Plant Acclimation to Environmental Stress || Epigenetic Modifications in Plants Under Adverse Conditions: Agricultural Applications

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  • 233N. Tuteja and S. Singh Gill (eds.), Plant Acclimation to Environmental Stress,DOI 10.1007/978-1-4614-5001-6_10, Springer Science+Business Media New York 2013

    1 Introduction

    Global climate change and a continuous decrease in the amount of agricultural land together with the growing demand for food production present a signi cant chal-lenge to plant breeding and crop improvement programs. Unlike the classical bread-ing approaches, plant transgenesis permits the fast improvement of economically important crops. Since plant transgenesis often involves the introduction of foreign DNA into the plant genome, its safety is frequently debated. Consequently, the com-mercial application of transgenic crops is still severely restricted in many countries.

    In very general terms, the ability to improve plant tness and increase crop yield often depends on altering genome transcription to mediate speci c agricultural characteristics or traits in the eld. While conventional breeding utilizes random mutagenesis and breeding-mediated transfer of desired traits from related species, plant transgenesis relies on relatively site-speci c and controlled gene integration events. Furthermore, it allows the introduction of genes from distant and even non-plant species. The use of both classical plant breeding and genetic engineering help achieve the desired transcriptional output of the genome by irreversibly changing the genetic composition of the plant.

    During the past decades, the attention was drawn toward elucidating the mecha-nisms that could allow genetically identical cells or even whole organisms to achieve and maintain different terminal phenotypes. This was accomplished by using differ-ent non-genetic or epigenetic determinants that could modify gene expression

    A. Boyko Institute of Plant Biology, University of Zrich , Zollikerstrasse 107 , 8008 Zrich , Switzerland

    I. Kovalchuk (*) Department of Biological Sciences , University of Lethbridge , Lethbridge , AB , Canada T1K 3M4 e-mail: igor.kovalchuk@uleth.ca

    Chapter 10 Epigenetic Modi fi cations in Plants Under Adverse Conditions: Agricultural Applications

    Alex Boyko and Igor Kovalchuk

  • 234 A. Boyko and I. Kovalchuk

    heritably (mitotically and/or meiotically) and reversibly (without changing the gene sequence encoded in DNA). These epigenetic determinants/marks are enzyme-mediated chemical modi cations of DNA and DNA-associated proteins. They include DNA methylation, histone modi cations, nucleosome positioning, and small (sm) RNAs. Epigenetic marks modify the properties of chromatin and change gene transcriptional states on the scale from the entire genome to a single speci c gene. These marks allow for greater genome plasticity which results in better adap-tation of plants to changing environmental conditions. Understanding a role of epi-genetic modi cations in plant responses to stress and adaptation and uncovering the mechanisms which mediate and guide the deposition of these modi cations through-out the genome may provide us with new insights into possible strategies to improve economically important crops. It would be of vital importance to incorporate newly acquired knowledge of epigenetic mechanisms mediating stress responses and plant adaptation into an already existing system of genetic-based knowledge and tools which would provide crop improvement.

    2 Epigenetic Modi fi cations and Gene Expression Control

    In order to be considered as an epigenetic signal, any molecular signal should sat-isfy three main criteria, including the presence of a mechanism for its propagation, evidence of transmission, and the effect on gene expression (Bonasio et al. 2010 ) . Depending on how they act, epigenetic signals can be further divided into the cis - (e.g., DNA methylation and histone modi cations) and trans -acting (e.g., smRNAs) groups. Perhaps, DNA methylation is the best and most studied example of the molecular signal which satis es all three epigenetic criteria. The ample experimen-tal evidence supports its involvement in gene expression control, mitotic and trans-generational epigenetic inheritance. DNA methylation is maintained by a highly complex network of molecular mechanisms which are very sensitive to various developmental and environmental cues. On the contrary, the current knowledge about histone modi cations and smRNAs is still far from complete. It is still debat-able whether the posttranslational modi cation of histone tails and regulation of gene expression by smRNAs are true epigenetic marks. Nevertheless, in this review, we will consider and discuss both these marks as the epigenetic ones (Table 10.1 ).

    2.1 DNA Methylation

    DNA methylation is a cis -acting repressive epigenetic signal. It involves a covalent modi cation of cytosine by a methyl group for producing 5-methyl-cytosine. Cytosine methylation can occur in several nucleotide sequence contexts, including symmetric CG and CHG and asymmetric CHH (where H is C, T, or A) sites. Methylation of CG, CHG, and CHH occurs with the frequency of 24, 6.7, and 1.7%

  • 23510 Epigenetic Modi cations in Plants Under Adverse Conditions

    Tabl

    e 10

    .1 S

    elec

    ted

    exam

    ples

    of t

    he e

    pige

    netic

    pat

    hway

    s tha

    t con

    trol a

    gric

    ultu

    rally

    impo

    rtant

    cha

    ract

    erist

    ics a

    nd tr

    aits

    Epig

    enet

    ic p

    athw

    ay

    Effe

    ctor

    pro

    tein

    Tr

    ansc

    riptio

    n Ph

    enot

    ype

    Ref

    eren

    ce

    DN

    A H

    yper

    met

    hyla

    tion

    DN

    A m

    ethy

    ltran

    s-fe

    rase

    s (M

    ET1;

    CMT3

    ; DRM

    2)

    Rep

    ress

    ion

    A tw

    o-fo

    ld in

    crea

    se in

    CH

    G m

    ethy

    latio

    n un

    der h

    igh

    salin

    ity

    condi

    tions

    was

    ass

    ocia

    ted

    with

    switc

    hing

    from

    C3

    -pho

    tosy

    nthe

    sis to

    CA

    M m

    etab

    olism

    in M

    . cry

    stal

    linum

    pl

    ants

    Dya

    chen

    ko e

    t al.

    ( 2006

    )

    An

    incr

    ease

    in D

    NA

    met

    hyla

    tion

    in th

    e ge

    nom

    ic re

    gion

    s inv

    olve

    d in

    pa

    thog

    en d

    efen

    se in

    resp

    onse

    to v

    irus i

    nfec

    tion

    in to

    mat

    o M

    ason

    et a

    l. ( 20

    08 )

    An

    age-

    depe

    nden

    t inc

    reas

    e in

    met

    hyla

    tion-

    med

    iate

    d re

    sista

    nce

    to

    blig

    ht p

    atho

    gen

    X. o

    ryza

    e in

    rice

    Sh

    a et

    al.

    ( 2005

    )

    Inse

    rtion

    and

    met

    hyla

    tion

    of th

    e M

    utat

    or -lik

    e tra

    nspo

    son

    in th

    e r

    st

    intro

    n of

    the

    FLC

    gene

    esta

    blish

    ed a

    phe

    noty

    pe o

    f ear

    ly

    ow

    erin

    g in

    Lan

    dsbe

    rg e

    rect

    a (L

    er ) ac

    cessi

    on pl

    ants

    Liu

    et a

    l. ( 20

    04 )

    DN

    A H

    ypom

    ethy

    latio

    n Pa

    ssiv

    e or

    act

    ive

    DN

    A de

    met

    hyla

    -tio

    n by

    DN

    A gl

    ycos

    ylas

    es

    (ROS

    1; DM

    E;

    DM

    L2; D

    ML3

    )

    Act

    ivat

    ion

    Tem

    pera

    ture

    -indu

    ced

    dem

    ethy

    latio

    n ac

    tivat

    ed T

    am

    3 tr

    ansp

    ositi

    on

    from

    the

    nive

    a ge

    ne p

    rom

    oter

    resu

    lting

    in th

    e re

    d- o

    wer

    phen

    otyp

    e

    Has

    hida

    et a

    l. ( 20

    03, 2

    006 )

    Tran

    spos

    on im

    mob

    iliza

    tion

    may

    resu

    lt in

    the

    form

    atio

    n of

    a n

    ew

    stre

    ss-in

    duci

    ble

    alle

    le (e

    .g., a

    n acq

    uired

    tran

    script

    ional

    respo

    nsiv

    enes

    s to

    high

    tem

    pera

    ture

    at t

    he O

    nsen

    neo

    -inse

    rtion

    site

    s)

    Ito e

    t al.

    ( 2011

    )

    Stab

    ly-in

    herit

    ed D

    NA

    hypo

    met

    hyla

    tion

    at se

    vera

    l MS-

    AFL

    P m

    arke

    r lo

    ci c

    orre

    late

    d w

    ith lo

    w re

    spira

    tion

    rate

    s, hi

    gh E

    UE

    and

    impr

    oved

    seed

    yie

    ld u

    nder

    nor

    mal

    phy

    siolo

    gica

    l and

    dro

    ught

    co

    ndi

    tions

    in c

    anol

    a pl

    ants

    Hau

    ben

    et a

    l. ( 20

    09 )

    Dem

    ethy

    latio

    n of

    the

    Xa21

    G re

    sista

    nce

    gene

    pro

    mot

    er b

    y a

    pulse

    tr

    eatm

    ent i

    n ric

    e se

    eds w

    ith 5

    -aza

    deox

    ycyt

    idin

    e res

    ulte

    d in

    the

    acqu

    isitio

    n of

    a st

    ably

    -inhe

    rited

    trai

    t of d

    iseas

    e re

    sista

    nce

    Aki

    mot

    o et

    al.

    (2009

    )

    Loci

    -spe

    ci c

    hyp

    omet

    hyla

    tion

    in th

    e gl

    obal

    ly h

    yper

    met

    hyla

    ted

    geno

    me

    med

    iate

    d th

    e in

    crea

    sed

    expr

    essio

    n of

    DN

    A tr

    ansc

    riptio

    n an

    d re

    pair

    gene

    s in

    the

    prog

    eny

    of p

    lant

    s exp

    osed

    to sa

    lt;

    Enha

    nced

    tole

    ranc

    e to

    hig

    h sa

    lt co

    ncen

    tratio

    ns a

    nd M

    MS

    acqu

    ired

    by th

    e pr

    ogen

    y of

    pla

    nts e

    xpos

    ed to

    salt

    Boy

    ko e

    t al.

    ( 2010

    a ; 2

    010b

    )

    (conti

    nued

    )

  • 236 A. Boyko and I. Kovalchuk

    Epig

    enet

    ic p

    athw

    ay

    Effe

    ctor

    pro

    tein

    Tr

    ansc

    riptio

    n Ph

    enot

    ype

    Ref

    eren

    ce

    Hist

    one

    deac

    etyl

    atio

    n H

    DA

    6, H

    iston

    e de

    acet

    ylas

    e R

    epre

    ssio

    n A

    ctiv

    ity o

    f HD

    A6

    is in

    duce

    d by

    jasm

    onic

    acid a

    nd et

    hylen

    e Zh

    ou e

    t al.

    ( 2005

    )

    HD

    A19

    , Hist

    one

    deac

    etyl

    ase

    The

    incr

    ease

    d ex

    pres

    sion

    of th

    e ER

    F1 an

    d PR

    ge

    nes a

    nd e

    nhan

    ced

    resis

    tanc

    e to

    fung

    al p

    atho

    gen

    in tr

    ansg

    enic

    pla

    nts t

    hat o

    vere

    xpr

    ess H

    DA1

    9

    Zhou

    et a

    l. ( 20

    05 )

    Dow

    n-re

    gula

    tion

    of li

    ght-r

    espo

    nsiv

    e an

    d ph

    otom

    orph

    ogen

    esis

    gene

    s B

    enha

    med

    et a

    l. ( 20

    06 )

    AtH

    D2C

    , Hist

    one

    deac

    etyl

    ase

    Incr

    ease

    d to

    lera

    nce

    to sa

    linity

    and

    dro

    ught

    con

    ditio

    ns in

    tran

    sgen

    ic

    plan

    ts th

    at o

    vere

    xpre

    ss A

    tHD

    2C

    Srid

    ha a

    nd

    Wu

    ( 2006

    ) H

    OS1

    5, W

    D-4

    0 do

    mai

    n pr

    otei

    n;

    inte

    ract

    s with

    hi

    stone

    H4

    Free

    zing

    stre

    ss-h

    yper

    sens

    itive

    phe

    noty

    pe in

    hos

    15 m

    uta

    nts

    Zhu

    et a

    l. ( 20

    07b )

    Hist

    one

    acet

    ylat

    ion

    GCN

    5, H

    iston

    e ac

    etyl

    trans

    fera

    se

    prot

    ein

    Act

    ivat

    ion

    Up-

    regu

    latio

    n of

    ligh

    t-res

    pons

    ive

    and

    phot

    omor

    phog

    enes

    is ge

    nes

    Ben

    ham

    ed e

    t al.

    ( 2006

    ) A

    ctiv

    atio

    n of

    col

    d-re

    spon

    sive

    gene

    tran

    scrip

    tion

    Stoc

    king

    er e

    t al.

    ( 2001

    ) H

    AF2

    , Hist

    one

    acet

    yltra

    nsfe

    rase

    pr

    otei

    n

    Up-

    regu

    latio

    n of

    ligh

    t-res

    pons

    ive

    and

    phot

    omor

    phog

    enes

    is ge

    nes

    Ben

    ham

    ed e

    t al.

    ( 2006

    )

    HA

    C1, H

    iston

    e ac

    etyl

    trans

    fera

    se

    Tran

    scrip

    tiona

    l up-

    regu

    latio

    n of

    the

    heat

    -sho

    ck g

    ene

    HSP

    17

    Bha

    rti e

    t al.

    ( 2004

    )

    Tabl

    e 10

    .1

    (conti

    nued

    )

  • 23710 Epigenetic Modi cations in Plants Under Adverse Conditions Ep

    igen

    etic

    pat

    hway

    Ef

    fect

    or p

    rote

    in

    Tran

    scrip

    tion

    Phen

    otyp

    e R

    efer

    ence

    H

    iston

    e m

    ethy

    latio

    n Po

    lyco

    mb

    grou

    p ( P

    c G) p

    rote

    ins,

    Hist

    one

    met

    hyltr

    ansf

    eras

    e

    Rep

    ress

    ion

    Tran

    scrip

    tiona

    l up-

    regu

    latio

    n of

    col

    d-re

    spon

    sive

    gene

    s CO

    R15A

    an

    d AT

    GO

    LS3

    med

    iate

    d by

    a d

    ecre

    ase

    in H

    3K27

    me3

    K

    won

    et a

    l. ( 20

    09 )

    MSI

    1, W

    D-4

    0 do

    mai

    n pr

    otei

    n;

    subu

    nit o

    f PRC

    2 co

    mpl

    ex

    Dro

    ught

    stre

    ss to

    lera

    nce

    in m

    si1-

    cs tr

    ansg

    enic

    pla

    nts

    Ale

    xand

    re e

    t al.

    ( 2009

    )

    Trith

    orax

    gro

    up

    (trxG

    ) prot

    eins,

    Hist

    one

    met

    hyltr

    ansf

    eras

    e

    Act

    ivat

    ion

    Tran

    scrip

    tiona

    l act

    ivat

    ion

    of d

    roug

    ht st

    ress

    -indu

    cibl

    e ge

    nes

    med

    iate

    d by

    the

    enric

    hmen

    t in

    H3K

    4me3

    K

    im e

    t al.

    ( 2008

    )

    Hyp

    oxia

    stre

    ss to

    lera

    nce

    in th

    e su

    bmer

    ged

    rice

    seed

    lings

    via

    the

    enha

    nced

    exp

    ress

    ion

    of th

    e AD

    H1

    and

    PDC1

    ge

    nes m

    edia

    ted

    by th

    e en

    richm

    ent i

    n H

    3K4m

    e3

    Tsuji e

    t al. (

    2006

    )

    Hist

    one

    varia

    nts

    HIS

    1-S,

    Hist

    one

    1 var

    iant

    N

    /A

    Alle

    viat

    es n

    egat

    ive

    effe

    cts o

    f dro

    ught

    stre

    ss b

    y re

    duci

    ng tr

    ansp

    iratio

    n ra

    tes w

    hen

    pres

    ent i

    n ch

    rom

    atin

    of w

    ilted

    tom

    ato

    leav

    es

    Scip

    pa e

    t al.

    ( 2004

    ) H

    IS1-

    3, H

    iston

    e 1

    var

    iant

    Im

    prov

    ed d

    roug

    ht to

    lera

    nce

    and

    ABA

    -hyp

    erse

    nsiti

    vity

    phe

    noty

    pes

    in tr

    ansg

    enic

    pla

    nts t

    hat o

    vere

    xpre

    ss a

    n ac

    tive

    form

    of A

    REB1

    , a

    posit

    ive

    regu

    lato

    r of H

    IS1-

    3

    Fujita

    et al

    . ( 200

    5 )

    H2A

    .Z, H

    iston

    e H

    2A

    var

    iant

    D

    epen

    ds o

    n

    the

    inte

    r-ac

    ting

    tran

    scrip

    -tio

    n fa

    ctor

    s

    Enric

    hed

    with

    in tr

    ansc

    riptio

    n sta

    rt sit

    es o

    f hig

    h te

    mpe

    ratu

    re st

    ress

    -re

    spon

    sive

    gene

    s K

    umar

    et a

    l. (20

    10)

    Dow

    n-re

    gula

    tion

    of th

    e ex

    pres

    sion

    of p

    hosp

    hate

    -sta

    rvat

    ion

    resp

    onse

    ge

    nes

    Smith

    et a

    l. ( 20

    10 )

    Dow

    n-re

    gula

    tion

    of g

    enes

    med

    iatin

    g sy

    stem

    ic a

    cqui

    red

    resis

    tanc

    e in

    Ar

    abid

    opsis

    Mar

    ch-D

    az

    et a

    l. ( 20

    08 )

    Up-

    regu

    late

    d FL

    C tr

    ansc

    riptio

    n an

    d re

    pres

    sion

    of

    ower

    ing

    upon

    the

    enric

    hmen

    t in

    the

    H2A

    .Z v

    aria

    nt a

    t the

    FLC

    ge

    ne lo

    ci

    Dea

    l et a

    l. ( 20

    07 )

  • 238 A. Boyko and I. Kovalchuk

    of all genome-wide sites available, respectively. The DNA methylation landscapes are largely responsible for the transcriptional genome output and can direct the deposition of other epigenetic marks and chromatin remodeling (Zilberman et al. 2007 ) . While CG methylation represents a very stable epigenetic mark that can be faithfully preserved throughout multiple rounds of cell division and

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