genes are mostlikely to be methylated at gene body [15 16] Genic regionsdo not contain non-CG methylation while transposons andrepeats abundantly possess CpNpG or CpNpN methylationMethylation at 51015840 portion (promoter plus some transcribedregion) and 31015840 portion inhibits gene expression

Stress can cause hypermethylation or hypomethylationof DNA In maize roots cold induced expression of ZmMI1was accompanied with a decrease in DNAmethylation whichdid not revert to basal level even after 7 days of recoveryIn tobacco aluminium salt cold and paraquat stresses in-duced DNA demethylation at CG nucleotides in the codingsequence of NtGPDL gene (glycerophosphodiesterase-likeprotein) [17] Heavy metal stress is known to induce hypo-methylation at specific sites in the genome of both the metal-sensitive Trifolium repens L and metal-tolerant Cannabissativa L [18] DNA hypermethylation at CG but not CNGat two heterochromatic loci was induced in cell suspensionculture of tobacco by osmotic stress [19] Drought-inducedhypermethylation has been proposed to play a primary anddirect role in reducing the metabolic activity in pea root tipsafter 72-hour water deficit [20 21] Suji and Joel [22] reporteddrought induced hypermethylation and hypomethylation indrought tolerant and drought susceptible varieties of ricerespectively Stress induced hypermethylation of satelliteDNA was associated with a switch in photosynthesis modefrom C3 to CAM in Mesembryanthemum crystallinum L afacultative halophyte [23]

Promoter demethylation is known to abolish constitutivegene silencing established because of hypermethylation ofXa21G gene thereby conferring disease resistance in rice [24]Changed methylation level in maize exposed to osmotic andsalt stress helps in stress acclimation [25] Stressful environ-ment produces transgenerational epigenetic modificationsleading to enhanced stress adaptability in future progenies[26] Nonstressed progenies of stressed rice plants carryingmodified methylation patterns acquired from the parentexhibit enhanced stress tolerance [27]

Transposons and other repeats constitute large part of theplant genome and cytosine methylation is chiefly targetedtowards transposon silencing [28 29] CG and non-CGmethylation contribute towards transposon immobilizationIn plants non-CG methylation is proposed to have evolvedas an epigenetic tag committed to transposon control [30]A close relationship between methylation and low temper-ature dependent transposition (LTDT) has been reportedwhere low temperature caused reduction inmethylation levelopposed to hypermethylation resulting from higher temper-ature in Antirrhinum majus [31] Transposon methylationchanges which control transposition activity of transposonsare also reported to spread silencing signal to neighboring


H3H4 H2B

H2A

RNA Pol

mRNA

Active chromatin

UMUM

UM

UM

UM UM

UM

Unmethylated CpGs

A AA

M3

M2

M1

4 9 23 27
















ofhisto


ClassI

ClassII

ClassIII

ClassIV

ClassV

SUVH

SUVR

Mem

bers

Thesea

reho

mologueso

fE(Z)

(enh

ancero

fzeste

from

Drosophila

)three

E(Z)-like

proteins

are

encodedby

Arabidopsis

geno

me

CURL

YLE

AF(C

LF)

MED

EA(M

EA)

SWIN

GER

(SWN)

Thiscla

ssis

constituted

bySD

G8

SDG4

Thiscla

sscontains

homologueso

fTritho

rax

thereforemem

bersare

calledAT

X(Arabidopsis

Trith

orax-like)p

roteins1ndash5

Five

genese

ncod

eTrithorax

homologuesAT

X1ndash5

Arabidopsis

has

twomem

bers

belong

ingto

this

classA

TXR5

and

ATXR

6

SUVH(SU(VAR3-9))

Tenplantspecific

mem

bers

[SU(VAR)

3-9related]

Dom

ains

Con

tainsS

ET(sup

pressor

ofvarie

gatio

nenhancer

ofzeste

andTrith

orax)

domain

E(Z)

domain

SANTdo

main(SW13

ADA2NCO

Rand

TFIIIB-binding

)and

CXC(cysteiner

ichregion

)

Con

tain

SETdo

main

andAW

Smotif

(associatedwith

SET)

Con

tain

SETpo

st-SE

Tdo

main

PHD(plant

homeodo

main)

PWWP

(prolin

e-tryptoph

an-

tryptoph

an-prolin

e)

FYRN

(FY

rich

N-te

rminus)and

FYRC

(FY

rich

C-term

inus)

Con

tain

SET

domainandPH

Ddo

main

Con

tain

SETdo

main

pre-SE

Tdo

main

post-

SETdo

main

and

SRA(SET

andRING

fingera

ssociated

domain)

Con

tain

allother

domains

except

SRA

domain

somem

embersare

repo

rted

topo

ssessa

novelW

IYLD

domainsim

ilarto

DNA-

bind

ingprotein

Role

CLFhelpsinflo

weringtim

eregu

latio

nMEA

isinvolved

inseed

developm

ent

SWNisrequ

iredforfl

ower

developm

ent

SDG8isinvolved

inFL

Cexpressio

nwhich

regu

lates

flowering

time

SDG4isinvolved

inprop

erpo

llenand

stam

endevelopm

ent

Involved

indrou

ghtstre

ssrespon

seatx1m

utantis

hypo

sensitive

todehydration

Play

rolein

cell

cycle

regu

lation

Markinactiv

echromatingene

silencing

Potentialrolein

heterochromatic

siRNAprod

uctio

nmachinery

EpigeneticRo

leTh

eyhave

H3K

27methyltransfe

rase

activ

ity

They

carryou

tdi-or

trim

ethylatio

nof

H3K

36

ATX1

andAT

X2are

involved

inH3K

4me3

and

H3K

4me2

Functio

nof

ATX345is

stillno

tkno

wn

They

carryou

tmon

omethylatio

nof

H3K

27

H3K

9methylatio

ndifferent

SRAdo

mains

have

preferentia

laffinity

ford

ifferentcytosine

methylatio

ncontext

(sym

metric

orasym

metric

)

Functio

nun

clear

yet

howeveritresem

bles

proteins

involved

inheterochromatin

form

ation

















MM

M

H3H2A

H4H2B

M

Heterochromatin

Methylated CpGs

Inactive chromatin

M3

M2

M1 M1

M3

M2

M1

4 9 23 27

















ATPases



3 Conclusion




Acknowledgments


References
































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


H3H4 H2B

H2A

RNA Pol

mRNA

Active chromatin

UMUM

UM

UM

UM UM

UM

Unmethylated CpGs

A AA

M3

M2

M1

4 9 23 27
















ofhisto


ClassI

ClassII

ClassIII

ClassIV

ClassV

SUVH

SUVR

Mem

bers

Thesea

reho

mologueso

fE(Z)

(enh

ancero

fzeste

from

Drosophila

)three

E(Z)-like

proteins

are

encodedby

Arabidopsis

geno

me

CURL

YLE

AF(C

LF)

MED

EA(M

EA)

SWIN

GER

(SWN)

Thiscla

ssis

constituted

bySD

G8

SDG4

Thiscla

sscontains

homologueso

fTritho

rax

thereforemem

bersare

calledAT

X(Arabidopsis

Trith

orax-like)p

roteins1ndash5

Five

genese

ncod

eTrithorax

homologuesAT

X1ndash5

Arabidopsis

has

twomem

bers

belong

ingto

this

classA

TXR5

and

ATXR

6

SUVH(SU(VAR3-9))

Tenplantspecific

mem

bers

[SU(VAR)

3-9related]

Dom

ains

Con

tainsS

ET(sup

pressor

ofvarie

gatio

nenhancer

ofzeste

andTrith

orax)

domain

E(Z)

domain

SANTdo

main(SW13

ADA2NCO

Rand

TFIIIB-binding

)and

CXC(cysteiner

ichregion

)

Con

tain

SETdo

main

andAW

Smotif

(associatedwith

SET)

Con

tain

SETpo

st-SE

Tdo

main

PHD(plant

homeodo

main)

PWWP

(prolin

e-tryptoph

an-

tryptoph

an-prolin

e)

FYRN

(FY

rich

N-te

rminus)and

FYRC

(FY

rich

C-term

inus)

Con

tain

SET

domainandPH

Ddo

main

Con

tain

SETdo

main

pre-SE

Tdo

main

post-

SETdo

main

and

SRA(SET

andRING

fingera

ssociated

domain)

Con

tain

allother

domains

except

SRA

domain

somem

embersare

repo

rted

topo

ssessa

novelW

IYLD

domainsim

ilarto

DNA-

bind

ingprotein

Role

CLFhelpsinflo

weringtim

eregu

latio

nMEA

isinvolved

inseed

developm

ent

SWNisrequ

iredforfl

ower

developm

ent

SDG8isinvolved

inFL

Cexpressio

nwhich

regu

lates

flowering

time

SDG4isinvolved

inprop

erpo

llenand

stam

endevelopm

ent

Involved

indrou

ghtstre

ssrespon

seatx1m

utantis

hypo

sensitive

todehydration

Play

rolein

cell

cycle

regu

lation

Markinactiv

echromatingene

silencing

Potentialrolein

heterochromatic

siRNAprod

uctio

nmachinery

EpigeneticRo

leTh

eyhave

H3K

27methyltransfe

rase

activ

ity

They

carryou

tdi-or

trim

ethylatio

nof

H3K

36

ATX1

andAT

X2are

involved

inH3K

4me3

and

H3K

4me2

Functio

nof

ATX345is

stillno

tkno

wn

They

carryou

tmon

omethylatio

nof

H3K

27

H3K

9methylatio

ndifferent

SRAdo

mains

have

preferentia

laffinity

ford

ifferentcytosine

methylatio

ncontext

(sym

metric

orasym

metric

)

Functio

nun

clear

yet

howeveritresem

bles

proteins

involved

inheterochromatin

form

ation

















MM

M

H3H2A

H4H2B

M

Heterochromatin

Methylated CpGs

Inactive chromatin

M3

M2

M1 M1

M3

M2

M1

4 9 23 27

















ATPases



3 Conclusion




Acknowledgments


References
































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology



ofhisto


ClassI

ClassII

ClassIII

ClassIV

ClassV

SUVH

SUVR

Mem

bers

Thesea

reho

mologueso

fE(Z)

(enh

ancero

fzeste

from

Drosophila

)three

E(Z)-like

proteins

are

encodedby

Arabidopsis

geno

me

CURL

YLE

AF(C

LF)

MED

EA(M

EA)

SWIN

GER

(SWN)

Thiscla

ssis

constituted

bySD

G8

SDG4

Thiscla

sscontains

homologueso

fTritho

rax

thereforemem

bersare

calledAT

X(Arabidopsis

Trith

orax-like)p

roteins1ndash5

Five

genese

ncod

eTrithorax

homologuesAT

X1ndash5

Arabidopsis

has

twomem

bers

belong

ingto

this

classA

TXR5

and

ATXR

6

SUVH(SU(VAR3-9))

Tenplantspecific

mem

bers

[SU(VAR)

3-9related]

Dom

ains

Con

tainsS

ET(sup

pressor

ofvarie

gatio

nenhancer

ofzeste

andTrith

orax)

domain

E(Z)

domain

SANTdo

main(SW13

ADA2NCO

Rand

TFIIIB-binding

)and

CXC(cysteiner

ichregion

)

Con

tain

SETdo

main

andAW

Smotif

(associatedwith

SET)

Con

tain

SETpo

st-SE

Tdo

main

PHD(plant

homeodo

main)

PWWP

(prolin

e-tryptoph

an-

tryptoph

an-prolin

e)

FYRN

(FY

rich

N-te

rminus)and

FYRC

(FY

rich

C-term

inus)

Con

tain

SET

domainandPH

Ddo

main

Con

tain

SETdo

main

pre-SE

Tdo

main

post-

SETdo

main

and

SRA(SET

andRING

fingera

ssociated

domain)

Con

tain

allother

domains

except

SRA

domain

somem

embersare

repo

rted

topo

ssessa

novelW

IYLD

domainsim

ilarto

DNA-

bind

ingprotein

Role

CLFhelpsinflo

weringtim

eregu

latio

nMEA

isinvolved

inseed

developm

ent

SWNisrequ

iredforfl

ower

developm

ent

SDG8isinvolved

inFL

Cexpressio

nwhich

regu

lates

flowering

time

SDG4isinvolved

inprop

erpo

llenand

stam

endevelopm

ent

Involved

indrou

ghtstre

ssrespon

seatx1m

utantis

hypo

sensitive

todehydration

Play

rolein

cell

cycle

regu

lation

Markinactiv

echromatingene

silencing

Potentialrolein

heterochromatic

siRNAprod

uctio

nmachinery

EpigeneticRo

leTh

eyhave

H3K

27methyltransfe

rase

activ

ity

They

carryou

tdi-or

trim

ethylatio

nof

H3K

36

ATX1

andAT

X2are

involved

inH3K

4me3

and

H3K

4me2

Functio

nof

ATX345is

stillno

tkno

wn

They

carryou

tmon

omethylatio

nof

H3K

27

H3K

9methylatio

ndifferent

SRAdo

mains

have

preferentia

laffinity

ford

ifferentcytosine

methylatio

ncontext

(sym

metric

orasym

metric

)

Functio

nun

clear

yet

howeveritresem

bles

proteins

involved

inheterochromatin

form

ation

















MM

M

H3H2A

H4H2B

M

Heterochromatin

Methylated CpGs

Inactive chromatin

M3

M2

M1 M1

M3

M2

M1

4 9 23 27

















ATPases



3 Conclusion




Acknowledgments


References
































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

















MM

M

H3H2A

H4H2B

M

Heterochromatin

Methylated CpGs

Inactive chromatin

M3

M2

M1 M1

M3

M2

M1

4 9 23 27

















ATPases



3 Conclusion




Acknowledgments


References
































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


MM

M

H3H2A

H4H2B

M

Heterochromatin

Methylated CpGs

Inactive chromatin

M3

M2

M1 M1

M3

M2

M1

4 9 23 27

















ATPases



3 Conclusion




Acknowledgments


References
































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology








ATPases



3 Conclusion




Acknowledgments


References
































































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology





























































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology


























































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology
























Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology








Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

Documents

Review Article Epigenetic Dynamics: Role of Epimarks and ...downloads.hindawi.com/journals/ijg/2014/187146.pdf · Review Article Epigenetic Dynamics: Role of Epimarks and Underlying