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Functional role of DRE-binding transcription
factors in abiotic stress
ABDELATY SALEH, VICTORIA LUMRERAS AND MONTSERRAT PAGES*
Departamento de Genètica Molecular, Instituto de Biología Molecular de Barcelona (IBMB)
Consejo Superior de Investigaciones Científicas (CSIC)
18-26 Jorge Girona, 08034, Barcelona, Spain
*Corresponding author: [email protected]
Abstract
The growth and development of plants is greatly affected by abiotic stress conditions such as drought, soil salinity and low temperature. Plants respond to these
environmental challenges through a number of homeostatic mechanisms that
maintain the water balance and the integrity of tissues. This includes several regulatory mechanisms that activate the expression of tolerance-effector genes. Here, we
summarize recent studies highlighting the role of specific members of the
DRE-binding family of transcription factors in the adaptive responses to abiotic
stresses.
Introduction
Plants are exposed to many types of abiotic stress during their life cycle. Water
deficit caused by drought, low temperature or high salt concentration in the
soil, is one of the most common environmental stresses that affects growth and
development of plants and leads to alterations in metabolism and gene expression. Water deficit causes various alterations in plants, such as stomatal closure,
decrease of turgor and changes in the composition of the cell wall or plasma
membranes, which can act as signals triggering adaptation responses. Although
relatively little is known about the mechanisms for sensing these changes, it is well
established that abscisic acid (ABA) is a major physiological signal that induces
drought responses (Gomez et al. 1988; Mundy and Chua 1988). ABA-dependent
signalling systems have been described that mediate adaptation to drought by activation of bZIP proteins, which then bind to ABA-responsive regulatory elements
(ABREs) in target genes and induce their transcription (Busk and Pagés 1998; Shinozaki and Yamaguchi-Shinozaki 2000). Another ABA-dependent pathway
Tuberosa R., Phillips R.L., Gale M. (eds.), Proceedings of the International Congress
“In the Wake of the Double Helix: From the Green Revolution to the Gene Revolution”,
27-31 May 2003, Bologna, Italy, 193-205, ©2005 Avenue media, Bologna, Italy.
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requires protein biosynthesis of the MYC and MYB transcription factors, which
function cooperatively to regulate the expression of target genes (Abe et al. 1997).
However, in Arabidopsis not all drought responses appear to be mediated by
ABA, since a number of genes are known to be induced by drought, salt and cold
in aba (ABA-deficient) and abi (ABA-insensitive) mutants (Yamaguchi-Shinozaki and Shinozaki 1994). This suggests the existence of alternative regulatory systems of gene expression during the stress response. In addition, recent studies
have identified ABA-dependent and ABA-independent pathways that lead to
rapid responses to drought or cold and function through members of the
AP2/ERF family of transcription factors (Yamaguchi-Shinozaki and Shinozaki
1994, Kizis and Pagés, 2002). Although these different pathways are usually considered to function independently from each other, it is certainly possible that
some cross-talk exists between them (Figure 1).
Figure 1. Regulation of Drought-Responsive gene expression via ABA-dependent and independent
pathways.
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Drought Responsive Elements (DREs)
Molecular analyses of genes induced under environmental stress conditions have led
to the identification of specific cis-regulatory elements that mediate this activation.
Drought Responsive Elements (DREs) have been reported to be involved in various
types of abiotic stress responses via ABA-dependent and ABA-independent pathways
as shown in Table 1 (Busk et al. 1997; Shinozaki and Yamaguchi-Shinozaki 1997;
Busk and Pagès 1998; Haarke et al. 2002; Kizis and Pagès 2002). The DRE sequence
(5'-TACCGACAT-3') plays an important role in regulating gene expression in
response to drought and other types of abiotic stress in plants. The DRE element was
first identified in the promoter of the drought-responsive gene rd29A (also, known as
cor78 and lti78) (Yamaguchi-Shinozaki and Shinozaki 1994). rd29A encodes a protein similar to the so-called late embryogenesis abundant proteins (LEAs, Wise 2003),
which is induced both during the maturation of embryos and by several types of
stresses in vegetative tissues and probably functions as a tolerance effector. The DRE
element is essential for the induction of rd29A gene expression by osmotic stress such
as drought and high salinity as well as by low temperature, but not for the activation
of this gene in response to ABA (Yamaguchi-Shinozaki and Shinozaki 1994).
Subsequently, new cis-elements related to the DRE motif have been identified.
One such motif is the C-repeat responsive element (CRT), which contains the core
(5'-CCGAC-3') and was initially identified in the promoter of cold-inducible genes
from Arabidopsis. This sequence is essential for induction of several genes by low-temTable 1. DRE cis-elements.
Cis-element
Plant specie
Protein
Ref.
Drought Responsive Element
(DRE)
Arabidopsis thaliana
DREBs
Liu et al. 1998
5'-TACCGACAT-3'
Oriza sativa
OsDREBs
Dubouzet et al. 2003
Triticum aestivum
TaDREB
Shen et al. 2003b
Atriplex hortensis
AhDREB1
Shen et al. 2003a
Arabidopsis thaliana
CBFs
Brassica napus
BnCBFs
Stockinger et al. 1997
Gilmour et al. 1998
Haake et al. 2002
Gao et al.2002
Drought Responsive Element 1
(DRE1)
5'-ACCGAG -3'
Zea mays
Unidentified Busk et al. 1997
maize protein
Drought Responsive Element 2
(DRE2)
5'-ACCGAC-3'
Zea mays
DBF1
and
DBF2
C-repeat Responsive Element
(CRT)
5'-TGGCCGAC-3'
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perature including the Brassica napus BN115 gene and the wheat gene WCS120
(Baker et al. 1994; Jiang et al. 1996; Ouellet et al. 1998). The CRT motif was also
described in the promoters of kin1, kin2 and rab18, three other cold-regulated genes,
from Arabidopsis (Kurkela and Borg-Franck 1992; Lang and Palva 1992). Studies of
these genes in ABA-deficient and ABA-insensitive mutants showed activation of the
genes during drought and cold stress independently of ABA. However, recent evidence indicates that some DRE/C-repeat motifs behave differently and can respond
to an ABA-dependent mechanism (Haake et al. 2002). For example, the dehydration
responsive element 2 (DRE2) identified in the maize rab17 promoter is involved in
ABA-dependent responses to osmotic stress. This site includes the typical core motif
(5'-ACCGAC-3') and was identified by in vivo footprinting analysis of embryos and
leaves (Busk et al. 1997). Increased DRE2 occupancy was observed after both
drought treatment and ABA induction, and in vivo analyses showed that this element
is important for activation of the rab17 promoter in both situations. In addition, the
rab17 promoter contains the related DRE1 cis-element (5'-ACCGAG-3'), which
mediates ABA-dependent regulation in the embryo but appears insensitive to stimulation by drought in vegetative tissues (Busk et al. 1997; Busk and Pagès 1998).
DRE-binding factors: a complex family
Several DRE-binding proteins have been identified from Arabidopsis, rice, maize
and other plants that specifically interact with the DRE sequence. The first cDNA
clone for a DRE-binding protein was isolated in a yeast one-hybrid screening; it
was named CBF1 (CRT-binding factor1) (Stockinger et al. 1997). In parallel, other
authors have cloned additional CBF-related genes such as DREBs from Arabidopsis (Gilmour et al. 1998; Haake et al. 2002), ZmDBFs from maize (Kizis and Pagès
2002), BnCBFs from Brassica napus, HvCBF1 from barley (Xue 2002), OsDREBs
from rice (Chen et al. 2003; Dubouzet et al. 2003), AhDREB1 from Atriplex hortensis (Shen et al. 2003a) and TaDREB1 from wheat (Shen et al. 2003b).
The DRE-binding factors constitute a subgroup within a large family of plant
transcription factors present in many plant species. These proteins, collectively known
as AP2/ERF proteins, share a conserved DNA-binding domain of about 60-70 amino
acids (Figure 2). This AP2/ERF domain was originally identified in APETALA2 of
Arabidopsis (Jofuku et al. 1994) and EREBP1 of tobacco (Ohme-Takagi and Shinshi
1995). The AP2/ERF domain is a new type of DNA-binding sequence that includes
two regions: the YRG region (YRG element) of about 20-amino acids-long and the
N-terminal stretch rich in basic and hydrophilic residues. It was proposed to have a
role in the DNA binding by making a direct contact with the DNA due to its basic
character (Okamuro et al. 1997). The second region is the RAYD sequence of about
40 amino acids, which contains 18 amino acids capable of forming an amphipathic
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α-helix in the C-terminal sequence and is thought to have an important role for the
structure and function of the domain (Jofuku et al. 1994; Okamuro et al. 1997). The
RAYD element was proposed to mediate protein-protein interactions through α-helix
or to have an alternative role in DNA binding through interactions of the hydrophobic face of the α-helix with the major groove of DNA.
DRE-binding proteins contain specific residues within their AP2/ERF domain
that may determine their capacity to bind the DRE/CRT element (Jofuku et al.
1994; Okamuro et al. 1997; Kizis et al. 2001; Sakuma et al. 2002). These factors
do not present any apparent similarity outside this region. Together, these observations suggest the existence of a complex family of DRE-binding proteins with the
potential to mediate different responses to abiotic stresses.
Gene regulation
Various stress conditions induce the expression of DRE-binding factor genes. Increased
accumulation of these transcripts has been found in response to drought, high salinity, low temperature and ABA treatments. Also, the induction of these transcripts is
organ-specific and proportional to the length of the stress treatment. Transcription fac-
Figure 2. Multiple alignment of the AP2/ERF domain of DRE-binding proteins. The amino acid
sequences of the AP2/ERF domain of DRE-binding proteins were aligned. The shaded boxes presented the amino acid identity (dark grey; the identical amino acids, medium grey: the similar
amino acids, light grey: the rest of the amino acids). Protein names are indicated at the left. Accession numbers correspond to NCBI database of analysed proteins: ZmDBF1 (AAM80486),
ZmDBF2 (AAM80485), OsDBF1 (AAP56252), OsDBF2 (AAP70033), OsCBF (AAG59619)
OsDBF1 (AAP92125), OsDREB1A(AAN02486), OsDREB2A (AAN02487), TaDREB1
(AAL01124), DREB1A/CBF3 (BAA33791), DREB1B/CBF1 (BAA33792), DREB1C/CBF2
(BAA33793), CBF4/DREB1D (NP_200012), DREB2A (BAA33794), DREB2B (BAA33795),
BnCBF5 (AAM18958), BnCBF7 (AAM18959), BnCBF16 (AAM18960), BnCBF17
(AAM18961) and LeDREB3 (AAO13360).
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tors CBF/DREBs control the expression of many stress-inducible genes in Arabidopsis
(Stockinger et al. 1997; Gilmour et al. 1998; Seki et al. 2003; Shinozaki et al. 2003).
Under normal conditions, neither CBF nor CBF-regulated target genes, such as COR
genes are expressed. However, at 4 ºC they are rapidly activated in response to cold
treatments. The expression of the CBF genes is induced very early, followed by the
expression of CBF-regulated target genes (Gilmour et al. 1998; Fowler and
Thomashow 2002). Genes of the CBF family are mainly induced by cold stress (Zarka
et al. 2003) However, a new member of the CBF family, CBF4, has recently been identified. This factor is up-regulated by drought, stress and ABA but not by low temperature (Haake et al. 2002). On the other hand, DREB2A and DREB2B subfamilies are
induced by drought stress and are able to induce the expression of genes that contain
the DRE/CRT cis-acting element in their promoters (Liu et al. 1998).
CBF homologues have also been found in other plants. BnCBFs factors from Brassica napus function in the same way, as trans-acting factors in low-temperature
responses, controlling the expression of cold-induced genes through an ABA-independent pathway. In wheat, the TaDREB1 product is induced by low temperature,
salinity and drought, and regulates the expression of the target gene, Wcs120, which
contains DRE motifs in its promoter (Shen et al. 2003b). In rice, expression of
OsDREB1A and OsDREB1B was induced by cold, whereas expression of
OsDREB2A was induced by dehydration and salt stress.
In maize, we have identified a new DRE-binding factors subfamily (Figure 3).
ZmDBF1 (Figure 3A), but not the related ZmDBF2 gene (Figure 3B), is induced
during maize embryogenesis and in all tissues of seedlings exposed to desiccation, salt
and ABA. Functional analyses using particle bombardment showed that ZmDBF1 acts
as an activator of DRE2-dependent transcription of rab17 by ABA. However,
ZmDBF2 overexpression causes the opposite effects and represses rab17 basal expression and its induction by ABA. These results suggest that ABA plays a role in the regulation of ZmDBFs activity, and indicates the existence of an ABA-dependent pathway
for the regulation of genes through the DRE/CRT element (Kizis and Pagès 2002).
Figure 3a and 3b. Sequence comparison between ZmDBFs and close homologues.
3a. Comparison between ZmDBF1 and their homologues. The protein sequences of ZmDBF1, rice
DBFs (OsDBF1 and 2), two putative DNA-binding proteins from Arabidopsis and tomato DREB3
were aligned. The shaded boxes presented the amino acid identity (dark grey: the identical amino
acids; medium grey: the similar amino acids; light grey: the rest of the amino acids). Protein names
are indicated at the left. Accession numbers correspond to NCBI database of analyzed proteins.
ZmDBF1 (AAM80486), OsDBF1 (AAP56252), OsDBF2 (AAP70033), LeDREB3 (AAO13360),
NP_195688 and NP_201318 from Arabidopsis.
3b. Comparison between ZmDBF2 and its homologue. The protein sequences of ZmDBF2
(AAM80485) and rice putative DNA binding protein (NP_922723) were aligned. The shaded
boxes presented the amino acid identity (dark grey: the identical amino acids; medium grey: the similar amino acids; light grey: the rest of the amino acids). Protein names are indicated at the left.
Accession numbers corresponding to NCBI database of analyzed proteins are also indicated.
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Figure 3a.
Figure 3b.
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An increasing number of DRE-binding factors have been identified in recent years
that mediate stress responses. The challenge now is to understand the relative roles
of these proteins in different pathways, their coordinated regulation and the interaction with other signalling elements. In the case of stress-regulatory factors, functional analyses in vivo are important not only to understand the molecular mechanisms of stress tolerance in plants but also to provide tools that might improve crop
productivity. In this regard, transcription factors are promising tools for genetic
engineering because their overexpression can lead to the up-regulation of a large
array of downstream genes.
Indeed, overexpression of specific DRE-binding genes in transgenic plants
resulted in plants more tolerant to drought, salt and freezing stresses, as shown in
Table 2. Arabidopsis plants overexpressing CBF1 showed increased tolerance to cold
stress without a cold acclimation period (Gilmour et al. 1998; Liu et al. 1998),
while expression of cbf1 gene in tomato increased drought (Hsieh et al. 2002). The
overexpression of CBF4 under non-stress conditions activated genes that are normally induced by cold and drought. These transgenic plants are also more tolerant
to freezing and osmotic stress. These results indicate that CBF4 plays a role in the
signal transduction of drought adaptation in Arabidopsis and suggest a cross-talk
between DREB2 and CBF/DREB1 regulatory systems (Haake et al. 2002). Transgenic Arabidopsis plants expressing OsDREB1A up-regulate stress-inducible target
genes regulated by DREB1A in Arabidopsis and present higher tolerance to drought,
salinity and freezing (Dubouzet et al. 2003). In transgenic tobacco, AhDREB1 led
to the accumulation of its putative downstream genes and these transgenic lines
showed an increased stress tolerance (Shen et al. 2003a).
On the other hand, constitutive overexpression of CBF/DREB genes generally
causes negative effects on plant growth and development. One solution to overcome this problem is the use of stress-inducible promoters to control the expression
specifically. This approach has been successfully used for the DREB1A/CBF3 Arabidopsis gene. Plants expressing DREB1A/CBF3 under control of the constitutive
cauliflower mosaic virus 35S promoter show a dwarf phenotype; however, plants
expressing the same gene under the regulation of rd29A, a stress-inducible promoter, were phenotypically normal and more tolerant to drought, salinity and
freezing (Kasuga et al. 1999; Yamaguchi-Shinozaki and Shinozaki 2001). Similarly,
tomato plants overexpressing CBF1 under the control of cauliflower mosaic virus
35S promoter showed severely reduced growth and were more tolerant to drought
stress, while transgenic plants expressing the factor directed by the barley ABRC1
or the Arabidopsis cor15a stress-inducible promoters showed normal growth, while
retaining water deficit resistance (Hsieh et al. 2002).
Post-translational modification such as phosphorylation may be necessary for
the activation of protein factors under drought stress conditions (Busk and Pagès
1998). This modification enhances the DNA-binding activity of several transcription factors. Among the DRE-binding proteins, the DREB2A subfamily is induced
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Table 2. Functional analysis of DRE-binding proteins in transgenic plants.
Overexpression
result
Drought tolerance
High salinity tolerance
Freezing tolerance
Gene overexpressed
Plant
AtDREB1A
Arabidopsis
AtCBF1
AtCBF4
OsDREB1A
AhDREB1
Tomato
Arabidopsis
Arabidopsis
Tobacco
AtDREB1A
Arabidopsis
AtCBF1
OsDREB1A
AhDREB1
Arabidopsis
Arabidopsis
Tobacco
AtDREB1A
Arabidopsis
AtCBF1
Arabidopsis
Brassica napus
Arabidopsis
Arabidopsis
Arabidopsis
AtCBF3
AtCBF4
OsDREB1A
References
Kasuga et al. 1999. YamaguchiShinozaki and Shinozaki 2001
Hsieh et al. 2002
Haake et al. 2002
Dubouzet et al. 2003
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Kasuga et al. 1999. YamaguchiShinozaki and Shinozaki 2001
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by drought and high-salinity stress, which indicates an important role of this group
of proteins in dehydratation-responsive gene expression. However, the overexpression in Arabidopsis of both AtDREB2A and OsDREB2A genes induced a weak
expression of the target genes. The authors suggest that not only transcriptional regulation but also post-translational modification may be required for the activation of
DREB2A proteins under drought stress conditions. Both AtDREB2A and
OsDREB2A factors contain a conserved serine/threonine-rich region adjacent to
the AP2/ERF domain, with putative sites of phosphorylation (Liu et al. 1998;
Nakashima et al. 2000; Dubouzet et al. 2003).
DBF1 defines a new family of DRE-binding factors
Sequence comparison of ZmDBF1 from maize, and CBF/DREBs from Arabidopsis and other plants (Liu et al. 1998; Kizis and Pagès 2002; Dubouzet el al. 2003),
show that sequence similarities are restricted to the AP2/ERF DNA-binding
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domain (Figure 2). In this domain, two amino acids, the 14th valine and the 19th
glutamic acid conserved in all DREB/CBF proteins have important roles in the
determination the DNA-binding specificity (Liu et al. 1998; Sakuma et al. 2002;
Dubouzet el al. 2003). However, DBF1 proteins have a conserved valine in the 14th
position but there is a highly-conserved leucine at the 19th position which is present in all DBF1 homologues identified to date. The conversion of the glutamic
acid to leucine might be responsible for different DNA-binding specificities
between DBF1s and CBF/DREB proteins.
There is no significant homology outside the AP2/ERF domain between DBF1
and CBF/DREB factors. It has been shown that AP2/ERF proteins contain a basic
region in the N-terminal that might function as nuclear localization signal and an
acidic C-terminal region that might function as a transcriptional activation
domain. The highly conserved C-terminal region of the maize DBF1 in rice, tomato and Arabidopsis homologues suggests that the DBF1 C-terminal region might be
involved in specific transcriptional roles of these proteins (Figure 3A).
Expression analyses of ZmDBF1, DREB2A, OsDREB2A and CBF4 show that
these genes are induced by dehydration and high-salt stresses (Liu et al. 1998;
Haake et al. 2002; Kizis and Pagès 2002; Dubouzet el al. 2003). The corresponding proteins specifically bound to the DRE sequence in vitro and activated the transcription of the β-glucuronidase (GUS) reporter gene driven by the DRE sequence
in Arabidopsis leaf, rice protoplasts and maize callus cells (Liu et al. 1998; Kizis and
Pagès 2002; Dubouzet et al. 2003). Comparative analyses under stress conditions
of organ-specific gene expression revealed several differences. Thus, in roots and
stems the ZmDBF1 gene expression is strongly induced by high salt, dehydration
and ABA treatment, while DREB2A expression is induced only by high salt and
dehydration in roots and specifically by high salt in stems. A weak induction of
DREB2A was also observed in leaves by osmotic stress, while the ZmDBF1 expression was induced by dehydration, salt, and ABA treatment in this organ
(Nakashima et al. 2000; Kizis and Pagès 2002).
The main difference between DBFs and CBF/DREB subfamilies consisted of the
up-regulation by ABA. The CBF/DREB members with the CBF4 exception and the
DBF2 factors are not induced by exposure to exogenous ABA, suggesting that these
proteins probably participate in an ABA-independent signalling transduction pathway. By contrast, the CBF4 factor and the DBF1 subgroup are up-regulated by
exogenous ABA and participate in ABA-dependent pathways (Liu et al. 1998;
Haake et al. 2002; Kizis and Pagès 2002; Dubouzet el al. 2003). Like CBF4, DBFs
factors may also be involved in the cross-talk between DREB/CBF regulatory networks in response to environmental stress.
In summary, based on sequence characteristics, specific expression in response to
environmental stresses and regulation by ABA, the maize DBF1 defines a new family of DRE-binding factors that may play an important role in drought tolerance in
plants.
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Conclusions and perspectives
Understanding the molecular mechanisms of plant responses to environmental
stresses such as drought, high salinity and low temperature is crucial for the manipulation of plants in order to improve their stress tolerance and crop productivity.
DRE-binding factors are a subfamily of AP2/ERF transcription factors with important roles in directing changes in gene expression during stress. This family of transcription factors regulate various stress-inducible genes separately or co-operatively
and constitute gene networks. Functional analysis of DRE-binding factors will provide more information on the complex regulatory networks that are involved in the
responses to abiotic stresses and future work should help delineate the different signalling pathways and their cross-talk during adaptation of plants to drought and
other stresses.
Acknowledgements
This work was supported by grants BIO2003-01133 from the Spanish MCYT and
QLRT 2001-00841 ROST from the EU.
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