OMICS A Journal of Integrative Biology
Volume 15, Number 12, 2011
ª Mary Ann Liebert, Inc.
DOI: 10.1089/omi.2011.0095
Transcription Regulation of Abiotic Stress
Responses in Rice: A Combined Action of Transcription
Factors and Epigenetic Mechanisms
Ana Paula Santos, Tânia Serra, Duarte D. Figueiredo, Pedro Barros, Tiago Lourenço,
Subhash Chander, Maria Margarida Oliveira, and Nelson J.M. Saibo
Abstract
Plant growth and crop production are highly reduced by adverse environmental conditions and rice is particularly sensitive to abiotic stresses. Plants have developed a number of different mechanisms to respond and try to
adapt to abiotic stress. Plant response to stress such as drought, cold, and high salinity, implies rapid and
coordinated changes at transcriptional level of entire gene networks. During the last decade many transcription
factors, belonging to different families, have been shown to act as positive or negative regulators of stress
responsive genes, thus playing an extremely important role in stress signaling. More recently, epigenetic mechanisms have been also involved in the regulation of the stress responsive genes. In this review, we have performed a comprehensive analysis of the rice transcription factors reported so far as being involved in abiotic stress
responses. The impact of abiotic stresses on epigenomes is also addressed. Finally, we update the connections
made so far between DNA-binding transcription factors (TFs), and epigenetic mechanisms (DNA methylation
and histones methylation or acetylation) emphasizing an integrative view of transcription regulation.
Introduction
R
ice production is severely affected by adverse environmental conditions, such as drought, submergence,
and salinity, and the climate change is expected to raise carbon dioxide levels, temperatures, and to increase the frequency of flooding. Given that rice is one of the world’s most
important staple food, providing 30% of the calories consumed in Asian countries, it is important to better understand
the molecular mechanisms underlying tolerance to abiotic
stresses. Plant response to environmental changes is associated with changes in signaling molecules [e.g., sugars, hormones, calcium, reactive oxygen species (ROS), nitrous oxide
(NO)] (Tuteja and Sopory, 2008), but also with large-scale
genomic restructuring (McClintock, 1984), including transposon activation (Cheng et al., 2006), and rapid changes on
gene expression patterns (e.g., genes encoding transcription
factors) (Wang et al., 2011a).
Many transcription factors (TFs) from different plants have
been shown to play central roles in abiotic stress responses.
The ability of TFs in acting as master regulators has been
regarded as a sustainable approach to modify complex traits
in crop plants (Century et al., 2008). In the previous decade,
diverse TF families such as AP2/ERF, bZIP, Zn-finger,
NAC, MYB, and WRKY have been described as playing a
major role in abiotic stress tolerance (Century et al., 2008;
Hirayama and Shinozaki, 2010; Saibo et al., 2009). In rice,
three major strategies have been used to identify TFs associated with abiotic stress responses: comparative genomics—
abiotic stress-responsive genes from Arabidopsis and maize
were used to identify rice orthologs; forward genetics—genes
related with traits, such as drought or hypoxia tolerance, were
identified through association mapping; genome-wide expression profiles—transcriptome analysis using microarrays
have been used to identify novel abiotic stress responsive
genes.
Chromatin remodeling and nuclear organization has been
also involved in plant response to stress (Kim et al., 2010). For
example, in rice and wheat the salinity and heat-shock stresses
caused decondensation of interphase ribosomal chromatin
(Santos et al., 2011). Heterochromatin maintenance mechanisms may repress transcription under normal conditions but,
under stress, those mechanisms may fail causing chromatin
remodeling and novel patterns of gene expression (ArnholdtSchmitt, 2004; Madlung and Comai, 2004).
Environmental epigenetics refers to the impact of stresses
on epigenetic marks in the genome, with consequences on
gene expression control (Chinnusamy and Zhu, 2009). An
Instituto de Tecnologia Quı́mica e Biológica, Universidade Nova de Lisboa and Instituto de Biologia Experimental e Tecnológica, Oeiras.
Portugal.
839
840
epigenetic memory can be achieved through the interplay of
several molecular mechanisms such as DNA methylation,
posttranslational modifications of the N-terminal regions of
nucleosome core histone proteins and chromatin remodeling
(Zhang, 2008). Although many proteins have been shown to
modulate the epigenetic response to environmental stresses,
namely, TF-interacting proteins, only a few were already reported in rice. Rice epigenetic factors have been identified
mainly through comparative genomics.
In this review we discuss the most recent findings on the
transcriptional control of abiotic stress responses with special
focus on rice. First, a comprehensive updated list of the rice
TFs is described and then epigenetic changes occurring in
response to abiotic stress are referred. The discussion section
is mainly dedicated to the crosstalk between TFs and epigenetic mechanisms underlying regulation of gene expression in
abiotic stress responses.
Rice Transcription Factors Known To Be Involved
in Abiotic Stress Responses
Many rice TFs, belonging to different families, have been
shown to be involved in abiotic stress (e.g., drought, salinity,
cold, heat, and hypoxia) responses. Although numerous reports are only based on gene expression analysis (Supplementary Table S1), a number of abiotic stress-related TFs have
already been functionally characterized through transgenic/
mutant lines (Table 1). Although Supplementary Table S1
only includes validated gene expression data, our discussion
will mainly consider Table 1. The total number of TF family
members (in rice and other plant species with completed sequenced genomes) is shown in Supplementary Table S2.
AP2/ERF family
The AP2/ERF (APETALA2/ethylene response factor)
family of transcription factors is characterized by the presence
of the highly conserved AP2 DNA-binding domain (Dietz
et al., 2010). This family was initially characterized as plant
specific; nevertheless, there are evidences suggesting that a
horizontal transfer of an HNH-AP2 endonuclease from bacteria or viruses may be related to the origin of this TF family
(Magnani et al., 2004). Several AP2/ERF TFs have been isolated from various plants such as rice (Dubouzet et al., 2003),
Arabidopsis (Sakuma et al., 2002), tobacco (Wu et al., 2007),
wheat (Agarwal et al., 2006), and poplar (Dietz et al., 2010).
Based on the similarity of the DNA binding domains, this
family is divided in five subfamilies: AP2, RAV, ERF, DREB,
and ‘‘others’’ (Sakuma et al., 2002). The AP2 subfamily contains two AP2 DNA-binding domains and is mainly involved
in plant development (Dietz et al., 2010). Proteins containing a
single AP2 domain and a B3 DNA binding domain are classified as members of the RAV subfamily. In Arabidopsis,
members of this subfamily were shown to be mainly involved
in plant development, but may also have a function in abiotic
stress responses (Swaminathan et al., 2008; Woo et al., 2010).
In rice, a RAV-like gene was identified, RAVL1, and shown to
coordinate the brassinosteroid biosynthetic and signaling
pathways, indicating a putative function in plant development ( Je et al., 2010).
The DREB and ERF regulatory proteins contain a single
AP2 DNA-binding domain, being characterized as regulators
of biotic and/or abiotic stress responses. These subfamilies
SANTOS ET AL.
can be distinguished by their DNA binding specificity. DREB
proteins interact with the DRE/CRT cis-element usually
present in the promoter of genes involved in cold, drought,
and high salinity responses. ERF proteins usually interact
with the GCC box element present in several pathogenesisrelated (PR) genes; nevertheless, other reports have suggested
that this TFs can also bind to DRE elements (Sakuma et al.,
2002; Xu et al., 2008b). In rice, most AP2/ERF proteins involved in biotic and abiotic stress responses belong to the
ERF or DREB subfamilies. The ERF proteins were initially
designated ethylene-responsive element binding proteins
(EREBPs) due to their putative involvement in ethylene responses (Ohmetakagi and Shinshi, 1995). These proteins were
able to bind to the GCC box element present in PR genes,
suggesting a role in disease resistance responses (Gutterson
and Reuber, 2004; Ohmetakagi and Shinshi, 1995; Zhou et al.,
1997). Studies in Arabidopsis, tobacco, and tomato have shown
that overexpression of ERF genes conferred resistance to
fungal and bacterial pathogens (Xu et al., 2008b). Recent
studies have also revealed the role of some ERF proteins in
abiotic stress responses. OsBIERF2 (BENZOTHIADIAZOLEINDUCED ERF 2) overexpression in rice enhanced tolerance
to drought, high salinity, and low temperature (Oh et al.,
2009). In field conditions, the same transgenic plants showed
increased grain yield under drought stress conditions. ERF
proteins identified in rice were shown to be involved in both
biotic and abiotic stress responses. OsBIERF1, OsBIERF3, and
OsBIERF4 were induced by pathogen infection and also by
cold, drought, and salt stress (Supplementary Table S1) (Cao
et al., 2005, 2006). Moreover, overexpression of OsBIERF3
enhanced disease resistance against viral and bacterial pathogens, and improved tolerance to drought and high salinity
(Cao et al., 2005). Multifunctional ERF genes responding to
biotic and abiotic stress stimuli were also identified in pepper,
CaPF1 (Capsicum annuum Pathogen and Freezing ToleranceRelated Protein) (Xu et al., 2007), and wheat, TaERF1 (Yi et al.,
2004). The ERF subfamily also includes genes whose expression is induced by hypoxia. SUB1A, SUB1B, and SUB1C belong to the quantitative trait locus Submergence-1 (Sub1)
involved in rice submergence tolerance. SUB1A has two alleles and was shown to be present only in indica cultivars. The
allele carried by the cultivar will define its susceptibility to
submergence (Fukao et al., 2006). Introgression of SUB1A in
japonica cultivars increased tolerance to submergence and also
to drought stress (Fukao et al., 2011).
Transcription factors belonging to the DREB subfamily
have been extensively studied in several plants, such as Arabidopsis, rice, wheat, tomato, and barley (Agarwal et al., 2006;
Dietz et al., 2010; Yamaguchi-Shinozaki and Shinozaki, 2006).
Based on studies in Arabidopsis this subfamily was further
divided in two subclasses, DREB1/CBF and DREB2, according to their transcriptional response to abiotic stress conditions (Agarwal et al., 2006; Yamaguchi-Shinozaki and
Shinozaki, 2006). The initially identified DREB1/CBF genes,
DREB1A, DREB1B, and DREB1C were rapidly and transiently
induced by cold, but not by drought or high salt stress, suggesting that in Arabidopsis they may be involved in cold stress
responses. Contrastingly, DREB2 genes, DREB2A and
DREB2B, were induced by drought and high salt, but not by
cold, indicating a putative function in the tolerance to drought
and high salt stress (Agarwal et al., 2006; Nakashima et al.,
2009). The identification of new members of the DREB1/CBF
841
+
+
0
+
0
OsDREB1D
OsDREB1E
OsDREB2A
OsDREB2B
AS form 1
OsDREB2B
AS form 2
ARAG1
OsBIERF2,
AP37,OsERF3
OsBIERF3, AP59
Os06g06970
Os04g48350
Os01g73770
Os08g43210
Os01g07120
Os05g27930
Os05g27930
Os04g46410
Os01g58420
OsDREB1G
MYB
+
+
ND
OsDREB1F
+
+
0
0
+
ND
+
+
+
+
0
+
0
0
+
+
OsMYB4
MYBS3
Os04g43680
Os10g41200
+
0
0
ND
0
+
+
ND
OsRAF
SUB1A
Os03g08470
+
+
+
0
ND
ND
BGIOSGA038325
Os02g43790
ND
-
ND
+
0
+
0
Os09g35010
+
0
0
ND
ND
ND
ND
ND
+
0
+
ND
ND
ND
ND
+
ND
Cold Drought Salt Heat
OsDREB1B
TF Family
AP2/ERF
+
Gene
OsDREB1A
Os09g35030
+
Locus
-
0
-
0
-
0
+
ND
ND
0
ND
+
-
0
0
- /0
ABA
ND
0
+
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
Hypoxia
Gene expression under abiotic stress
Binds to the OsDREB1B and aAmy3
promoter and represses
transcription.
Osmyb4 transactivates the PAL2,
ScD9 SAD cold inducible
promoters
ND
ND
Binds to GCC-box in vitro.
ND
ND
OsDREB2B1 did not bind to DRE in
Arabidopsis protoplasts.
Binds to DRE and activates
transcription in yeast.
Binds to DRE and activates
transcription in yeast.
Binds to DRE in vitro and activates
transcription in yeast.
Binds to DRE in vitro and activates
transcription in rice protoplasts.
No significant DRE
transactivation in Arabidopsis
protoplasts and with the GAL4
system in rice protoplasts.
OsDREB2B2 binds to DRE and
activates transcription in
Arabidopsis protoplasts.
GUS expression driven by
OsDREB1B promoter in response
to cold, ABA, drought, salt,
methyl viologen, and salicylic
acid.
Binds to DRE and LTRE and
activates transcription in yeast.
Binds to DRE in vitro and activates
transcription in rice protoplasts.
Molecular studies
OX in rice improved cold tolerance. Rice
knockdown lines displayed cold
sensitivity.
Rice knockdown lines did not show
phenotypical changes.
OX in japonica rice improves submergence
tolerance. Introgression in japonica rice
improves drought and submergence
tolerance. OX in rice increases ABA
sensitivity. OX in Arabidopsis decreases
ABA sensitivity.
Overexpression in Arabidopsis and apple
improves cold and drought tolerance.
Overexpression in tomato improves
drought tolerance.
OX in Arabidopsis improved drought and heat
tolerance. OsDREB2B2 stress-inducible
expression improved drought tolerance.
Rice knockdown lines hypersensitive to ABA
and slightly sensitive to drought. OX in
rice slightly improves drought tolerance
but did not affect ABA sensitivity.
OX in rice improves salt, drought and low
temperature tolerance.
OX in rice improves salt and drought
tolerance. OX in tobacco improves salt
tolerance.
OX in Arabidopsis did not induce
phenotypical changes; in rice improved
drought tolerance.
OX in Arabidopsis did not induce target stressinducible genes.
OX in Arabidopsis enhances salt, drought and
freezing tolerance. OX in rice improves
salt, drought and cold tolerance.
OX in rice improves tolerance to salt, cold and
drought. OX in Arabidopsis improves
freezing and heat tolerance. OX in tobacco
improves drought, salt, and freezing
tolerance.
OX in Arabidopsis improves cold and salt
tolerance and decreases sensitivity to
ABA.
OX in rice slightly improves drought
tolerance.
OX in Arabidopsis and rice improves salt,
drought and cold tolerance.
OX in rice improves drought tolerance.
Functional analysis
aAmy3 and
OsDREB1B.
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
Targets
Involved in sugar
metabolism.
Possible role in
ethylene responses.
Involved in plant
development,
carbohydrate
metabolism,
ethylene and GA
signalling.
Involved in biotic
stress responses.
Involved in biotic
stress responses.
ND
ND
ND
ND
ND
ND
ND
ND
ND
Possible role in biotic
stress responses
(wounding).
Involved in biotic
stress responses
and radical
scavenging.
Crosstalk
(continued)
(Fukao et al., 2006; Xu
et al., 2006; Fukao
and Bailey-Serres,
2008; Fukao et al.,
2011; Pena-Castro
et al., 2011)
(Vannini et al., 2004;
Mattana et al.,
2005; Vannini
et al., 2006;
Vannini et al.,
2007; Pasquali
et al., 2008;
Agarwal and Jha,
2010)
(Su et al., 2010)
(Cao et al., 2006; Oh
et al., 2009)
(Cao et al., 2005; Cao
et al., 2006; Oh
et al., 2009; Fukao
et al., 2011)
(Hu et al., 2008b)
(Chen et al., 2008;
Matsukura et al.,
2010)
(Zhao et al., 2010)
(Chen et al., 2008;
Matsukura et al.,
2010)
(Dubouzet et al., 2003;
Matsukura et al.,
2010)
(Chen et al., 2008)
(Chen et al., 2008;
Fukao et al., 2011)
(Wang et al., 2008)
(Dubouzet et al., 2003;
Zhang et al., 2009)
(Dubouzet et al., 2003;
Ito et al., 2006;
Fukao et al., 2011)
(Dubouzet et al., 2003;
Ito et al., 2006; Qin
et al., 2007; Gutha
and Reddy, 2008)
Reference
Table 1. List of Rice Transcription Factors Functionally Characterized, Through Transgenic/Mutant Lines, Regarding Abiotic Stress Tolerance
842
OsABF3, OsABF2
OsbZIP46
ABL1
OsbZIP72,
OsABF4
OsWRKY11
Os06g10880
Os06g10880
Os09g28310
OsWRKY13
WRKY45
OsWRKY08
(OsWRKY8v2)
Os01g54600
(EF143611
–indica)
Os05g25770
Os05g50610
Os01g43650
OsbZIP23
Os02g52780
WRKY
ND
+ /0
+
+
+
+
+
+ /0
+
ND
+
ND
-
+/-
0
+
+
+
+
+
+
+
+
+
+
+ /0
+
OsABF1,
OsbZIP12
Os01g64730
+
+
+
+/-
0
OsABI5, OsbZIP10
Os01g64000
+/-
ZFP252
Os12g39400
bZIP
0
+
+
ZFP245
Os07g39870
+
ND
ND
+
+
+
ZFP182
Os03g60560
+
0
+
-
+
ND
+
ND
ND
ND
ND
ND
ND
ND
ND
ND
Cold Drought Salt Heat
ND
Zinc Finger C2H2
TF Family
ND
DST
Os03g57240
Gene
OsMYB3R-2
Locus
Os01g62410
+
0/ + / -
ND
ND
+ /0
ND
+
+
+
+
0
ND
+
ND
ND
ABA
ND
ND
ND
ND
ND
ND
ND
ND
+
ND
ND
ND
ND
ND
ND
Hypoxia
Gene expression under abiotic stress
ND
Induced by benzothiadiazole (BHT).
Expressed in all tissues under
control conditions.
ND
Expressed in roots, shoots, stem,
mature leave, flag leave, and
panicle. Binds to ABRE and
activates transcription.
Expressed mainly in coleoptiles and
primary roots. Binds to ABRE.
Binds to ABRE and activates
transcription.
Expressed mainly in panicles under
control conditions
Expressed in mature pollen. Two
splice forms, with different
transactivation and DNA
binding activity. Binds to G-box.
Both proteins interact with each
other and with OsVP1.
Binds to ABRE and activates
transcription. Expressed in
schlerenchyma and epidermal
silica cells and immature leafs.
Expressed mainly in leaves.
Activates transcription.
ND
Constitutively expressed in leaves,
culms, roots and spikes in adult
plants.
Activates transcription.
Binds to conserved DNA motif and
activates transcription.
Binds to the OsCycB1 promoter
in vitro.
Molecular studies
Table 1. (Continued)
Functional analysis
OX in rice leads to enhanced resistance to
blast infection via BTH-inducible
responses. OX in Arabidopsis leads to
enhanced tolerance to drought and high
salinity. Decreased sensitivity to ABA in
germination and seedling growth.
OX in Arabidopsis leads to enhanced osmotic
stress tolerance. The results are not clear.
OX in rice leads to higher sensitivity to salt
and cold. Enhanced resistance to biotic
stress.
OX in rice with promHSP101– tolerance to
heat and drought.
Mutant is ABA-insensitive. OX in Arabidopsis
rescues abi5 ABA insensitive phenotype.
OX in rice improves drought tolerance.
OX in rice induces tolerance to drought and
salt, hypersensitivity to ABA. Mutant has
low tolerance to salt and drought, and
decreased sensitivity to ABA.
Rice mutant is more sensitive to salt, drought
and oxidative stress, and has reduced
sensitivity to ABA.
Rice mutants are more sensitive to salinity
and dehydration.
OX in rice improves cold and drought
tolerance and causes ABAhypersensitivity.
OX in rice improves salt and drought
tolerance.
OX in rice increases sensitivity to salt. RNAi
lines have decreased fertility, increased
tolerance to salt and drought. OX in
Arabidopsis results in ABA
hypersensitivity.
OX in tobacco and rice improves salt
tolerance.
OX in rice improves cold tolerance. OX in
Arabidopsis improves cold, drought and
salt tolerance. Seed germination
insensitive to ABA.
Rice mutant is drought- and salt-tolerant, has
thicker leaves, lower stomata density and
closed stomata.
ND
GST and a
cytochrome
P450
PR1a, AOS2, LOX,
OsWRKY24,
42, 45, 51, 74
ND
Os01g50100,
Os08g29660
LEA3 and Rab16
ND
ND
ND
ND
ND
OsP5CS and
OsProT.
ND
Biotic stress
Biotic stress
Involved in auxin
signalling.
Induced by ACC and
MeJA
ND
Induced by ACC.
GA3 antagonizes gene
induction by ABA.
Induced by ACC
and MeJA.
Induced by ACC.
Role in fertility:
Involved in pollen
development.
ND
ND
ND
Involved in H2O2induced stomata
closure.
Cytochrome P450
71D10,
Peroxidase 24
Precursor
ND
Crosstalk
Involved in cell-cycle
regulation.
Targets
OsCycB1
Reference
(continued)
(Qiu et al., 2004; Song
et al., 2009)
(Shobbar et al., 2008;
Lu et al., 2009)
(Ramamoorthy et al.,
2008; Wu et al.,
2009)
(Qiu et al., 2004; Qiu
et al., 2007; Cai
et al., 2008; Qiu
et al., 2009)
(Qiu et al., 2004; Ryu
et al., 2006;
Shimono et al.,
2007; Qiu and Yu,
2009)
(Shobbar et al., 2008;
Lu et al., 2009;
Hossain et al.,
2010a)
(Yang et al., 2011)
(Shobbar et al., 2008;
Lu et al., 2009;
Hossain et al.,
2010b)
(Xiang et al., 2008; Lu
et al., 2009)
(Zou et al., 2007, 2008;
Lu et al., 2009)
(Xu et al., 2008a)
(Huang et al., 2009a)
(Huang et al., 2007)
(Huang et al., 2009b;
Song and
Matsuoka, 2009)
(Dai et al., 2007; Ma
et al., 2009)
843
+
0
OsNAC52/
ONAC088
ONAC063
OsNAC10
Os05g34830
Os08g33910
Os11g03300
OsbHLH2/
OsICE1
Os11g32100
ND
+
+
ND
ND
ND
ND
ND
+
+
+
ND
ND
+
+
+
ABA
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
ND
Hypoxia
Molecular studies
Functional analysis
ND
ND
OX in Arabidopsis resulted in conferred
increased tolerance to salt and osmotic
stress.
Stress-responsive genes DREB1A/
CBF3, RD29A, COR15A and
KIN1 were up regulated in
transgenic plants
ND
OsLEA3
ND
ND
ND
ND
ND
ND
HVA22
Targets
OX in Arabidopsis resulted in thermotolerance
to transient heat and salt tolerance.
OX in Arabidopsis with higher basal
thermotolerance, not acquired.
OX in rice enhances tolerance to drought and
high-salinity
OX in rice – tolerance to high salinity and
drought
Arabidopsis OX the gene are hypersensitive to
ABA and more tolerant to dehydration.
OX in Arabidopsis resulted in thermotolerance
and higher germination rate under
salinity stress
OX in rice under GOS2 (constitutive
promoter) and the RCc3 (root-specific)
increased the plant tolerance to drought,
high salinity, and low temperature at the
vegetative stage.
OX in rice: improved tolerance to drought
and salt. More sensitive to ABA, with
increased stomata closure.
OX in Arabidopsis leads to enhanced
sensitivity to ABA, salt and osmotic
stresses and sugar starvation
OX in rice: improved tolerance to cold,
dehydration and salt. More sensitive to
ABA.
Activates transcription
Expressed in root and panicles.
RCc3:OsNAC10 plants showed
enhanced drought tolerance at
the reproductive stage due to
differences in expression of
OsNAC10-dependent target
genes in roots and leaves
Expressed in roots and leaves.
Activates transcription.
Northern blot. Shows transcriptional
activity in yeast but not in rice
protoplasts
Express in leaves & flowers (qRTPCR)
Increased expression mainly in
roots. Activates transcription.
Particularly induced in stomata
guard cells. Induced by blast,
MeJA and ethylene. Activates
transcription.
ND
Induced by wounding. Tissuespecific expression according to
stress. Transcriptional activator
Expressed in aleurone cells.
Promotes transcription.
Plus, minus, and zero correspond to upregulation, downregulation and not regulated, respectively.
ND, not determined; OX, overexpressed.
ND
ND
+
OsHsfA2e
Os03g58160
ND
+
+
0
OsHSF7/
OsHsfA2d
Os03g06630
HLH
+
+
+
OsNAC5
0
+
+
+
ONAC045
Os11g08210
HSF
+
+
+
0
+
ND
ND
+
ND
ND
+
0
Os11g03370
0
0
+
+
+
SNAC1/
OsNAC19
Os03g60080
+
+
+
NAC
SNAC2/ OsNAC6
Os01g66120
+
Cold Drought Salt Heat
+
TF Family
0
Gene
OsWRKY72
Os11g29870
Locus
Gene expression under abiotic stress
Table 1. (Continued)
Crosstalk
ND
ND
ND
ND
ND
ND
ND
ND
Auxin transport
pathway. Sugar
signalling.
Biotic stress
(overexpression
increases tolerance
to blast disease)
Reference
(Baniwal et al., 2004;
Yokotani et al.,
2008; Liu et al.,
2009; Mittal et al.,
2009; Liu et al.,
2010)
(Yokotani et al., 2008;
Mittal et al., 2009;
Liu et al., 2010)
(Zhou et al., 2009)
(Zheng et al., 2009)
(Fang et al., 2008)
(Takasaki et al., 2010)
( Jeong et al., 2010)
(Gao et al., 2010) (Fang
et al., 2008)
(Yokotani et al., 2009)
(Hu et al., 2008a),
(Takasaki et al.,
2010), (Nakashima
et al., 2007),
(Ohnishi et al.,
2005)
(Hu et al., 2006), (Lin
et al., 2007)
(Xie et al., 2005; Yu
et al., 2010)
844
subclass, DREB1D and DREB1F, which respond to drought
and salt stress, respectively, may suggest a crosstalk between
DREB1/CBF and DREB2 pathways in response to those abiotic stresses (Haake et al., 2002; Nakashima et al., 2009;
Sakuma et al., 2002). In rice, several DREB1 and DREB2 orthologs were shown to play a role in abiotic stress responses.
The rice DREB1A orthologs, OsDREB1A and OsDREB1B,
were differently expressed in response to abiotic stress. Rice
genes were induced by cold, but also by drought and high salt
conditions (Dubouzet et al., 2003; Ito et al., 2006). OsDREB1B
was also shown to respond to heat stress, suggesting a role in
the response to this abiotic stress (Qin et al., 2007). Furthermore, the overexpression of OsDREB1A and OsDREB1B in
rice resulted in tolerance phenotypes similarly to Arabidopsis
plants overexpressing the DREB1A (Ito et al., 2006; Nakashima et al., 2009). Rice DREB2 genes, OsDREB2A and OsDREB2B, showed a similar response to drought and salt, but
OsDREB2B was also induced by cold, suggesting a putative
role of DREB2 proteins in cold responses (Matsukura et al.,
2010). Furthermore, OsDREB2B was shown to be regulated at
the posttranscriptional level by alternative splicing (Matsukura et al., 2010). A similar mechanism of regulation was also
found for DREB2 proteins in barley, wheat, and maize (Nakashima et al., 2009). Most of the DREBs are involved in ABAindependent stress responses; however, some studies have
reported DREBs that are responsive to ABA (Haake et al.,
2002; Yamaguchi-Shinozaki and Shinozaki, 2006). For instance, OsDREB1F and ABA RESPONSIVE AP2-LIKE
(ARAG1) gene expression was shown to be upregulated in
response to ABA. Moreover, the ARAG1 knockdown line
displayed hypersensitivity to ABA and drought, suggesting a
role of this TF in the ABA-dependent drought stress response
(Zhao et al., 2010). Interestingly, a possible role of rice DREB
proteins in biotic stress responses was reported. OsDREB1B
overexpression in tobacco improved plant resistance to virus
infection and induced the expression of several PR genes
(Gutha and Reddy, 2008). Only few DREB proteins were involved in biotic stress responses. In Arabidopsis, DREB2A gene
expression was upregulated in ACTIVATED DISEASE RESISTANCE 1 (ADR1) overexpression lines (Agarwal et al.,
2006).
MYB family
MYB transcription factors are characterized by the presence
of MYB repeats (R) involved in DNA-binding and proteinprotein interactions (Feller et al., 2011). MYB proteins were
initially identified in animals, but similar proteins are reported in insects, plants (Supplementary Table S2) and fungi
(Stracke et al., 2001). In plants, MYB proteins can be classified
into three subfamilies, R-MYB, R2R3-MYB, and R1R2R3-MYB
(MYB3R) depending on the presence of one, two, or three
tandem MYB repeats, respectively (Feller et al., 2011). Several
members of this family were identified in rice, Arabidopsis,
maize, and soybean, and shown to be involved in a wide
variety of cell processes, such as cell cycle and cell morphogenesis (Feller et al., 2011; Jin and Martin, 1999; Stracke et al.,
2001). MYB proteins were also reported to be involved in
biotic and abiotic stress responses. Studies in soybean revealed that GmMYB76, GmMYB92, and GmMYB177 are induced by several abiotic stress conditions and overexpression
of these TFs improves tolerance to salt and freezing in
SANTOS ET AL.
Arabidopsis (Liao et al., 2008). In rice, only a few studies report
the involvement of MYB proteins in abiotic and biotic stress
responses. Response to cold seems to be a common feature
among the best characterized rice MYB proteins.
Rice MYBS3 protein contains a single MYB repeat (MYB1R)
and its gene expression is repressed by ABA and induced by
cold and salt (Su et al., 2010). MYBS3 overexpression in rice
significantly increases tolerance to cold and RNA interference
lines displayed enhanced sensitivity to this abiotic stress
suggesting a role of MYBS3 in rice cold responses. Moreover,
microarray analysis and transactivation assays revealed that
MYBS3 represses the cold signaling pathway dependent on
the DREB1/CBF regulon (Su et al., 2010).
MYB3R subfamily proteins are known to be involved in
cell-cycle regulation through the transcriptional control of
cyclins. However, some studies revealed that TFs from this
subfamily might play a role in abiotic stress responses (Feller
et al., 2011). OsMYB3R-2 gene expression is induced by cold,
drought, and high salinity and its overexpression in Arabidopsis has significantly enhanced cold tolerance (Dai et al.,
2007). OsMYB3R-2 was also shown to target cyclin genes involved in the G2/M transition and thereby regulates the
progress of the cell cycle during cold stress (Ma et al., 2009).
The R2R3-MYB proteins are the largest group of plant MYB
proteins, including hundreds of members throughout the
plant kingdom (Feller et al., 2011). The functions of these
proteins are mainly related to regulation of plant morphology
and metabolism, but a role in biotic and abiotic stress responses has also been reported. OsMYB4 was shown to be
involved in the regulation of both types of stress responses
and its overexpression confers varying levels of tolerance
depending on the species (Agarwal and Jha, 2010). Its overexpression in Arabidopsis increases plant tolerance to cold and
drought and the resistance to biotic stress (Mattana et al.,
2005; Vannini et al., 2004, 2006). Tomato plants overexpressing this TF displayed a higher tolerance to drought
and increased resistance to biotic stress, but no alteration on
cold sensitivity (Vannini et al., 2007). In the apple, enhanced
tolerance to drought and cold was reported in transgenic
plants overexpressing OsMYB4 (Pasquali et al., 2008). Besides
the different tolerance levels observed in different transgenic
hosts, the increase in drought tolerance seems to be a common
feature in all plants overexpressing OsMYB4.
Although several MYB proteins have been identified in
rice, so far only a few OsMYBs have been functionally characterized for their role in abiotic stress responses (Table 1). The
data already gathered suggest that rice MYBs play an important role in the cold stress response mechanisms.
Zinc fingers
The zinc-finger proteins play a major role in many cellular
pathways and are present in all eukaryotic organisms. Zn
finger TFs have been implicated in distinct pathways, such as
nutrient homeostasis and root development (Devaiah et al.,
2007), flower development (Wu et al., 2008), carbohydrate
metabolism (Tanaka et al., 2009) and light and hormonal
signaling (Feurtado et al., 2011).
The C2H2-type Zn finger TFs are one of the most abundant
Zn finger TFs and have been described as involved in the
response of different plants to abiotic stress conditions (Mittler et al., 2006; Sakamoto et al., 2004; Vogel et al., 2005). These
TFS AND EPIGENETIC MECHANISMS IN ABIOTIC STRESS RESPONSES
TFs, also referred to as TFIIIA-type finger, are characterized
by two cystein and two histidine residues that bind to a zinc
ion to form a structure that binds to the major groove of DNA
(Pavletich and Pabo, 1991). The first of such TFs identified in
plants was the petunia ZPT2-1, a zinc- finger protein TFIIIAtype (Takatsuji et al., 1992). In rice, despite the high number of
genes encoding C2H2-type Zn finger TFs (Agarwal et al.,
2007), only a few have been functionally characterized: ZINCFINGER PROTEINS 182 (ZFP182), ZFP245, ZFP252 and
DROUGHT SALT TOLERANCE (DST) (Huang et al., 2007,
2009a, 2009b; Xu et al., 2008a). The overexpression of the first
three of these TFs in rice plants yielded similar phenotypes:
increased tolerance to abiotic stress conditions (Huang et al.,
2007, 2009a; Xu et al., 2008a). The DST protein, on the other
hand, seems to have a different role in abiotic stress signaling,
because rice plants harboring a mutation in its gene are more
tolerant to abiotic stresses than the wild-type plants (Huang
et al., 2009b). As shown in Table 1 and also in Supplementary
Table S1, genes coding for different C2H2-type TFs in rice are
differentially regulated by several abiotic stress conditions.
This means that these TFs most likely have roles in different
signaling pathways mediating abiotic stress responses.
There is much crosstalk between different families of TFs
involved in abiotic stress signaling. C2H2-type TFs have been
particularly described as interacting with the DREB1/CBF
regulon. For example, Arabidopsis plants overexpressing
DREB1A/CBF3 were found to have altered levels of ZAT10/
STZ (Maruyama et al., 2004). This interaction is further
supported by the finding that ZAT12, a transcriptional repressor also described as a regulator of several abiotic stressresponsive genes in Arabidopsis (Davletova et al., 2005), has a
regulon partly overlapping that of DREB1C/CBF2 (Vogel
et al., 2005). Moreover, ZAT12 was also described as a negative regulator of DREB1A/CBF3 and DREB1B/CBF1 (Vogel
et al., 2005). In rice, plants overexpressing ZFP252 were reported to have altered levels of OsDREB1A (Xu et al., 2008a).
C2H2-type TFs are therefore signaling components that can
be located either up- or downstream the DREB1/CBF genes.
Other types of Zn fingers, such as the Zn finger HomeoDomain TFs (ZF-HD), have been reported to have a role in
abiotic stress signaling in plants. These proteins are characterized by the presence of Zn finger-like motifs upstream of a
homeodomain (Windhovel et al., 2001). These TFs act in
concert with NAC TFs in Arabidopsis, to regulate the expression of abiotic stress-related genes (Tran et al., 2006). In rice,
however, the involvement of these TFs in stress signaling
is yet to be described. Up to now, only microarray data is
available on the transcriptional regulation of these genes in
rice ( Jain et al., 2008).
Leucine zippers
bZIP proteins are a large family of TFs, present in all eukaryotes, and that are characterized by the presence of a basic
region, responsible for DNA-binding, and of a leucine zipper,
involved in protein homo- and heterodimerization ( Jakoby
et al., 2002). Many bZIP TFs have been linked to the ABAdependent signaling pathway in several plant species, such as
rice, Arabidopsis, and maize (Choi et al., 2000; Hobo et al.,
1999a; Uno et al., 2000; Zhang et al., 2011). The role of bZIPs in
this pathway was revealed by the reports that TFs belonging
to this family bind to the ABA Responsive Element (ABRE;
845
PyACGTGG/TC) (Choi et al., 2000; Guiltinan et al., 1990;
Hobo et al., 1999a; Uno et al., 2000). This cis-acting element
was initially identified in wheat (Guiltinan et al., 1990) and
rice (Mundy et al., 1990) and was later shown to be present in
the promoters of many ABA-responsive genes. The role of
bZIP TFs in ABA-signaling was further supported by the
findings that the overexpression of these TFs causes ABAhypersensitivity in transgenic plants (Fujita et al., 2005; Kang
et al., 2002; Zou et al., 2007; Xiang et al., 2008). In most cases,
the overexpression of OsbZIPs in rice improves tolerance to
abiotic stress conditions, namely, high salinity and drought,
whereas its downregulation/knockout leads to higher sensitivity (see Table 1). Nevertheless, rice plants overexpressing OsABI5/OsbZIP10 are an exception, because they
were reported to be more sensitive to salinity than the wildtype (Zou et al., 2008). It is also interesting to note that, most
rice genes coding for bZIP TFs involved in abiotic stress
signaling are induced by ABA and bind to the ABRE ciselement (Table 1). These results indicate that, in rice, abiotic
stress signaling though bZIP TFs preferably occurs in an
ABA-dependent manner. Moreover, the bZIP-mediated
ABA signaling pathway seems to be conserved in several
plant species, both monocots and dicots. For example, the
homologous proteins TRAB1 (rice TRANSCRIPTION FACTOR RESPONSIBLE FOR ABA REGULATION 1), HvABI5
(barley ABA INSENSITIVE 5), and ABI5 (Arabidopsis ABA
INSENSITIVE 5) interact respectively with their counterparts OsVP1 (rice VP1- VIVIPAROUS 1), HvVP1 (barley
VP1), and AtABI3 (Arabidopsis ABA INSENSITIVE 3), which
are themselves homologues, to modulate ABA-dependent
gene expression (Casaretto and Ho, 2003; Hobo et al., 1999b;
Nakamura et al., 2001).
Other than abiotic stress signaling, bZIP TFs have been
described as involved in other signaling pathways, such as
light signaling (Chattopadhyay et al., 1998), floral architecture
(Maier et al., 2009), hormone signaling (Fukazawa et al.,
2000), and pollen development (Iven et al., 2010). As can be
seen in Table 1 and Supplementary Table S1, rice genes coding
for bZIP TFs are regulated at the transcriptional level by
several hormones, such as auxins (Yang et al., 2011), gibberellins (Shobbar et al., 2008), and ethylene (in the form of ACC)
(Lu et al., 2009). This is indicative of a crosstalk between
several signaling pathways, mediated by bZIP TFs.
Another group of bZIP TFs that has been implicated in
abiotic stress responses are the HDZIP TFs. These proteins are
characterized by the presence of a homeodomain directly
before the bZIP domain (Ruberti et al., 1991). These HDZIP
domains are responsible for homo- and heterodimerization of
the TFs, and also for the DNA-binding specificity (Meijer
et al., 2000). These proteins are plant-specific and do not occur
in other Eukaryotes. Similar to bZIPs, HDZIP TFs have been
implicated in several cellular processes, such as hormone
(Ilegems et al., 2010) and light signaling (Wang et al., 2003),
and also in plant development (Vernoud et al., 2009). Even
though there are some reports on the involvement of HDZIPs
in abiotic stress signaling, only a few of these TFs have so far
been characterized. The heterologous expression of the sunflower gene Hahb-4 in Arabidopsis led to plants that were more
tolerant to water stress (Dezar et al., 2005). Moreover, in the
drought-resistant species Craterostigma plantagineum, all genes
coding for the seven HDZIP TFs identified respond to
drought stress at the transcriptional level (Deng et al., 2002;
846
Frank et al., 1998), which is a strong indication that these TFs
play an important role in abiotic stress signaling. In rice,
however, other than gene expression studies (Agalou et al.,
2008; Jain et al., 2008), not much is known about the function
of HDZIPs in the stress signaling pathways. Nevertheless, it is
interesting to note that drought is the stress to which most of
the genes coding for HDZIPs respond (Supplementary Table
S1). This, together with previous data from other plant species
(Deng et al., 2002; Dezar et al., 2005; Frank et al., 1998), seems
to support a prominent role of these TFs in water stress signaling. It is also noteworthy that some, but not all of HDZIPcoding genes, respond to the hormone ABA (Deng et al., 2002;
Dezar et al., 2005; Johannesson et al., 2003). This probably
means that HDZIPs play a role in both ABA-dependent and independent signaling pathways.
WRKY family
The WRKY family of TF is one of the largest and oldest
families of transcriptional regulators in the plant kingdom
(Rushton et al., 2010). However, the first descriptions of this
TF family came out on the mid-1990s (Ishiguro and Nakamura, 1994; Rushton et al., 1995). WRKY TFs are exclusive of
plants and can be found from green algae to land plants. The
WRKY TFs are characterized by a DNA-binding domain with
approximately 60 a.a., the WRKY domain, which contains an
almost invariant WRKY amino acid sequence at the N terminus and a zinc-finger like motif in the C terminus (Rushton
et al., 2010). The WRKY TF family is divided into three groups
based on the number of WRKY domains (two domains in
Group I and one in Groups II and III) and the structure of their
zinc fingers (C2HC in Group III). The WRKY domain has been
crystallized (Yamasaki et al., 2005) and the proposed structure
is consistent with the cis-element where it should bind, the
highly conserved W-box (TTGACC/T). Because this ciselement is conserved, the specificity for the different TFs must
be obtained by the neighbouring areas of the W-box (Ciolkowski et al., 2008). WRKY TFs have been described as having a
role in the regulation of biotic and/or abiotic stress responses,
germination, senescence, and developmental processes
(Rushton et al., 2010). Research has however been focused on
biotic stress responses (Rushton et al., 2010; Shimono et al.,
2007; Tao et al., 2009). Although novel WRKY TFs have been
described, clear phenotypes are difficult to obtain by reversegenetics approaches (Berri et al., 2009), which may be due to
regulatory redundancy among the members of this family.
More than 100 WRKY family members, belonging to five
main phylogenetic groups, have been predicted/described in
rice (Berri et al., 2009). Despite their well-known response to
biotic stress, some WRKY TFs have been reported as responding to abiotic stress (Table 1 and Supplementary Table
S1). They are mainly upregulated in response to drought,
salinity, and ABA, and downregulated in response to cold
(Berri et al., 2009; Ramamoorthy et al., 2008). Nevertheless,
despite the extensive list of rice WRKY TFs studied, only a few
have been functionally characterized regarding their response
to abiotic stress (Table 1). OsWRKY13 overexpression in rice
increased sensitivity to salt and cold stress (Qiu et al., 2008),
whereas OsWRKY45 enhanced tolerance to salt and drought
in Arabidopsis (Qiu and Yu, 2009). The overexpression of
OsWRKY11, known to be induced by drought and heat, enhanced heat, and drought tolerance after heat pretreatment as
SANTOS ET AL.
compared to wild-type plants (Wu et al., 2009). When
OsWRKY08 was overexpressed in Arabidopsis, besides an
improvement of primary root growth in the transgenic plants
under osmotic stress, no clear phenotype regarding survival
under abiotic stress was shown (Qiu et al., 2004; Song et al.,
2009). OsWRKY72 was known to be involved in the ABA
signaling (Xie et al., 2005) and its overexpression in Arabidopsis increased sensitivity to ABA, salt, and osmotic stress
(Yu et al., 2010). Although the salt and osmotic stress phenotype was not obvious, there is a clear function of OsWRKY72 in ABA signaling and a crosstalk with the sugar
metabolism and auxin transport pathways (Yu et al., 2010).
OsWRKY13 (Qiu et al., 2007) and OsWRKY45 (Shimono et al.,
2007; Qiu and Yu, 2009) were also shown to be involved in
biotic stress resistance, whereas OsWRKY08, OsWRKY11, and
OsWRKY72 were not investigated for their putative involvement in biotic stress response (Table 1).
Although few reports have clearly demonstrated the
WRKY TFs function in abiotic stress in rice, they suggest that
WRKY TFs are mainly involved in osmotic stress-related responses (Table 1). The overexpression of WRKY rice TFs can
induce either improved tolerance or higher sensitivity to the
stress, thus acting as positive or negative regulators in stress
signalling pathways (Rushton et al., 2010).
NAC family
The NAC TF family is plant specific and one of the largest
TF families. NAC proteins contain a highly conserved Nterminal DNA-binding domain (NAC domain) and a variable
C-terminal domain that plays a major role in the regulation of
transcription as an activator or repressor. This TF family was
originally named from three consensus sequences identified
from Petunia and Arabidopsis, both with similar DNA-binding
domains, that is, NAC domain [NAM (no apical meristem),
ATAF1-2 (Arabidopsis transcription activation factor), and
CUC2 (cup-shaped cotyledon)] (Aida et al., 1997, 1999; Souer
et al., 1996). NAC TFs have been involved in several aspects of
plant development such as formation of boundary cells of
the meristem, transition between cell division and cell expansion in stamen and petals, anther dehiscence, flowering,
lateral root development, hormone signaling, senescence, and
seed quality. Furthermore, this family was also found to
participate in the responses to pathogens, viral infections, and
environmental stimuli of different plant species (reviewed in
Olsen et al., 2005; Tran et al., 2010).
Only a few members of this family were described in the
last decade of the 20th century. The postgenomic era, with the
availability of high-quality genome sequences of both Arabidopsis and rice, has offered an unprecedented opportunity to
identify complete TF families and their networks. Comprehensive genome-wide analyses of the NAC TF family suggested that there are at least 117 and 151 putative members of
the NAC TF family in Arabidopsis and rice, respectively
(Nuruzzaman et al., 2010). In rice, sequence analysis of NAC
TFs suggested that NAC family proteins could be classified
into two major groups, A and B, further subdivided into seven
and nine subgroups, respectively. Group A consists of 65
OsNAC proteins having low homology with the Arabidopsis
NACs, whereas the 86 OsNAC genes assigned to group B
showed high homology with the Arabidopsis and other NAC
proteins (Nuruzzaman et al., 2010). The NAC TFs related to
TFS AND EPIGENETIC MECHANISMS IN ABIOTIC STRESS RESPONSES
development and stresses belong to group B. The OsNAC
genes were distributed all over the 12 rice chromosomes and
36 OsNAC genes were observed in tandem duplication. This
suggests that the NAC family increased rapidly during the
course of evolution through tandem duplications of chromosomal regions (Fang et al., 2008; Nuruzzaman et al., 2010).
Analysis of OsNAC gene promoter sequences revealed the
presence of 17 cis-acting regulatory DNA elements known to
be responsive to plant hormones (e.g., auxin, gibberellic acid,
and salicylic acid) and environmental stimuli (light and cold)
and related with seed specific expression (Fang et al., 2008).
Different authors have reported the differential expression
of 151 NAC genes in microarray analyses of rice plants subjected to abiotic stress. According to the author, the number of
differentially expressed genes was 15% (Fang et al., 2008) or
30% (Nuruzzaman et al., 2010), which may be due to the
different varieties used in the study and the number of
stresses analyzed. Among 20 OsNAC genes identified as responsive to abiotic stress, only 3 are induced by drought, salt,
and cold, whereas the remaining genes were either induced
by one or two stresses (Fang et al., 2008). On the basis of
individual stress responses, 5 genes are induced by drought,
19 genes by salt, and 16 genes by cold (Supplementary Table
S1). Moreover, all the 20 stress-inducible OsNAC genes
were found to contain at least one of the stress-responsive ciselements such as ABRE (ABA-responsive element), DRE
(dehydration-responsive element), and LTRE (low temperature-responsive element) (Fang et al., 2008).
Despite all the research on rice NAC TF genes, so far only
seven members of the family (OsNAC5, OsNAC6/SNAC2,
OsNAC10, OsNAC19/SNAC1, ONAC045, OsNAC52, and
ONAC063) have been functionally characterized for abiotic
stress tolerance (Table 1). Apart from OsNAC063, which is not
drought stress induced, all the other genes are induced under
salt and drought stress. The overexpression of each of these
genes in rice and/or Arabidopsis improved tolerance to
drought and salt (except OsNAC52) stress in transgenic
plants. Among these seven OsNAC genes, at least five
are induced by ABA (Table 1). Furthermore, transgenic
plants overexpressing OsNAC6/SNAC2, OsNAC19/SNAC1,
and OsNAC52 were reported to be hypersensitive to exogenous ABA (Table 1), indicating that NAC TFs may be involved in the ABA signaling pathway.
The stress-inducible NAC TFs are promising candidates to
improve tolerance to abiotic stress, particularly to salt and
drought. However, so far only a few members of the NAC TF
family have been overexpressed in rice.
Heat-shock factors
Heat-shock transcription factors (HSFs), although present
in all living organisms known so far, are mostly represented in
plants (Baniwal et al., 2004). These TFs are known to bind to
heat-shock elements (HSEs) in the promoter regions of heatshock proteins (HSPs). The HSEs are constituted by a palindromic sequence, the conserved nGAAnnTTcn motif, to
where HSFs can bind (Pelham, 1982). Plants HSFs are characterized by a DNA-binding domain on the N-terminal,
oligomerization motif, nuclear localization signal, nuclear
export signal, and an activation domain. Based on the oligomerization domain structure, HSFs are classified into three
different classes, A, B, and C (Kotak et al., 2004). Although
847
mostly described as involved in mechanisms related to heat
stress (Charng et al., 2007; Schramm et al., 2008), HSFs have
also been related to other stress response networks, such as
oxidative stress (Li et al., 2005), chilling stress (Li et al., 2003)
and high-salinity stress (Yokotani et al., 2008).
Among the 26 HSFs predicted in rice, the members of the
class A are the most abundant and the best studied so far.
Recently, the gene expression of HSF family members has
been studied under different stress conditions such as heat,
oxidative stress, drought, cold, and high-salinity (Liu et al.,
2010; Mittal et al., 2009). The members of this family are differentially expressed under abiotic stress conditions and are
developmentally regulated in diverse tissue types under
control conditions (Liu et al., 2010; Mittal et al., 2009). In addition, different HSF classes can be related to different stresses. For example, genes encoding HSF class C members seem
to be more responsive to cold stress (Mittal et al., 2009) and
class A members are more responsive to heat stress (Liu et al.,
2010; Mittal et al., 2009). In fact, several members of the class A
respond extremely fast to heat stress, eventually acting as heat
sensors.
Many HSF genes are known to be differentially regulated by
diverse abiotic stresses (Liu et al., 2010; Mittal et al., 2009),
however, only two members of the HSF family (all from class A)
have been functionally characterized in overexpression/
mutant analyses (Table 1). The overexpression of OsHsfA2e in
Arabidopsis greatly enhanced the thermotolerance of transgenic
plants during germination, vegetative, and flowering stage
(Yokotani et al., 2008). In addition, transgenic plants also
showed improved tolerance to high-salinity both at seedling
and vegetative stage. Another HSF, OsHSF7, was identified by
Yeast-One hybrid screening using a dimeric HSE as bait (Liu
et al., 2009). The overexpression of OsHSF7 in Arabidopsis did
not lead to a higher level of HSPs (HSF targets) in transgenic
plants. In addition, the transgenic plants showed a higher basal
thermotolerance than wild-type plants. HSFs seem to play an
important role in the response to high temperature and may be
useful to improve heat tolerance in crop plants. It is known that
a rise of + 1C could lead to a 10% decline in rice yield (Peng
et al., 2004).
Epigenetic Mechanisms and Regulation
of Gene Expression in Abiotic Stress Responses
Epigenetic mechanisms have a key role on plant plasticity
responses to unpredictable abiotic stresses. This review is
focused on DNA methylation and histone modification
changes associated to abiotic stress responses reported in
several plant species, including rice and Arabidopsis model
plants.
DNA Methylation and Abiotic Stress
Cytosine methylation is a conserved epigenetic mark involved in genome defense against endogenous transposable
elements or viral DNA and in regulation of gene expression
throughout plant development. The addition of a methyl
group to cytosine residues is catalyzed by methyltransferases
(MTases) and in plants this may occur in both asymmetric
(CHH) and symmetric (CG and CHG) contexts. Four main
families of plant MTases have been identified so far, with
distinct functions in de novo and/or maintenance methylation: DOMAINS REARRANGED METHYLTRANSFERASE
848
SANTOS ET AL.
(DRM), METHYLASE 1 (MET1), CHROMOMETHYLTRANSFERASE (CMT), and DNA methyltransferase homolog 2 (Dnmt2) (reviewed by Zhang et al., 2010). The
establishment of DNA methylation is counteracted by passive
or active demethylation. While in the first, metylated cytosines are replaced with unmethylated ones during DNA
replication, active demethylation involves a base excision repair mechanism, mediated by DNA glycosylases, without the
occurrence of DNA replication (Ikeda and Kinoshita, 2009).
Additionally, DNA methylation is modulated by other
mechanisms, such as RNA-directed DNA methylation
(RdDM) pathway, mediated by siRNAs (Chan et al., 2005)
and chromatin remodeling factors (Meyer, 2010; Zhang et al.,
2010). All together, these regulatory pathways provide a dynamic platform for establishment of DNA methylation patterns, which may be crucial to guarantee the epigenomic
plasticity and enable an efficient response to developmental
cues and environmental stress. The mechanistic effect of DNA
methylation in transcription is still unclear and several lines of
evidence suggest that the roles of cytosine methylation are
equally diverse and likely individualized for different genes
(Zhang et al., 2010). Methylated cytosines may attract methylbinding proteins, which in turn recruit histone modifiers and
chromatin remodeling proteins, forming a complex that can
perturb the binding of transcription factors (Fransz and de
Jong, 2002). High-resolution mapping of DNA methylation
have uncovered some common aspects related to its distri-
bution along plant genomes (Li et al., 2008; Yan et al., 2010;
Zhang et al., 2006; Zilberman et al., 2007). Transcriptional
inactive heterochromatic regions, which contain highly
abundant transposable elements (TEs) and repetitive sequences, contain the highest density of methylated cytosines.
In euchromatic regions, lower but still significant levels of
cytosine methylation were also found. Surprisingly, in both
Arabidopsis (Zhang et al., 2006; Zilberman et al., 2007) and rice
(Li et al., 2008; Yan et al., 2010), DNA methylation related to
active genes was more abundant in transcribed regions than
in promoters. In Arabidopsis, the transcript elongation efficiency was negatively correlated to the extent of methylation
within the gene body (Zilberman et al., 2007). One might expect that a similar mechanism also occurs in rice.
Abiotic stresses may induce changes in DNA methylation
levels, which may be associated with chromatin remodeling
and transcription regulation of stress responsive genes (Table 2).
Genome-wide analyses in several plant species evidence a
global rearrangement of DNA methylation after stress application, mostly due to demethylation (Aina et al., 2004; Labra
et al., 2002; Wang et al., 2011b; Zhong et al., 2009). The use of
AFLP-based methylation-sensitive approach (MSAP) revealed that some of these changes (methylation/demethylation) are site-specific, because conserved patterns were
observed between distinct genotypes or tissues (Labra et al.,
2002; Wang et al., 2011b). Because this technique is restricted
to CG methylation analysis through specific restriction
Table 2. Plant Epigenetic Landscape Modifications Under Abiotic Stresses
Stress
Cold
Drought
Plant
Zea mays
Arabidopsis thaliana
Cell lines:
Nicotiana (By2)
Arabidopsis thaliana (T87)
Pisum sativum
Oryza sativa
Arabidopsis thaliana
Arabidopsis thaliana
Salinity
Laguncularia racemosa
Triticum aestivum
Nicotiana (By2)
Arabidopsis thaliana
Heat
Arabidopsis thaliana
Hypoxia
Oryza sativa
Aluminium
UV
Nicotiana tabacum
Arabidopsis thaliana
Chromatin mark
Enrichement ( + ) depletion
( - ) no change (0)
5-mC
H3K27me3
H3ac
H3Ser10P
H3Ser10PK14ac
H4ac
5-mC
5-mC
H3K23ac
H3K27ac
H3K4me3
H3K4me3
H3K4me2
H3K4me
5-mC
5-mC
H3Ser10P;
H3K14ac
H3K9ac
H3K14ac
H3K4me3
H3K9me2
5-mC
H3K9me2
H3K4me3
H3K4me2
H3ac
H3K4me3
5-mC
H3ac
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
0
0/+
+
+
Reference
(Steward et al., 2002)
(Kwon et al., 2009)
(Pavangadkar et al., 2010)
(Sokol et al., 2007)
(Labra et al., 2002)
(Wang et al., 2011b)
(Kim et al., 2008b)
(van Dijk et al., 2010)
(Lira-Medeiros et al., 2010)
(Zhong et al., 2009)
(Sokol et al., 2007)
(Chen et al., 2010)
(Pecinka et al., 2010a)
(Tsuji et al., 2006)
(Choi and Sano, 2007)
(Lang-Mladek et al., 2010)
TFS AND EPIGENETIC MECHANISMS IN ABIOTIC STRESS RESPONSES
enzymes it is possible that a higher level of rearrangements
may occur in other methylation sites. Transcriptional activation of specific loci associated with changes in DNA methylation have been identified for transposons and protein-coding
sequences in response to abiotic stress (Choi and Sano, 2007;
Hashida et al., 2006; Steward et al., 2002). For example, the
aluminium and oxidative stresses were shown to induce
DNA demethylation and transcription of a gene encoding a
glycerophosphodiesterase-like protein (Choi and Sano,
2007). However, other studies reported transcriptional induction of silent loci after stress, without loss of DNA
methylation, but instead a decrease in nucleosome occupancy (Lang-Mladek et al., 2010; Pecinka et al., 2010b; TittelElmer et al., 2010). A decrease in DNA methylation in the
Arabidopsis met1-3 mutant was also associated to higher expression of the AtHKT1 gene, which encodes for a vacuolar
Na + /H + transporter (Baek et al., 2011). The methylation
pattern of a putative small RNA target region located in the
AtHKT1 promoter is important for the differential expression of
this gene in roots and leafs, which may affect salt response and
sensitivity (Baek et al., 2011). Differences in global DNA
methylation patterns were observed between two populations
of Laguncularia racemosa that grow in salt marsh and riverside
habitats (Lira-Medeiros et al., 2010) suggesting that epigenetic
variation under natural conditions also play an important role
in helping plants to adapt to different environments. In rice,
several MTases have been identified, and microarray data
suggested that some are preferentially upregulated during the
initiation of floral organs (Sharma et al., 2009; Yamauchi et al.,
2008). Additionally, higher levels of methylation in rice leaves
(determined through MSAP) were detected at the booting and
heading stages as compared to the tillering stage (Wang et al.,
2011b). In turn, demethylation levels induced by drought were
significantly higher at the tillering stage than at the booting and
heading stages (Wang et al., 2011b). These studies suggest that
changes in DNA methylation may also differentially modulate
plant response to abiotic stress throughout development.
Histone Modifications and Abiotic Stress
In eukaryotic cells, nuclear DNA is packed and organized
in association to a histone protein core forming nucleosomes,
which are the structural units of chromatin. Changes in nucleosome structure through combinations of histone variants
and covalent modifications of histone tails, by acetylation,
methylation, phosphorylation, ubiquitination, biotinylation
or SUMOylation, constitute an integrated histone code which
has been correlated with regulation of gene expression
(Bannister and Kouzarides, 2011; Jayani et al., 2010; Jenuwein
and Allis, 2001; Strahl and Allis, 2000; Winter and Fischle,
2010; Zhou, 2009). The methylation of lysine residues on
histone H3 has been correlated with either transcription activation or repression depending on which lysine is methylated and how many methyl groups are added (Chinnusamy
and Zhu, 2009; Strahl and Allis, 2000; Zhang, 2008). For example, in maize, histone H3 lysine 4 trimethylation,
(H3K4me3) has been associated to euchromatin and gene
activation, being present in active gene sequences but absent
in transposons (Wang et al., 2009). In Arabidopsis, histone H3
lysine 9 dimethylation (H3K9me2) has been regarded as a
marker for heterochromatin and repressed transcription, thus
associated with transposons (Zhang, 2008; Zhou, 2009). On
849
the other hand, the H3K9me3 and H3K27me3 is enriched in
genes of euchromatic regions (Zhang, 2008). Other histone
modifications such as biotinylation and sumoylation have
been associated to gene repression (Strahl and Allis, 2000).
Regarding histone lysine acetylation, strong acetylation of
histones has been associated to a more relaxed chromatin
structure and thus to enhanced transcription, while weak
acetylation has been related to compaction of chromatin and
gene silencing (Berger, 2007; Zhu et al., 2008). Histone lysine
acetylation is modulated by histone acetyltransferases (HAT)
and histone deacetylases (HDAC). HDAC encoding genes are
divided in four major classes (Pandey et al., 2002) being the
HD2 class exclusive in plants (Lusser et al., 1997). In rice the
OsHDT1 is involved in differential gene expression in hybrids
(Li et al., 2011). Globally, the rice genome has at least 19
HDAC genes and most of them show to be differentially
regulated by distinct abiotic stress conditions (Fu et al., 2007;
Hu et al., 2009). Microarray data revealed that most rice
HDAC genes were particularly responsive to drought or salt
stresses, mainly through transcriptional repression (Hu et al.,
2009). Thus, chromatin modifier enzymes themselves may be
transcriptionally regulated by abiotic stresses and in this case
the down regulation of HDAC could be necessary to allow the
induction of stress responsive genes (Fu et al., 2007).
Histone modifications and DNA methylation crosstalks
have been implicated on gene expression regulation. For example, in Arabidopsis, the abolishment of DNA methylation in
the ddm1 mutants was correlated with lower levels of dimethylation of histone H3 at lysine 9 (H3K9me2) (Gendrel
et al., 2002). An SUVH [Su(var)3–9 homologs] protein involved in H3K9 methylation was found to directly bind
to methylated DNA, suggesting the occurrence of a selfreinforcing feedback loop for the maintenance of DNA and
histone methylation in this species ( Johnson et al., 2007).
Several rice SUVH genes with a deduced role heterochromatin formation were recently identified (Qin et al., 2010).
Some of these showed to mediate retrotransposon repression
through DNA methylation and H3K9me3 (Ding et al., 2007;
Qin et al., 2010). Moreover, in rice most protein-coding genes
with methylated DNA are associated with H3K4me2 and/or
H3K4me3 and in this case, the repressive effect of DNA
methylation on gene expression was attenuated when
H3K4me3 is also present (Li et al., 2008).The impact of abiotic
stresses on genome-wide landscape of histone modifications
starts to be deciphered (Table 2) mainly due to recent technical
advances such as chromatin immunoprecipitation (ChIP) and
genome-wide sequencing (ChIP-Seq). In rice, the submergence stress caused a decrease on H3K4me2 levels, an increase
of H3K4me3 levels and a gradual increase of H3 acetylation
at the 5¢- and 3¢-coding regions of the ALCOHOL DEHYDROGENASE 1 (ADH1) and PYRUVATE DECARBOXYLASE
1 (PDC1) genes (Tsuji et al., 2006). These modifications were
correlated with enhanced expression of the ADH1 and PDC1
observed in response to this stress (Tsuji et al., 2006). In Arabidopsis, the drought stress (Kim et al., 2008a) caused an increase of H3K4me3 and H3K9ac in the promoter region of
stress responsive genes, while the coding region showed enrichment of H3K23ac and H3K27ac (Kim et al., 2008a). A
genome-wide analysis of transcripts and H3K4 methylation
patterns in dehydration stressed Arabidopsis plants revealed
different dynamics on specific patterns of changes in
H3K4me1, H3K4me2, and H3K4me3 profiles for upregulated,
850
downregulated, and unaffected genes being the level of
H3K4me3 particularly correlated to gene expression regulation (van Dijk et al., 2010). In turn, cold stress caused a decrease of H3K27me3 in the promoter of two cold-responsive
genes, COLD REGULATED 15A (COR15A) and GALACTINOL SYNTHASE 3 (ATGOLS3) (Kwon et al., 2009), while salt
stress caused an enrichment of H3K9ac, H3K14ac, and
H3K4me3, and a depletion of H3K9me2 at stress-responsive
genes (Chen et al., 2010). Additionally, the HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES 15 (HOS15)
protein, a repressor of gene expression with an important role
in cold tolerance, was shown to promote H4 deacetylation at
the RESPONSIVE TO DESSICATION 29A (RD29A) promoter
(Zhu et al., 2008). Collectively, these studies demonstrate the
importance of the histone code plasticity in transcriptionally
regulation during plant responses to different abiotic stresses.
Epigenetic Mechanisms and Transcription
Factors Crosstalk in Abiotic Stress Responses
An intriguing question is how epigenetic mechanisms and
TFs crosstalk to achieve a coordinated and specific gene regulation. In a simple view, a compact chromatin configuration
can prevent the access of TFs and RNA polymerase to gene
promoters and transcription start sites, while a more relaxed
chromatin structure would facilitate the access to TFs enabling enhanced gene expression (Ahringer, 2000). TFs are
essentially characterized by the presence of DNA binding
domains with specificity to regulatory DNA sequences.
Contrastingly, many other proteins also involved in the regulation of gene expression such as chromatin remodelers,
histone acetylases, deacetylases, kinases, and methylases, do
not have such DNA-binding domains. Thus, their inability to
interact directly with target promoter genes implies the need
of recruiting TFs. In Brassica napus, a novel protein, KIDCONTAINING PROTEIN (BnKCP1), which acts as a TF,
contains a putative KID domain required for interaction with
an HDAC (Gao et al., 2003). In Arabidopsis, it was also reported
that the cold inducible TF CBF1 could interact with the GCN5
(Stockinger et al., 2001), an HAT required for acetylation of
several H3 lysine residues (Servet et al., 2010). GCN5 is the
component of chromatin modifying complexes related to
transcriptional activation. Such interaction was also predicted
for an additional putative TF AtEML protein, which is also
regulated by cold stress (Gao et al., 2007). In a similar way, the
Arabidopsis ERF genes, which are regulators of gene expression, were showed to interact with members of protein cosupressor complexes associated to HDACs (Song et al., 2005;
Song and Galbraith, 2006). In addition, the interaction of two
WRKY TFs (WRKY38 and WRKY62) with an HDAC (HDA19)
appeared to be determinant to fine-tune basal response to biotic
stress in Arabidopsis (Kim et al., 2008a). Thus, TFs involved in
stress response may be important players in the recruitment of
histone modifying enzymes to target gene promoter regions,
contributing for transcription modulation of TF-specific regulons (Gao et al., 2003, 2007; Song et al., 2005; Servet et al., 2010;
Stockinger et al., 2001). Furthermore, in Arabidopsis, the
WRKY70 TF was shown to be activated by the ATX1, which has
a histone methyltransferase (HMT) activity with the ability to
trimethylate H3K4 (Alvarez-Venegas et al., 2007). Thus, genes
encoding TFs can be the primary targets of epigenetic factors
while the entire networks of genes controlled by the TFs would
SANTOS ET AL.
be secondary targets also containing epigenetic marks that will
facilitate transcription in case rapid changes are needed e.g. on
stress response (Alvarez-Venegas et al., 2007). Taken together,
these studies point out for a crucial role of TFs in the establishment of locus-specific chromatin remodeling, essential for
transcriptional regulation, directly affecting nucleosome structure with consequences in gene activation/repression.
Conclusions and Perspectives
Plant response to abiotic stresses implies strict regulation
of the transcriptional networks. However, little is known
regarding regulation of gene expression under adverse environmental conditions. Crosstalk between TFs, DNA methylation, histone modifications, and chromatin remodeling
enzymes have been involved in the transcriptional regulation
of the stress responsive genes, pointing out for an integrated
view of transcription regulation.
In rice, many TFs from different families (e.g., AP2/ERF,
MYB, Zn finger, bZIP, NAC, WRKY, HSF) were already
shown to play important roles in plant response to abiotic
stress (Table 1), but much more are yet to be studied. Regarding the mechanisms underlying global epigenetic remodeling under environmental stress very little is known
(Table 2). Figure 1 summarizes our present knowledge on the
crosstalk between TFs and epigenetic mechanisms involved in
abiotic stress responses in rice.
FIG. 1. Integrative view of the crosstalk between TF families and epigenetic mechanisms described so far as involved
in abiotic stresses in rice. The diagram includes TF families
that contain stress responsive members as presented in
Table 1 and Supplementary Table S1. The TFs characterized
so far may only be a small fraction of the total number involved in abiotic stress responses in rice. It should also be
noticed that not all TFs of a given family respond to all the
stresses indicated, but that a TF family includes members
responsive to each stresses. The epigenetic events depicted
are illustrative of what is currently known for rice in response to specific abiotic stresses (Table 2) but epigenomic
changes are expected to occur in response to several abiotic
stress conditions. Future studies on histone modification
enzymes will shed new light into the crosstalk between TFs
and epigenetic regulatory mechanisms in rice.
TFS AND EPIGENETIC MECHANISMS IN ABIOTIC STRESS RESPONSES
Based on the recent advances, investigation on plant responses to abiotic stress must follow several promising research
lines, such as (1) charting gene regulatory networks, (2) deciphering genome-wide changes in the epigenome state, (3)
characterizing protein/protein interactions involved in the
transcription regulatory complexes, (4) integration of histonemodification pattern with transcriptomes and also with spatial
nuclear architecture, (5) identification of TF targets and their
interactions with chromatin regulators, (6) identification and
functional studies on histone modification enzymes. These
exciting issues count with technological advances, such as RNAseq, chromatin immunoprecipitation (ChIP) coupled with nextgeneration sequencing technology (ChIP-seq), ChIP on chip, as
well as shotgun proteomics. Nevertheless, advanced techniques
to screen for proteins interactions need to be developed. The
acquired knowledge on the molecular mechanisms underlying
plant stress responses will be essential to generate transgenic
crops or to unveil new allelic variations (e.g., EcoTILLING) in the
natural population with enhanced tolerance to abiotic stresses.
Definitely, a collaborative work between different researcher
areas, for example, cell and molecular biology, genomics, transcriptomics, proteomics, and bioinformatics, will be needed.
Acknowledgments
The work of our research group was supported by research
grants from the Fundação para a Ciência e a Tecnologia
through National Funds (PTDC/BIABCM/64215/2006,
PTDC/BIA-BCM/099836/2008, and PTDC/BIA-BCM/
111645/2009). A.P.S. (SFRH/BPD/40707/2007), T.S. (SFRH/
PD/31011/2006), D.F. (SFRH/BD/29258/2006), P.B. (SFRH
/ BD / 31594 / 2006) T.L. (SFRH/BPD/34943/2007), and S.C.
(SFRH / BPD / 64193 / 2009) are also grateful to Fundação
para a Ciência e a Tecnologia for their Post-Doc (BPD) and
PhD (BD) fellowships. N.S. was supported by Programa
Ciência 2007, financed by POPH (QREN).
Author Disclosure Statement
No conflicting financial interests exist.
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Address correspondence to:
Nelson J.M. Saibo
Instituto de Tecnologia Quı́mica e Biológica
Universidade Nova de Lisboa
and Instituto de Biologia Experimental e Tecnológica
Av. da República
2780-157 Oeiras, Portugal
E-mail: [email protected]