Plant Science 180 (2011) 421–430

Contents lists available at ScienceDirect

Plant Science
journal homepage: www.elsevier.com/locate/plantsci

Review

More than the sum of its parts – How to achieve a specific transcriptional
response to abiotic stress
Lauri Vaahtera a , Mikael Brosché a,b,∗
a
Division of Plant Biology, Department of Biosciences, University of Helsinki, P.O. Box 65, (Viikinkaari 1), FI-00014 Helsinki, Finland
b
Institute of Technology, University of Tartu, Nooruse 1, Tartu 50411, Estonia

a r t i c l e i n f o a b s t r a c t

Article history: A rapid and appropriate response to stress is key to survival. A major part of plant adaptation to abiotic
Received 11 September 2010 stresses is regulated at the level of gene expression. The regulatory steps involved in accurate expres-
Received in revised form sion of stress related genes need to be tailored to the specific stress for optimal plant performance.
17 November 2010
Accumulating evidence suggests that there are several processes contributing to signalling specificity:
Accepted 19 November 2010
post-translational activation and selective nuclear import of transcription factors, regulation of DNA
Available online 26 November 2010
accessibility by chromatin modifying and remodelling enzymes, and cooperation between two or more
response elements in a stress-responsive promoter. These mechanisms should not be viewed as indepen-
Keywords:
Abiotic stress
dent events, instead the nuclear DNA is in a complex landscape where many proteins interact, compete,
Transcription factor and regulate each other. Hence future studies should consider an integrated view of gene regulation
Chromatin remodelling composed of numerous chromatin associated proteins in addition to transcription factors. Although most
Response element studies have focused on a single regulatory mechanism, it is more likely the combined actions of several
Signalling specificity mechanisms that provide a stress specific output. In this review recent progress in abiotic stress signalling
is discussed with emphasis on possible mechanisms for generating specific responses.
© 2010 Elsevier Ireland Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 422
2. Transcription factor activation and transport . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 422
2.1. General and gene specific transcription factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 422
2.2. Regulation of transcription factors through redox modification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 422
2.3. Regulation of transcription factors through protein degradation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423
2.4. Regulation of transcription factors through proteolytic activation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423
2.5. Regulation of transcription factors through protein–protein interaction and phosphorylation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424
2.6. Where does regulation of transcription factors take place? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424
2.7. Combined regulatory mechanisms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424
3. Chromatin remodelling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424
3.1. Post-translational histone modifications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 424
3.2. Histone modification enzymes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425
3.3. Chromatin-remodelling complexes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425
3.4. Other proteins associated with chromatin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425
4. Response elements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 426
4.1. Can response elements be predicted? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 426
4.2. Physical constraints of the transcription factor – response element interaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 426
4.3. Cooperation between response elements and transcription factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 426
5. Conclusions and perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 427
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 428
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 428

∗ Corresponding author at: Division of Plant Biology, Department of Biosciences,

University of Helsinki, P.O. Box 65, (Viikinkaari 1), FI-00014 Helsinki, Finland. Tel.:
+358 919159436; fax: +358 919157788.
E-mail address: mikael.brosche@helsinki.fi (M. Brosché).

0168-9452/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.plantsci.2010.11.009
422 L. Vaahtera, M. Brosché / Plant Science 180 (2011) 421–430
1. Introduction
Due to their sessile lifestyle plants are constantly confronted
with unfavourable growth conditions. Extreme temperatures,
drought, salinity, air pollutants, or changes in light intensity or
quality – commonly referred to as “abiotic stress” – impose con-
straints on the plant. One of the hallmarks of plant defences against
these stresses is a large reprogramming of gene expression through
regulation of transcription. The development of microarray tech-
nology in the early 2000s led to identification of several hundred to
thousands of genes in plants with altered expression in response to
abiotic stress [1]. Genes with altered expression during stress are
often important for adaptation to stress, and transgenic plants that
overexpress such a gene can have increased stress tolerance [2–4].
Both specific and non-specific effects contribute to the mecha-
nisms of damage for each abiotic stress. Examples of specific effects
include salt stress, where the toxic Na+ need to be transported
out of the cytoplasm [5]. Another example is ultraviolet-B radi-
ation (UV-B, 280–320 nm) which causes formation of cyclobutane
pyrimidine dimers in DNA, a damage which can be repaired by DNA
photolyases [6]. In addition to specific effects many stresses share
a common mode of action (general effects): salt, drought and cold
stress all lead to osmotic stress [3], and most (if not all) stresses lead
to transient increase in reactive oxygen species (ROS) and cytosolic
Ca2+ , and activation of kinase cascades [7–9]. Abiotic stresses also
lead to increased concentrations of the stress related hormones sal-
icylic acid (SA), jasmonic acid (JA), abscisic acid (ABA) and ethylene
[10–14].
To translate a stress exposure into appropriate changes in
gene expression suitable signalling pathways needs to be acti-
vated, ultimately ending up with a transcription factor (TF) at
the promoter of the gene to be transcribed. Given that a stress is
composed of specific and general effects on the plant it could be pre-
dicted that a comparison of several different stresses would reveal
both specific and universal stress induced transcriptome changes.
Indeed, such complex transcriptome changes were first described
in yeast [15,16], subsequently meta-analysis of several hundred
array experiments found a similar response in Arabidopsis thaliana
[17–20]. What is the role of a universal stress response? In yeast it
is involved in cross-protection, i.e. exposure to one stress increases
the resistance to a second, unrelated stress [16]. In plants cross-
protection (or cross-tolerance) has long been observed, although
the mechanisms involved are still mostly unknown [21,22].
Changes in gene expression can be detected within 15–30 min
of an applied stress [19] and can last for several days reflect-
ing a remarkable capacity of the plant to regulate and adjust
gene expression. We are still oblivious to many of the regulatory
mechanisms integrating and controlling the specific and universal
changes in gene expression that every stress induces. Gene spe-
cific TFs have long been studied as the executers of transcriptome
changes [3]. Some of the mechanisms which can be used to gener-
ate a stress specific gene expression response include TF activation
and nuclear transport, chromatin remodelling to allow appropriate
DNA binding, and response element (RE) specificity. Undoubtedly
post transcriptional events including mRNA splicing and stabil-
ity, small RNA regulation and translation initiation are important
as well to generate a specific response, for these mechanisms the
reader is referred to a recent review [23]. This review focus mainly
on Arabidopsis, but examples from other species will be used to
illustrate key concepts.
2. Transcription factor activation and transport
TFs can be broadly classified into general TFs (transcription ini-
tiation complex) and gene specific TFs. The general TF complex is
required to activate RNA polymerase II and transcription of genes.
However, this complex has received relatively little attention in
plants. Instead most focus has been directed towards studies on
gene specific TFs which regulate several processes in plants includ-
ing development and stress responses. To achieve specificity in
abiotic stress responses, a specific TF should bind only to genes
whose transcription is required for adaptation to that particu-
lar stress. The first step in gene regulation is to activate the TF
through post-translational modification and/or import of the TF to
the nucleus. Post-translational modifications of TFs include redox
modification, proteolytic activation, protection from degradation,
and phosphorylation (Table 1).
2.1. General and gene specific transcription factors
Transcription is initiated by the activation of RNA polymerase
II at the transcription start site. General TF complexes bind to core
promoter elements to form preinitiation complexes, exemplified
by the TFIID complex containing a TATA binding protein (TBP)
and several TBP-associated factors [24,25]. Our knowledge of these
complexes is almost completely derived from non-plant species.
However, components of the TFIID complex appear conserved
across species, including Arabidopsis. Furthermore, protein interac-
tion studies indicate a similar structure and function of the complex
in plants [25]. Most studies in plants have instead focused on gene
specific TFs, which bind to more upstream promoter elements and
regulate genes in a specific context, for example development and
stress. A TF typically contains at least two different domains – a
DNA binding domain and a transcriptional activation or repres-
sor domain. Slightly different classification criteria have been used
by different authors in the definition of TFs, thus it was recently
estimated that the Arabidopsis genome encodes about 2000 TFs,
corresponding to 7% of the genes in this species [26]. This high
number could contribute to strict control of transcription through
regulated TF activation and location. Since protein synthesis takes
place in the cytosol, in principle all TFs could be regulated by
restricting access to the nucleus [27]. However, direct regulation
of TF subcellular localization has only been demonstrated for rela-
tively few TFs in response to abiotic stress. A frequent observation
in genome-wide expression analysis is that many genes with rapid
changes in gene expression after abiotic stress treatments encode
TFs [19,20]. Therefore, gene specific TFs can be divided into two
classes, early acting TFs have a role in the immediate response and
are regulated through post-translational mechanisms. The early
TFs increase the expression of a second class of TFs with a role in
later and prolonged stress responses. A variety of post-translational
modifications are used to activate TFs; these modifications should
be rapid and target specific amino acids or amino acid motifs to
provide specificity.
2.2. Regulation of transcription factors through redox
modification
Cysteine residues in proteins provide a rich target for modifi-
cation by a variety of oxidant molecules including ROS and nitric
oxide, and reduction through enzymatic mechanisms [28]. The
NPR1 (NONEXPRESSOR OF PATHOGENESIS-RELATED (PR) GENES1)
protein provides protection against many biotic stresses; it is an
essential regulator of many SA inducible genes and of systemic
acquired resistance. In addition NPR1 is also a signalling compo-
nent of abiotic stress responses, for example signalling induced by
the air pollutant ozone [29]. Direct targets of NPR1 include several
TGA class bZIP TFs that regulate responses to both biotic and abiotic
stresses [30]. Localization, activation and interaction of NPR1 with
TGA TFs are regulated through redox changes and protein–protein
interactions. In non-stressed plant cells NPR1 is maintained in the
 L. Vaahtera, M. Brosché / Plant Science 180 (2011) 421–430 423

Table 1 cytosol in an oligomeric state through disulfide bridges. Reduction

Representative mechanisms involved in control of stress induced transcriptional
of Cys-82 and Cys-216 through THIOREDOXIN H5 leads to forma-
regulation.
tion of NPR1 monomers that translocate to the nucleus [31,32].
Protein Functional Regulatory mechanism Reference Inside the nucleus NPR1 interacts with TGA type TFs including
category
TGA1 and TGA2. The NPR1–TGA1 interaction is also under redox
NPR1 Transcriptional Kept inactive in as an [31] control, NPR1 only interacts and enhances DNA binding activity of
co-regulator oligomer in the cytosol. reduced TGA1 [33]. Specific cysteines of TGA1 and NPR1 are targets
Activated through reduction
for S-nitrosylation by nitric oxide [32,34]. NPR1 regulation of TGA2
of Cys82 and Cys216 leading
to monomer formation and follows a different mechanism; TGA2 alone binds to its promoter
nuclear transportation. element as an oligomer that represses transcription. Addition of
TGA1 Transcription TGA1 DNA binding activity is [33,34] activated NPR1 leads to formation of a new complex consisting of
factor regulated through redox and
2:2 copies of NPR1 and TGA2 that activate transcription [35]. Con-
S-nitrosylation, and
interaction with NPR1. stitutive activation of defence responses is energetically costly, thus
TGA2 Transcription TGA2 oligomer repress [35] prolonged defence activation should be avoided [36,37]. Consistent
factor expression. Interaction with with this, NPR1 in the nucleus is phosphorylated and targeted for
NPR1 leads to formation of proteasome-mediated degradation through the E3 ligase compo-
2:2 complex capable of
nent CULLIN3 and the COP9 (CONSTITUTIVE PHOTOMORPHOGENIC
activating expression.
DREB2A Transcription Constitutively targeted for [39,40] 9) signalosome [38].
factor degradation in control
conditions. Nuclear localized
in response to heat or 2.3. Regulation of transcription factors through protein
drought stress.
degradation
bZIP17 Transcription ER membrane tethered TF. In [43,46,47]
bZIP28 factor response to heat or ER stress
bZIP60 N-terminal part is cleaved off Arabidopsis DREB2A (DEHYDRATION-RESPONSIVE ELEMENT
and is transported to the BINDING PROTEIN 2A) is a TF with dual functions in regulating
nucleus.
drought and heat stress induced transcriptional changes [39,40].
NTL6 Transcription Plasma membrane tethered [48]
factor TF. In response to cold stress Full length DREB2A-GFP is undetectable under normal growth con-
transmembrane part is ditions but strongly accumulates in the nucleus after heat shock.
cleaved off and the processed Dissection of the protein structure of DREB2A revealed a negative
form is transported to the regulatory domain and its deletion lead to a constitutively active
nucleus.
protein. The presence of a PEST sequence in the regulatory domain
WRKY25 Transcription Regulated through [56]
WRKY33 factor phosphorylation by MPK4 suggests that DREB2A is under control of the ubiquitin–proteasome
and interaction with MKS1. system, and thus DREB2A would only accumulate in the nucleus
WRKY53 Transcription WRKY53 DNA binding [62] during stress [39,40]. DREB2A binds to the promoter of the heat
factor enhanced by phosphorylation
shock TF HsfA3 which in turn regulates heat shock protein expres-
by MEKK1, expression of
WRKY53 regulated by MEKK1.
sion [41]. Thus DREB2A–HsfA3 form a transcriptional cascade in
WRKY70 Transcription Expression of WRKY70 is [89] heat stress responses. Similarly, in light signalling the level of sev-
factor regulated by histone H3K4 eral TFs, including PIF3 and HY5, are regulated through degradation
methylation. [42].
HDA6 Histone HDA6 regulates the level [77]
deacetylase histone acetylation, and
expression of salt and ABA
regulated genes. 2.4. Regulation of transcription factors through proteolytic
HDA19 Histone HDA19 regulates the level of [79] activation
deacetylase H3K9ac and interacts with
WRKY38 and WRKY62.
The endoplasmic reticulum (ER) membrane-tethered TF bZIP
HOS15 Histone HOS15 binds and regulates [81]
deacetylation the acetylation status of 17 and bZIP28 are activated through proteolytic release of the N-
histone H4, and regulates terminus followed by relocalization to the nucleus. This activation
expression of cold regulated occurs in response to heat shock or chemical treatments (tuni-
genes.
camycin), which increase the amount of unfolded protein in the ER
SPLAYED Chromatin Loss of function of the [85]
remodeler SWI/SNF2 ATPase SPLAYED
[43,44]. In the heat stress response bZIP28 regulates various genes
causes defects in including HSP26.5-P and Bip2, furthermore the bzip28 mutant is
developmental and biotic sensitive to heat stress. Cleavage of bZIP17 and bZIP28 are mediated
stress responses. by a subtilisin-like serine protease S1P and a metalloprotease S2P
H2A.Z Histone variant H2A.Z wraps DNA more [90]
[45,46]. The s1p and s2p mutants are sensitive to salt stress, which
tightly which restricts gene
expression. in s2p could be rescued by expression of the truncated, active ver-
ERSE1 – Two short sequences [44] sions of bZIP17 and bZIP28 [45,46]. A third ER membrane localized
response separated by 10 nucleotides – TF, bZIP60, is also involved in the ER stress response and activated
element CCAAT-N10-CACG – provide
through proteolytic cleavage [47]. Interestingly, S1P and S2P are not
specificity for expression of
genes involved in the
involved in processing of bZIP60 indicating that other proteases are
unfolded protein response. also involved in ER stress signalling [47].
EE + ABREL – Two response elements, [102] In cold stress the plasma membrane bound TF NTL6 is cleaved
response evening element and an ABA to an active form which is imported into the nucleus and acti-
elements response element like motif,
vates defence gene expression [48]. Genomewide analysis predicts
together regulate cold
induced genes. at least 85 membrane bound TFs in Arabidopsis [49]; collectively
they may represent a quick way for plants to alter gene expression
by proteolytic release of an active TF.
424 L. Vaahtera, M. Brosché / Plant Science 180 (2011) 421–430
2.5. Regulation of transcription factors through protein–protein
interaction and phosphorylation
The Arabidopsis chloroplast magnesium–protoporphyrin IX
chelatase H subunit (CHLH/ABAR) spans the chloroplast envelope
and the cytosolic C-terminus interacts with the TFs WRKY18, 40
and 60 [50]. Interestingly these TFs are usually found in the nucleus
where they act as negative regulators of transcription of ABA related
TFs including ABI5 (ABA INSENSITIVE 5). The WRKY TFs relocate to
the cytosol by an unknown mechanism in response to an increase
in ABA concentration, and interact with ABAR; hence their removal
from the nucleus leads to activation of transcription. These three
WRKYs also play a role in biotic stress responses; triple mutants
are more resistant to the hemibiotrophic bacterial pathogen Pseu-
domonas syringae and sensitive to necrotrophic Botrytis cinerea
infection [51]. Marker gene analysis indicates that these WRKYs
are negative regulators of SA signalling and positive regulators of
JA signalling. The proteins form various hetero- and homodimers
which affect their DNA binding properties [51].
Both biotic and abiotic stress signalling pathways utilize WRKY
TFs [52]. Plants lacking WRKYs or overexpressing WRKYs often
have similar phenotypes. This raises the question whether the TFs
in this family can be used to generate a sufficiently specific response
and if so, how? Interaction between WRKY TFs could increase the
potential for distinct responses. WRKY70 has been proposed to
mediate cross talk between SA- and JA-dependent defence sig-
nalling. While activating the expression of pathogenesis-related
SA-induced genes, it suppresses JA-inducible genes [53]. WRKY70
probably acts together with the closely related WRKY54 since the
wrky54 wrky70 double mutant display enhanced phenotypes com-
pared to the single mutants [54]. One mechanism to achieve the
required specificity, shown in parsley, could be to constantly keep
the WRKY binding sites (W-box) occupied by WRKY TFs [55]. Acti-
vation of defences involves post translational activation of the TF
and/or replacement by a competing WRKY TF. Thus the final “out-
put” from WRKY TFs would be a result of competition between
several WRKYs for their binding sites. One candidate mechanism to
activate WRKY TFs is through phosphorylation by protein kinases.
MPK (Mitogen-activated protein (MAP) kinase) cascades are impli-
cated in multiple abiotic stresses and in particular MPK3, MPK4
and/or MPK6 are activated by most stresses [9]. MPK4 phospho-
rylates WRKY25 and WRKY33, which are further regulated by the
MPK4 interacting protein MKS1 [56]. MPK regulation of TFs extend
beyond the WRKYs, experiments with a protein microarray plat-
form identified the most prominent targets of ten different MPKs
as TFs including WRKY, TGA, MYB and bZIP TFs [57].
Ca2+ is a ubiquitous signalling molecule during stress. Among
the proteins responding to Ca2+ signals are calcium dependent
kinases (CDPKs) [7]. CPK4 and CPK11 are components in ABA sig-
nalling where they phosphorylate the TFs ABF1 (ABA RESPONSIVE
ELEMENT BINDING FACTOR1) and ABF4 [58]. Further support for
a role of Ca2+ in ABA signalling comes from promoter analyses of
genes with rapid, increased expression in response to Ca2+ . These
promoters are significantly enriched for ABA response elements
suggesting that Ca2+ is an intermediate in ABA signalling [59].
2.6. Where does regulation of transcription factors take place?
A simple pathway for TF regulation would suggest an ordered
model for TF regulation–translation of the TF in the cytosol, activa-
tion by post-translational modification leading to nuclear import,
where the TF can regulate gene expression. However, experimental
data indicates much greater complexity in TF regulation. MPK3 and
MPK6 are rapidly transported to the nucleus following ozone stress
[60]. The MAP kinase phosphatase ATMKP2 resides in the nucleus
[61]. Thus the regulatory components for phosphorylation of TFs
are present in the nucleus as well as in the cytosol, and the pres-
ence of the phosphatase in the nucleus suggests a potential rapid
turn off mechanism of the kinases. Interestingly, at least one kinase
is also a DNA binding protein. MEKK1 (a MAP kinase kinase kinase)
has a dual role in regulation of senescence: it can directly bind to the
promoter of WRKY53, secondly it phosphorylates WRKY53 and reg-
ulates the activity of the TF [62]. Targeting TFs or co-repressors for
degradation is a common event in the nucleus, an illustrative exam-
ple is provided in JA signalling. In the inactive state, the MYC2 TF is
kept in a complex with JAZ (JASMONATE-ZIM-DOMAIN PROTEIN),
NINJA (NOVEL INTERACTOR OF JAZ) and TOPLESS which silence
transcription. Activation of JA signalling by binding of bioactive JA-
isoleucine to the receptor COI1 leads to rapid degradation of JAZ,
resulting in release of MYC2 to activate transcription [63]. In sum-
mary, regulation of TF activity can occur both in the cytosol and the
nucleus, and furthermore nuclear transport does not necessarily
have to be coupled with TF activation.
2.7. Combined regulatory mechanisms
As seen above, for a given TF its activity and/or localization can
be regulated through a variety of different mechanisms includ-
ing rapid degradation, proteolytic activation, phosphorylation and
redox regulation. This division into separate mechanisms is arti-
ficial and most likely several mechanisms act together to activate
appropriate TFs although this remains to be experimentally veri-
fied. Overall, the molecular mechanisms by which TFs are retained
in the cytosol remain largely unknown. An interesting example for
a possible mechanism is provided by the mammalian NRF2. This
TF is retained in the cytosol and targeted for proteasomal degra-
dation by Keap1 [64,65]. Several small molecules (including ROS,
antioxidants and electrophiles) have the ability to modify specific
cysteine thiol groups on Keap1 resulting in release and transloca-
tion of NRF2 to the nucleus. NRF2 activates xenobiotic resistance
phase 2 genes in the nucleus, such as glutathione transferases
and NAD(P)H:quinone oxidoreductase (NQO1) [64,66]. This redox
mechanism shares some similarities with the redox activation of
NPR1 and TGA1, and suggests that more plant TFs might be reg-
ulated through redox modification. For example, most Arabidopsis
MYB TFs contain a conserved pair of cysteines that could be used
to regulate protein stability or activity [67].
3. Chromatin remodelling
Once inside the nucleus, the TF will not immediately have access
to the promoter of target genes. Nuclear DNA is packed on his-
tones forming chromatin. This structure prevents transcription
[68], and regulated opening of the chromatin structure can pro-
vide specificity in allowing TF binding to selected genes. Changes
in chromatin structure are mediated by post-translational mod-
ification of histones catalyzed by histone modifying enzymes. In
addition the position of nucleosomes can be altered by chromatin
remodelers.
3.1. Post-translational histone modifications
It would be impossible to contain the genetic material in the
nucleus without tight packing of DNA [69]. This is accomplished
through wrapping of DNA onto the core histones, octamers con-
sisting of two copies each of H2A, H2B, H3 and H4, followed
by assembly into higher order chromatin structures. The tightly
packed DNA is not accessible for TFs and the transcription machin-
ery. Relaxation of the nucleosome structure provides a suitable
control point for giving TFs access to only a specific subset of
genes. In several eukaryotes, including Arabidopsis, correlation of
the physical position of genes with analysis of whole genome
 L. Vaahtera, M. Brosché / Plant Science 180 (2011) 421–430
expression data indicates that neighbouring genes tend to have
similar expression profiles [70]. Thus, the local overall chromatin
structure has a significant impact on gene expression, but this by
itself is unlikely to provide sufficient specificity. Analysis of spe-
cific modifications shows that Arabidopsis has a similar set of post
translational histone modifications as other eukaryotes including
humans and yeast [71]. These include acetylation or methylation of
histones, for example histone H3 Lys4 trimethylation (H3K4me3)
a marker of active genes, and H3K9 deacetylation, H3K9me2 and
H3K27me2 dimethylation, markers for silenced genes [72]. For
a comprehensive review of all histone modifications see [73].
Genome-wide investigation of H3K9 modifications indicates that
H3K9ac correlates with high gene expression and H3K9me2 with
low gene expression [74]. Comparison with other histone modifi-
cations suggests that a balance of several modifications determines
the final output in gene expression; genes with H3K9ac alone are
highly expressed, whereas genes also modified with H3K27me3 or
DNA methylation are expressed to a lower extent [74]. One sim-
ple genetic tool to quickly estimate the contribution of chromatin
status on gene expression utilizes a transcriptionally silenced GUS
reporter Arabidopsis line. Treatment of this line with heat or UV-B
stress result in strong GUS staining, demonstrating that stress expo-
sure removes the silenced state of chromatin which furthermore is
associated with increased histone H3 acetylation [75].
3.2. Histone modification enzymes
The N-terminal part of histones is the target for post trans-
lational modifications affecting the structure of chromatin [68].
Histone modification enzymes include histone acyltransferases,
histone deactetylases, histone methytransferases and histone
demethylases. A few of these proteins have been shown to be
involved in regulation of gene expression in response to cold,
drought or osmotic stress. A direct role for histone acyltrans-
ferases in regulation of cold induced genes was demonstrated
through reduced expression of cold induced COR genes in Ara-
bidopsis mutants (ada2b and gcn5) encoding subunits of the ADA
and SAGA histone acyltransferases complex [76]. Similarly, plants
with low histone deacetylase HDA6 levels displayed compro-
mised expression of ABA and salt stress marker genes including
DREB2A and RD29A (RESPONSIVE TO DESSICATION 29A) after stress
treatment [77]. Plants overexpressing the histone deactetylase
HD2C have increased expression of certain drought related genes
and increased tolerance to salt and drought [78]. In biotic stress
responses the histone deacetylase HDA19 interacts with the
TFs WRKY38 and WRKY62 and regulates resistance to bacterial
pathogens [79] and gene expression in the JA and ethylene sig-
nalling pathways [80]. HDA19 regulates the level of H3K9ac which
correlates with actively expressed genes [74]. Some of the tar-
get genes for this histone modification include genes encoding
proteins with a function in chromatin modification, e.g. UVR8 (UVB-
RESISTANCE 8) [74].
Arabidopsis HOS15 (HIGH EXPRESSION OF OSMOTICALLY
RESPONSIVE GENES 15) encodes a WD40 repeat protein with sim-
ilarities to human transducin beta-like 1 (TBL1), a protein complex
component involved in histone deacetylation. The elevated expres-
sion of cold regulated genes in the hos15 mutant indicates that
HOS15 acts as a transcriptional repressor [81]. HOS15 binds to his-
tone H4 and regulates the acetylation status of histone H4 and
subsequent transcriptional output [81].
3.3. Chromatin-remodelling complexes
The tight interaction between DNA and the core histones block
access for TFs to DNA, i.e. “hide” crucial response elements. The
position of nucleosomes can be temporarily altered by chromatin
425
remodelers using energy from ATP, thus providing access for TFs
and the transcription machinery [82]. In addition the chromatin
structure can be altered by replacing core histone subunits with
other histone variants (H2A.Z) [82].
The minimal functional core of the SWI/SNF (SWITCH/SUCROSE
NONFERMENTING) chromatin-remodelling complexes include
SWI/SNF2 ATPase, SNF5, SWP73 and a pair of SWI3 subunits
[83]. The Arabidopsis genome encodes four different SWI3 proteins
which form various homo- and heterodimers. Mutation in SWI3
genes causes embryo lethality or severe developmental defects
[83]. The ABA signalling component HAB1 (HOMOLOGY TO ABA
INSENSITIVE1) interacts with the SWI/SNF subunit SWI3B to nega-
tively regulate its function. Activation of ABA signalling in response
to stress inhibits HAB1 and releases the SWI/SNF complex to posi-
tively affect gene expression [84]. Loss of function of the SWI/SNF2
ATPase SPLAYED (SYD) causes defects in developmental and biotic
stress responses [85]. The Arabidopsis mutant syd has reduced
expression of JA responsive genes and increased susceptibility to
infection with B. cinerea [85]. Induction of SA marker genes is not
affected indicating a specific effect on JA signalling.
The SWR1 complex in plants controls the integration of the
alternate histone H2A.Z into chromatin. Mutants with reduced lev-
els of H2A.Z or with defects in the SWR1-dependent process of
integrating H2A.Z are early flowering and have altered expres-
sion of genes related to phosphate starvation and SA marker genes
[86,87]. One intriguing contrast of SWI1/SNF versus the SWR1 com-
plexes relates to their control of expression of genes regulated by
the hormones SA and JA. Mutants for the SWI1/SNF complex (e.g.
syd) are impaired in expression JA regulated genes; whereas SWR1
mutants (e.g. pie1, arp6, hta9 hta11) have altered expression of SA
regulated genes [85,87]. Positive and negative interactions between
SA and JA signalling pathways are frequently observed [88] and
could possibly be reflected also in differences in chromatin struc-
ture. Accordingly, the promoter of the WRKY70 TF is a target for
H3K4me3 modification resulting in altered WRKY70 expression and
a shift in the balance between SA and JA signalling [89].
The alternate histone H2A.Z also plays a major role in plant
sensing of temperature. New alleles of the SWR1 subunit APR6
(ACTIN-RELATED PROTEIN 6) were identified using a screen for
mutants with elevated expression of a temperature regulated
reporter gene construct, HSP70-Luc [90]. The arp6 mutant has con-
stitutive expression of genes at 12 ◦ C that the wild type would
express only at ambient temperature. In apr6, less nucleosomes
contain H2A.Z and a double mutant lacking two H2A.Z genes
(hta9 hta11) phenocopies arp6 [90]. H2A.Z-containing nucleosomes
wrap DNA more tightly resulting in blocked transcription. H2A.Z
is released from chromatin in response to increased temperature,
which activates transcription and provides the plant with a tem-
perature response mechanism [90].
3.4. Other proteins associated with chromatin
Several proteins with unknown molecular function associate
with or co-localize with chromatin, and could represent new regu-
lators of chromatin structure in response to stress. The OXIDATIVE
STRESS 3 (OXS3) gene was isolated from a Brassica juncea cDNA
expression library in yeast as a transformant that conferred toler-
ance to cadmium. In yeast and Arabidopsis OXS3 provides tolerance
to cadmium or oxidizing chemical exposure, but not to salt, osmotic
or heat stress [91]. OXS3 co-localized with histone H4, suggesting
that it could be part of a chromatin modifying complex [91].
UV-B radiation is a minor component of sunlight reaching the
earth surface but due to its high energy content it has the capacity to
affect multiple plant functions, including changes in gene expres-
sion [92]. Research in maize implicates chromatin remodelling as
an important regulator for adaptation to elevated UV-B. Plants
426 L. Vaahtera, M. Brosché / Plant Science 180 (2011) 421–430
adapted to growth at high altitudes (thus experiencing higher UV-
B doses) have increased expression of genes encoding putative
members of chromatin remodelling complexes [93]. Direct mea-
surement of histone acetylation indicates higher acetylation of
histones H3 and H4 after UV-B treatment in tolerant lines [94].
The Arabidopsis uvr8 mutant is specifically defective in mediating
responses to UV-B, including changes in gene expression. UVR8
is related to the human REGULATOR OF CHROMATIN CONDENSA-
TION1, however recent research suggests that UVR8 may possess a
yet unidentified activity [92]. UV-B promotes nuclear localization
of UVR8 where it associates with histone H2B and regulated gene
expression through the TF HY5 [95,96].
4. Response elements
A cis-acting DNA regulatory element, also known as response
element (RE) or promoter element, is a DNA-sequence to which
a specific transcription factor binds and regulates transcription.
In eukaryotes, REs are enriched within a few hundred base pairs
upstream from the transcription start site, but also occur down-
stream of the gene as well as far upstream. Usually REs is one
part of a larger assembly which consist of many REs, TFs, and their
co-regulators which together initiate transcription [97].
4.1. Can response elements be predicted?
Understanding how TFs bind to specific REs is necessary but
not sufficient to comprehend the regulatory network of gene
expression. Unfortunately no simple rules dictate how amino acids
interact with DNA bases and at present it is not possible to predict
the binding site of a TF based on its amino acid sequence. Simi-
larly, our ability to predict the sequence of REs from other types
of data is limited. One common strategy to suggest new putative
REs starts from large scale gene expression data sets, followed by
identification of a set of genes responding similarly to a given treat-
ment. Subsequently the promoters of these genes are analyzed for
statistical over-representation of short promoter motives (see [98]
for an example of this strategy in identifying oxidative stress REs).
Despite its importance in predicting candidate REs these purely
bioinformatic approaches are currently not sophisticated enough
to provide “true” REs. In vivo experiments are required to verify
the function of a putative RE in a biological context. Typically many
experimentally defined REs in the Arabidopsis genome (for an up to
date listing see the Arabidopsis Gene Regulatory Information Server
http://arabidopsis.med.ohio-state.edu/) are short and degenerate,
and are mostly derived from in vitro binding studies. Thus, it is
not uncommon to find a given RE distributed in thousands of sites
across the genome. Apparently underlying mechanisms must exist
that control TF binding to a RE only in a specific context. Some
of these mechanisms could include cooperation between two or
more REs, spacing between REs, nucleotides surrounding the RE
and competition between TFs with activator or repressor activity
domains.
4.2. Physical constraints of the transcription factor – response
element interaction
A simple model implies that each TF has a unique sequence pref-
erence and exclusively regulates genes containing this sequence in
their promoters. However, this probably does not reflect the real in
vivo situation. It would be difficult to produce a sufficiently large
collection of TFs with sequence specificities high enough to allow
accurate regulation of the complex gene networks in eukaryotes.
This simple model might work in bacteria, but calculations and in
vivo measurements suggest that the number of different DNA bind-
ing proteins in E. coli is close to the maximum allowed by physical
constraints [99]. Increasing the number of DNA binding proteins
in the cell further would result in a steep increase in the time that
it takes for a given TF to find its RE. This is the result of a molec-
ular “crowding effect”, which prevents the TF from sliding along
the DNA to find its RE faster. If the DNA strand is full of DNA bind-
ing proteins they block each other [99]. These results from bacteria
imply that eukaryotes cannot manage their more complex genomes
merely by increasing the number of TF species, because the absolute
number of TFs in the nucleus is limited.
Thus, the question is how eukaryotic TFs can regulate their
more complex genome without sacrificing specificity? One way
to achieve accuracy of regulation is by cooperation between sev-
eral REs and proteins. When two TFs with rather general sequence
specificities are combined into a dimer, they bind to a promoter
containing two appropriately spaced REs. Even weak or indirect
protein–protein interactions would result in a large increase in
specificity (for a review on TF synergy, see [100]).
4.3. Cooperation between response elements and transcription
factors
A search for REs in the promoter of a gene of interest will often
retrieve several predicted and relatively few experimentally val-
idated REs (http://arabidopsis.med.ohio-state.edu/AtcisDB/). This
means that currently it is only possible to evaluate whether two REs
and TFs interact to regulate a target gene on a case by case analysis
in wet lab experiments. Regulation of abiotic stress induced gene
expression by cooperation between REs and TFs take place in the
unfolded protein response and in cold and osmotic stress.
Activation of the unfolded protein response (UPR) by heat stress
or chemicals leads to endoplasmic reticulum stress-responsive ele-
ment I (ERSE-I) driven gene expression. ERSE-I (CCAAT-N10-CACG)
is composed of two REs to which bZIP28 and CCAAT box binding fac-
tors bind during the UPR. bZIP28 can bind to CACG of ERSE I alone,
but CCAAT box binding factors require bZIP28 to for binding to ERSE
I. Due to the helical nature of DNA, exact spacing of REs is important
to enable interaction between TFs. If the REs are on opposing sides
of the DNA helix the TFs might fail to interact. Addition or removal
of only one of the ten nucleotides in between the TF binding sites of
ERSE-I is enough to decrease DNA binding affinity and reporter gene
expression [44]. The CCAAT box binding factors are heterotrimeric
complexes composed of NF-Y (NUCLEAR FACTOR-Y) subunits in
a wide range of eukaryotes including Arabidopsis. In the fungus
Aspergillus nidulans both nuclear import and DNA binding affinity of
the NF-Y subunit HapC are regulated through redox modifications
of specific cysteine groups mediated by thioredoxin [101]. Over-
all UPR combines several of the mechanisms described in Section
2: TFs activated by different mechanisms, bZip28 through prote-
olytic cleavage of a membrane bound precursor and NF-Y through
redox modification; together they bind appropriately spaced
REs.
Combining two REs with separate functions can yield novel
specificity. Cold regulation of the genes COL1 (CONSTANS-LIKE 1)
and COR27 (COLD REGULATED GENE 27) is mediated by two separate
REs: a circadian clock evening element (EE) and an ABA response
element-like motif (ABREL) [102]. An artificial promoter consisting
of alternating EE and ABREL motives is sufficient to provide cold
regulation.
TFs belonging to the bZIP family usually bind DNA as homo-
or heterodimers. Transcriptional activation of proline dehydro-
genase in response to hypoosmolarity was regulated through
heterodimers of AtbZIP53 together with either AtbZIP10 or other
group-S bZIPs [103]. Interestingly the heterodimer appears to bind
to a single RE, the ACTCAT-motif, although since the reporter con-
struct used contained tandem ACTCAT-motives it remains possible
that two REs are required for efficient transcription. A requirement
 L. Vaahtera, M. Brosché / Plant Science 180 (2011) 421–430 427

Fig. 1. A model proposing how specificity in abiotic stress signalling may be conditioned through several layers of interdependent processes. Stress-induced post-translational
activation of TFs leads to migration from the cytosol to the nucleus. Post-translational modifications include redox modification of cysteine residues, phosphorylation and
cleavage of membrane bound TFs. Inside the nucleus target genes can be organized in a “locked” chromatin structure preventing transcription activation. In response to
abiotic stress chromatin modifying proteins, exemplified by the SWR1 complex, are recruited to “open” the chromatin in the promoter region which allows binding of TFs.
Several other proteins are bound to chromatin including histone modifying enzymes e.g. histone deacetylase. Proteins associated with chromatin could possibly also act as
guides (G) to help TFs find their right position through protein–protein interaction. Specificity is further increased through linked REs and transcription factor dimerization.
Regulatory proteins including kinases and components for targeted protein degradation are present both in nucleus and the cytosol. Entrance to the nucleus and positive
interactions are indicated with green arrows and cytosol retention or negative interactions with red arrows. A and B indicate cooperating REs and TFs.

for heterodimerization is that both partners are expressed in the
same tissues. Expression analyses of the whole C/S1 bZIP TF fam-
ilies have revealed some of the possible bZIP combinations that
could regulate stress and development responses (Weltmeier et al.
[103]).
Even a short, generic sequence, such as ACGT, can provide
specificity if partnered with a second RE. The UV-B-regulated CHS
(CHALCONE SYNTHASE) promoter contains an ACGT RE and MYB
RE spaced approximately 25 bp apart. Mutation of either element
repressed the activity of the promoter, indicating the requirement
of two TFs to activate the promoter [104]. The effect of altering spac-
ing between REs has been studied with the versatile promoter core
sequence ACGT that confers responsiveness to various stimuli, such
as light, SA, and ABA [105]. In stable transgenic plants a reporter
construct with two ACGT sequences separated by 5 nucleotides
was responsive to both SA and ABA. Increasing the spacer length
to 10 nucleotides suppressed both responses, however a promoter
with 25 bp spacer was again responsive to ABA, but not to SA. This
probably reflects the formation of different TF complexes at the
promoter. Extensive testing of pathogen inducible REs indicates
that proper spacing between REs is critical for high transcriptional
activity [106].
The examples above demonstrate that transcriptional activa-
tion is regulated through the interaction between REs and TFs in
response to different stresses. One crucial factor for the forma-
tion of suitable protein interactions is the proper spacing between
REs. The TF complexes may also include “bridging” or scaffold pro-
teins that facilitate formation of the active complex. An example
for this are the TFs TT2 (TRANSPARENT TESTA 2), TT8 (TRANSPAR-
ENT TESTA 8), and TTG1 (TRANSPARENT TESTA GLABRA 1), which
form a ternary complex to synergistically specify the expression of
BANYULS and proanthocyanidin biosynthesis in Arabidopsis [107].
One underexplored topic is the role of the nucleotides immediately
adjacent to the core binding motif. In the case of WRKY53 these sur-
rounding nucleotides define whether the TF activated or repressed
the transcription of downstream genes [108]. This suggests that in
addition to the core RE motif that mediates TF binding; there is an
additional role of the surrounding DNA in mediating the effect on
transcriptional regulation.
5. Conclusions and perspectives
Appropriate activation of gene expression is controlled by mul-
tiple regulatory steps: TF activation and/or nuclear translocation,
transcriptionally permissive chromatin status and specific REs
(Fig. 1). Recent high resolution maps of proteins associated with
chromatin in Drosophila indicate that on average all nucleosomes
are bound by one or more proteins [109]. Furthermore principal
component analysis indicates that chromatin can be divided into
five classes with different properties including transcriptional acti-
vation status. In plants the three processes chromatin status, TF
binding and RE sequence specificity have often been studied in
isolation, mostly due to the complexity of defence signalling. The
simplistic model where the DNA strand is “naked” and waiting
for a TF to bind and activate transcription should be replaced by
more complex models. The nuclear DNA is in a dynamic landscape
consisting of chromatin with various modifications, chromatin
modifying enzymes, chromatin remodelers, transcriptional repres-
428 L. Vaahtera, M. Brosché / Plant Science 180 (2011) 421–430
sors and REs which may or may not already be occupied by other
TFs or proteins.
If plant nuclear DNA is organized similarly to Drosophila then
all positions on chromatin are bound by various proteins. This sug-
gests that a new TF entering the nucleus will not immediately find
its target RE through protein–DNA interaction. Instead it would be
guided to its position through protein–protein interactions (exem-
plified by the “Guide” protein in Fig. 1), and only when it reaches the
right “neighbourhood”, perhaps marked by the chromatin struc-
ture, would protein–DNA interaction be the final step for the TF
to reach its target gene(s). Furthermore, if the target RE is already
occupied, the new TF will have to replace and/or compete with
other TFs. Targeted degradation of repressors and/or other block-
ing proteins could facilitate access to DNA and the transcription
machinery, as exemplified by the JA signalling pathway where rapid
degradation of JAZ proteins release the TF MYC2 from repression
[63].
Another open question is how the sequence specificity of chro-
matin modifications is generated? This could be achieved through
the combined action of three mechanisms discussed in this review.
Specific REs could recruit TFs, which in turn interact with compo-
nents of chromatin modification (exemplified by the interaction
of HDA19 with WRKY38 and WRKY62 [79]). Thus, one interesting
prospect for the future is to investigate whole protein complexes
associated with actively transcribed genes and determine all of the
involved components: chromatin modifying enzymes, TFs, repres-
sor proteins, and other proteins that regulate chromatin structure
or guide protein interactions and/or protein degradation. Undoubt-
edly, some of these proteins will be present in an active form only
in response to abiotic stress and by changing one component; the
complex can generate the required stress specificity.
Full understanding of the complex interactions at the chro-
matin “landscape” will require new technological developments
and genome-wide analysis methods. In particular, “next gener-
ation” sequencing technologies offer opportunities to map the
position of histone modifications, DNA methylation and REs at very
high resolution in planta [110]. The first steps in these methods
often require protein crosslinking and/or co-precipitation of the
DNA under study followed by sequencing to identify positions of
interest. Hence, specific antibodies need to be developed towards
various histone modifications and variants, histone modifying and
associated proteins and TFs. Several different treatments should be
compared side by side to determine the specificity of signalling.
Several in vitro high throughput methods can be employed
to complement the in vivo approaches. The in vitro DNA bind-
ing affinities and sequence specificities of many (if not all) TFs
can be determined by multiplexed massively parallel SELEX (sys-
tematic evolution of ligands by exponential enrichment) [111].
Improved yeast two and three hybrid analyses using pair-wise
interaction tests between all Arabidopsis TFs could reveal the extent
of homo- and hetero dimerization and higher order complexes, as
was recently illustrated with MADS box TFs [112].
Both in vivo and in vitro studies would benefit from improve-
ments in computational methods. Algorithms developed to find
novel REs are mostly designed to identify single, short REs. Thus,
more advanced search models should be designed to look for two
or more linked REs. A wealth of information has been generated
from large gene expression analysis and genome sequencing, which
can be queried through different web based databases [113]. Steps
are now being taken to integrate different data sources and pro-
vide new infrastructure to let scientists access the information and
generate new hypotheses in plant signalling pathways, exemplified
by the iPlant Colloborative http://iplantcollaborative.org/. Targeted
reverse genetics using improved gene network models can guide
which genes or gene families should be investigated in functional
studies for stress signalling [114]. Using a more global view of gene
regulation and taking into account all steps involved in stress sig-
nalling it is likely that new insights will be revealed into plant
adaptation to a harmful environment.
Acknowledgements
We thank Michael Wrzaczek, Kirk Overmyer and Jaakko Kan-
gasjärvi for comments on the manuscript. Work in MB laboratory
is supported by grants from the University of Helsinki, Academy of
Finland (decision no 135751 and 140981) and the Estonian Science
Foundation (contract MTT9).
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