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The regulation of transcription factor
activity in plants Claus Schwechheimer and Michael Bevan
The predominant mechanism for controlling gene expression in eukaryotes appears to be
regulation at the transcriptional level. Transcriptional regulation of gene expression is
mediated by transcription factors, which activate or repress transcription. These activators and
repressors act through several mechanisms (including DNA–protein interactions, protein–
protein interactions and modification of the chromatin structure) and are themselves regulated in a variety of ways. Using various modes, a single transcription factor can influence the
transcription of different target genes. Recent research on these regulatory mechanisms in
plants has provided insight into the underlying processes.
I
n multicellular organisms, the expression of thousands of
protein-encoding genes is subject to complex patterns of spatial
and temporal regulation. The first step in transcriptional regulation of any gene is the integration of various signals so that they
change the rate of transcription of their target gene1–3. The specificity of gene expression is at least in part governed by transcriptional activators and repressors, many of which bind DNA in a
sequence-specific manner4. These proteins are themselves subject
to regulation at different levels5 (Fig. 1).
assigned to one of several classes; these include basic regionleucine zipper (bZIP) proteins, MYB-like proteins, MADS-domain
proteins, helix–loop–helix proteins, zinc-finger proteins and homeobox proteins6,7. Within these classes, DNA-binding specificity is
brought about by subtle changes in the amino acid sequence of the
DNA-binding domain.
In sharp contrast to the DNA-binding domains of transcription factors, the amino acid sequences that comprise their activation and repression domains are not conserved, and consensus
sequences have yet to be derived from the many eukaryotic actiActivators and repressors
vation domains that have been functionally defined to date8,9. On
Transcriptional activators and repressors generally consist of several the basis of their amino acid composition, activation domains
functional modules with DNA-binding, activation and repression can only be classified as being rich in acidic amino acids, in
domains. On the basis of their usually highly conserved DNA- glutamines, prolines, or serine and threonine residues. Howbinding domains, most eukaryotic transcription factors can be ever, not all activation domains fit into these general categories,
and mutational analyses (also
carried out with plant transcription factors) have shown
that those amino acids that
Coactivator binding
predominate in activation doand other interactions
mains are not necessarily important for their function8,10,11.
Coact
DNA
Transcription
It may be that the precise
machinery
Transcription
molecular interactions that
TF
TF TF
lead to transcriptional actiDNA-binding
pre-mRNA
vation vary between different
Dimerization
Splicing
transcription factors in difPost-translational
P
mRNA
ferent promoter contexts, or
L modifications
that mechanisms other than
specific protein–protein interTF
TF
Nucleus
TF
actions govern transcriptional
activation.
mRNA export
The classification system of
Nuclear import
transcription
factor represmRNA
P
sion domains is poorly characL
Translation
terized9. This may be because
TF
TF
TF
research on repressors is comTF
plicated by the fact that it is
Post-translational
modifications
difficult to distinguish between
Dissociation
genuine effects of a repressor
Inhibitor binding
Cytoplasm
protein and the effects caused
IN
by a dominant negative form
TF
of the protein. It is thought that
IN
repressors act in one of three
ways:
Fig. 1. Regulatory mechanisms that can play a part in the regulation of transcription factor activity.
• By binding to a cognate proAbbreviations used TF, transcription factor; Coact, coactivator; IN, inhibitor; P, phosphate; L, ligand
moter site and blocking the
binding. Adapted from Ref. 5.
binding of general transcription factors or activators.
378
October 1998, Vol. 3, No. 10
Copyright © 1998 Elsevier Science Ltd. All rights reserved. 1360 - 1385/98/$19.00 PII: S1360-1385(98)01302-8
trends in plant science
reviews
(b)
Anthocyanins
A
B3
VP1
Light
ABA
GT Sph G-box
C1
Seed maturation
B2
ABA
VP1
EMBP1 (+ osZIP-1a)
osZIP-2a
osZIP-2b
RY
Fig. 2. (a) Two selfed maize ears segregating for Viviparous-1 (vp1).
The vp1 mutant seed germinate prematurely on the maize cob. In this
mutant, anthocyanin synthesis in the aleurone layer is suppressed (right
cob) because of the lack of VP1; VP1 activates Colourless-1 (C1) gene
expression, a transcriptional activator of genes that encode for enzymes
of the anthocyanin biosynthetic pathway. Light can activate C1 expression independently from VP1; this accounts for the anthocyanin pigmentation on the viviparous kernels of the left cob where the husks of the
ear have been removed to admit light. (b) VP1 participates in the activation of C1 and EM and the repression of a-amylase gene expression.
The schematic shows the different target genes, and factors that have
a positive or negative influence on gene expression. Domains of VP1
known to be involved in the particular processes are indicated above
the protein. Abbreviations: ABA, abscisic acid; GA, gibberellic acid.
• By blocking transcription by means of inhibitory interactions
with general transcription factors or activators.
• By altering the higher-order DNA structure in a way that inhibits transcription.
VIVIPAROUS-1, an activator and repressor of gene
expression
The complexities of transcriptional regulation have been elegantly
demonstrated in a series of studies on the maize transcription factor Viviparous-1 (VP1). VP1 is a key regulator of seed maturation
and germination and severe vp1 mutations cause premature germination of the seed on the maize cob12,13 (Fig. 2a). During seed
maturation, VP1 acts as transcriptional activator of the (wheat)
EM gene14 and the (maize) Colourless-1 (C1) genes15,16, but at the
same time it can mediate repression of (barley) a-amylase gene
expression17 (Fig. 2b). All vp1 mutants are insensitive to abscisic
acid (ABA), and as they do not express the C1 transcriptional regulator they are devoid of anthocyanin pigmentation in the seed in
the dark (Fig. 2a). However, there are colourless mutants of VP1
that do not express C1, but which undergo normal seed dormancy
and also express the EM gene18. This suggests that two different
mechanisms govern the activation of C1 and EM gene expression
during seed development.
Sph
1a
1b
EM
Seed germination
ABA
B1
VP1
?
GA
a-Amylase
VP1 activates C1 gene expression
The expression of C1 can be activated independently by three factors:
VP1 expression, ABA and light15,16 (Fig. 2a). The Sph-promoterelement of the C1 promoter has been shown to be sufficient and
necessary for VP1-mediated activation in transient expression
studies of maize vp1 embryos and suspension culture cells15,16. A
corresponding VP1 DNA-binding domain (B3 domain) was recently
identified that can bind to the Sph-element in vitro19. Transient expression experiments have revealed that this DNA-binding domain is
required for transcriptional activation of C1 in the absence of light20.
In addition, an activation domain (the A domain) was mapped to the
highly acidic N-terminus of VP1, which when deleted abolishes
transcriptional activation in transient expression assays14. The C1
promoter element that confers a response to ABA is tightly linked
to, but apparently distinct from, the VP1-responsive Sph-element16.
Light-inducibility of the C1 promoter is thought to be mediated
by a promoter region that comprises a light-responsive G-box element located downstream of the Sph-element16 (Fig. 2b). This latter finding is intriguing, because G-box binding factors (GBFs)
have been suggested to be important for the expression of lightregulated genes21. Synthesis of VP1 in organs other than seeds
cannot activate C1 expression, but light is sufficient to activate C1
expression in seeds and leaves (Fig. 2a).
October 1998, Vol. 3, No. 10
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VP1 activates expression of the EM gene
In the EM promoter, VP1 can activate transcription from several
promoter elements. VP1 is sufficient to activate transcription from
an Sph-like and an RY-promoter element and is necessary but not
sufficient for transcriptional activation from two G-box like motifs
(Em1a and Em1b)22,23 (Fig. 2b). The expression of EM from these
G-box elements is synergistically activated by VP1 and ABA. As
a tetramer, Em1a and Em1b can confer ABA-responsiveness to a
minimal promoter22. Studies using southwestern screening have
identified the bZIP transcription factor EMBP1 that binds the
Em1a promoter, and to a lesser extent the Em1b element23.
In contrast to its role on the C1 promoter, VP1 appears to act by
facilitating the binding of EMBP1 to the Em1a and Em1b elements.
Binding studies in vitro revealed that a basic region of VP1 (the BR2
domain) possessing a weak and non-specific DNA binding capacity
can greatly enhance the binding of EMBP1 to its target sites. Thus,
while VP1 activates the expression of C1 through direct promoter
binding and transcriptional activation, VP1 potentiates EM expression by encouraging binding of the transcription factor EMBP1.
mediated expression24. PvALF, a putative homolog of VP1, acts
as a transcriptional activator of the storage proteins phytohemagglutinin and b-phaseolin in cotyledons. In bombardment studies,
it was shown that the activation potential of PvALF can be further
enhanced by the addition of ABA – an effect similar to that observed with VP1. Transcriptional activation mediated by PvALF
appears to be counteracted by the two bZIP-like repressors ROM1
and ROM2, which are expressed at different stages during cotyledon development25,26 (Fig. 3). ROM1 represses transcription early
in seed maturation but its expression declines at the onset of
storage protein synthesis26, whereas the onset of ROM2 expression coincides with the decline of storage protein production25. A
reduction in storage protein concentrations has also been reported
for vp1 mutant maize plants27, and repressors similar to the ones
identified for PvALF may also control storage protein production
in maize.
Dimerization
Transcription factor activity is also affected by interactions with
other DNA-binding proteins or non DNA-binding accessory
VP1 is a repressor of a-amylase gene expression
proteins28. Dimerization increases the number of transcription
In contrast to its activating function, VP1 represses induction of factor complexes that can be formed from a smaller number of
a germination-specific a-amylase gene during seed maturation17 homeomeric components and can have a positive or negative in(Fig. 2b). Repression occurs even when the VP1 activation do- fluence on their DNA-binding characteristics, activation potenmain has been deleted. This suggests that the VP1 domain required tial, or nuclear localization. The dimerization process is regulated
for repression is distinct from the activation function, and that by the availability of their respective partners, their affinity for
VP1 is directly repressing a-amylase gene expression rather than each other and the affinity of the dimer for other components
activating the expression of another protein that in turn represses (such as DNA) – this sensitizes responses to minor fluctuations in
a-amylase gene expression. The repression domain on VP1 that is effector concentration.
responsible for this has yet to be determined. During seed germiThe bZIP and the MADS-domain class of transcription factors
nation, a-amylase production is induced by gibberellic acids, but are well characterized dimerizing proteins in plants. In the case of
VP1 overexpression can override hormone-induced activation dur- the wheat bZIP protein EMBP1, which acts together with VP1 on
ing seed germination.
the EM promoter, three bZIP proteins (osZIPs) that appear to
interact have been identified from rice using an in vitro interacPvALF-mediated gene expression
tion screen29. Gel retardation experiments have revealed that the
The regulation of storage protein expression during seed maturation heterodimer formed by EMBP1 and osZIP-1 shows enhanced
in cotyledons of Phaseolus vulgaris, has some similarities to VP1- binding to the Em-1a element in the EM-promoter, but the heterodimer formed by EMBP1
and osZIP-2a or osZIP-2b prevents binding of EMBP1 to
its cognate promoter binding
ROM1
PvALF
ROM2
site (Fig. 2b). In addition to
SPs
SPs
SPs
osZIP-1, histone H1 has also
been reported to enhance bindTranscription
Repression
Repression
Activation
status
ing of EMBP-1 to its promoter
> activation
> activation
> repression
binding sites in vitro30. This
suggests that the interplay
Days after
between inhibitory and stimu9
11
13
15
17
19 21
23
25
27 29 31
33
35
flowering
latory heterodimers is a reguROM1
Repressor
latory mechanism for EMBP-1
expression
activity, and DNA-binding in
ROM2
general. However, these difActivator
PvAlf
ferent proteins originate from
expression
different species, and further
Storage
b-Phaseolin
research will be needed to conprotein
firm these observations.
expression
The activity of the MybPhytohemagglutinin
like transcription factor C1 is
also regulated by heterodimerFig. 3. The activity of PvALF, a putative bean homologue of maize Viviparous-1 (VP1), is counteracted
ization31. Genetic studies and
by the repressor proteins ROM1 and ROM2, which are expressed at different stages during seed matutransient expression assays reration and germination. The three proteins together regulate the synthesis of the bean storage proteins
vealed that C1 is unable to acti(SPs) b-phaseolin and phytohemagglutinin.
vate expression of its target
genes (these encode enzymes
380
October 1998, Vol. 3, No. 10
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of the anthocyanin biosynthetic pathway) in the absence of the
helix-loop-helix transcription factor B-Peru32–34. Using the yeast
two-hybrid system, it was found that B-Peru can interact with
the DNA-binding domain of C1 (Ref. 33) and that this interaction enhances the DNA-binding specificity of C1. However,
the extent to which the putative basic helix–loop–helix DNAbinding domain of B-Peru participates in this DNA-binding is
unclear.
Dimerization can also regulate nuclear localization. Evidence
from genetic analysis have suggested that the activities of the homeotic MADS-box proteins APETALA-3 (AP3) and PISTILLATA
(PI), which in Arabidopsis are responsible for the initiation of
petal and pistil formation, are interdependent35. DNA-binding studies in vitro have revealed that AP3 and PI can form a heterodimer.
By transforming AP3- and PI-GUS fusion constructs into an
ap3/pi mutant background, it was possible to demonstrate that the
interaction between AP3 and PI is crucial for the nuclear import
of the transcription factors. In these transgenic plants, GUS activity was detected solely in the cytoplasm when only one of
the two MADS-box proteins was present, whereas reporter gene
activity was localized to the nucleus in plants expressing both
proteins.
Cytosol
(a)
COP1
HY5
Nucleus
CHS1-promoter
(b)
Light signal
?
COP1
Cytosol
Nuclear
export?
?
COP1
Nuclear localization
The import and export of proteins to and from the nucleus is a
highly regulated process36. Entry of transcription factors into the
nucleus can occur by diffusion or it can be a regulated process
responsive to exogenous or endogenous signals. Also, as observed
with AP3/PI, there may be co-transport of two or more factors.
The nuclear import of large proteins is carried out by transporter
proteins that shuttle between the cytoplasm and the nucleus, or by
receptors at the nuclear pores. Import is mediated by nuclear localization signals (NLSs), short peptide sequences rich in arginine
and lysine residues, which have been found in several transcription factors36.
Two NLSs have been identified in the transcription factor
OPAQUE-2 (O2), which regulates the production of zein storage
proteins in the maize endosperm37. One of the NLS domains was
mapped to the basic DNA-binding domain of O2, suggesting that
the DNA-binding domain of this bZIP protein is identical to its
nuclear localization domain. However, using an o2 mutant deficient for DNA binding, it was shown that nuclear localization and
DNA binding are independent functions38. This mutant protein
still entered the nucleus but could no longer activate transcription
of O2 target genes. In tobacco, a protein complex located at the
nuclear pores strongly binds to the NLS of O2 and may be implicated in nuclear import of this transcription factor39.
An example of the control of transcription by dimerization and
nuclear localization is the interaction between COP1 and the bZIP
transcription factor HY5. The pleiotropic Arabidopsis cop1 mutants have the phenotype of light-grown seedlings when grown
in the dark. The COP1 protein has therefore been assigned the role
of a repressor of photomorphogenesis. By contrast, on the basis
of the light-insensitivity of hy5 seedlings, HY5 has been defined
as a positive regulator of photomorphogenesis. Using COP1-GUS
fusions, it has been shown that COP1 protein is localized in the
nucleus in the dark but that it leaves the nucleus after light irradiation40. Genetical evidence had already suggested that COP1 and
HY5 interact directly, and a direct interaction between the two has
now been established in vitro and in vivo41–43. This led to the
development of a model in which COP1 interacts with HY5 in the
dark to keep it in an inactive state. In the light, COP1 releases
HY5 and leaves the nucleus, allowing subsequent activation of
target genes by HY5 (Ref. 42; Fig. 4).
HY5
Dissociation
Nucleus
HY5
CHS1-promoter
Fig. 4. The activity of the Arabidopsis bZIP transcription factor
HY5 is regulated by COP1. (a) In the dark, COP1 is localized to
the nucleus where it binds HY5. (b) After light irradiation, COP1
releases HY5 and leaves the nucleus such that HY5 can then activate its target genes.
Post-translational events
Post-translational modification by protein phosphorylation activates the nuclear import of transcription factors and stimulates or
represses the DNA-binding affinity or the activation potential of
many transcription factors44. Different phosphorylation events are
not mutually exclusive, as phosphorylation events at several sites
could play a part in different aspects of the regulation of transcription factor activity. In plants, the predominant kinase used in
phosphorylation studies is casein kinase II (CKII)45,46. The bZIP
transcription factor GBF1 from Arabidopsis can be phosphorylated
by purified CKII from broccoli46 and by extracts from nuclei of
Arabidopsis45. This modification greatly enhances its DNA-binding
activity.
Phosphorylation is also crucial for regulation of the DNAbinding activity of O2 (Ref. 47). Up to seven distinct phosphorylated forms of O2 can be identified in protein extracts from maize
endosperm separated on two-dimensional protein gels. Only the
unphosphorylated O2 forms bind DNA with high affinity, and the
phosphorylated forms only bind DNA after dephosphorylation by
phosphatase treatment. The phosphorylation pattern of O2 is subject to diurnal changes: hypophosphorylated forms accumulate by
day and hyperphosphorylated forms in the dark. This pattern suggests a temporal regulation of O2 activity ensuring that storage proteins are synthesized at times of high energy supply. The specific
kinases that participate in this process have yet to be identified.
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A link between a receptor kinase and
transcription has been established for the
plant disease resistance gene, Pto, which
confers resistance to bacterial speck disease in tomato. The Pto serine/threonine
kinase can interact directly not only with
the pathogenic elicitor avrPto, but also with
at least three transcription factors belonging
to the class of ethylene-responsive element
binding proteins (EREBP) from tobacco48.
The kinase activity of Pto and its interaction
with transcription factors suggests a direct
regulation of their activity through phosphorylation (Fig. 5), although their DNAbinding affinity was not influenced by
phosphorylation. Cognate promoter elements for EREBPs have been found in
several pathogenesis-related proteins and
upon infection with the pathogen the expression of some of these genes is upregulated.
Pseudomonas syringae
AvrPto
Secretion
P
?
Pto
Cytoplasm
Hypersensitive
response
Pto
?
?
?
P
P
P
Pti-6
Pti-4
Outlook
Pti-5
We have summarized some interesting
examples of the regulation of transcription
factors. The availability of large mutant collections, in particular from Arabidopsis and
maize, will lead to the isolation of more transcription factor mutants. Mutant analysis
will provide an important tool for the study
of these transcription factors. The inclusion
of genomics approaches in several plant
species combined with classical genetics
and improved in vitro techniques should
allow a more mechanistic understanding of
how plant transcription factors work. In this
respect, the development of reliable and
reproducible in vitro transcription systems
is an important objective49. In conjunction,
these tools will help us to decipher the
plant-specific regulatory networks and so
understand the process from signal transduction to transcriptional regulation.
Nucleus
Nuclear import?
P
PR-box
Fig. 5. The cytoplasmic receptor Pto-kinase interacts with the elicitor of Pseudomonas
syringae, AvrPto, and subsequently phosphorylates several Pti transcription factors belonging
to the class of ethylene-responsive element binding proteins (EREBPs). EREBP-promoter
binding sites have been found in several promoters of pathogenicity-related proteins. The role
of phosphorylation in regulating the activity of these transcription factors remains unclear.
Abbreviation: P, phosphate.
We thank Roderick Card for critical reading of the manuscript.
Our work is supported by the Ministry of Agriculture, Fisheries
and Food (MAFF).
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46 Klimczak, L.J., Schindler, U. and Cashmore, A.R. (1992) DNA binding
activity of the Arabidopsis G-box binding factor GBF1 is stimulated by
phosphorylation by casein kinase II from broccoli, Plant Cell 4, 87–98
47 Ciceri, P. et al. (1997) Phosphorylation of Opaque2 changes diurnally and
impacts its DNA binding activity, Plant Cell 9, 97–108
48 Zhou, J., Tang, X. and Martin, G.B. (1997) The Pto kinase conferring
resistance to tomato bacterial speck disease interacts with proteins that bind a
cis-element of pathogenesis-related genes, EMBO J. 16, 3207–3218
49 Sugiura, M. (1997) Plant in vitro transcription systems, Annu. Rev. Plant
Physiol. Plant Mol. Biol. 48, 383–398
Claus Schwechheimer and Michael Bevan* are at the
Molecular Genetics Dept, John Innes Centre, Norwich, Norfolk,
UK NR4 7UH; Claus Schwechheimer is presently at the
Dept for Molecular, Cellular and Developmental Biology,
Yale University, New Haven, CT 06520-8140, USA.
*Author for correspondence (tel +44 1603 452571;
fax +44 1603 505725; e-mail bevan@bbsrc.ac.uk).
Students – 50% off all new subscriptions
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October 1998, Vol. 3, No. 10
383
reviews
The regulation of transcription factor
activity in plants Claus Schwechheimer and Michael Bevan
The predominant mechanism for controlling gene expression in eukaryotes appears to be
regulation at the transcriptional level. Transcriptional regulation of gene expression is
mediated by transcription factors, which activate or repress transcription. These activators and
repressors act through several mechanisms (including DNA–protein interactions, protein–
protein interactions and modification of the chromatin structure) and are themselves regulated in a variety of ways. Using various modes, a single transcription factor can influence the
transcription of different target genes. Recent research on these regulatory mechanisms in
plants has provided insight into the underlying processes.
I
n multicellular organisms, the expression of thousands of
protein-encoding genes is subject to complex patterns of spatial
and temporal regulation. The first step in transcriptional regulation of any gene is the integration of various signals so that they
change the rate of transcription of their target gene1–3. The specificity of gene expression is at least in part governed by transcriptional activators and repressors, many of which bind DNA in a
sequence-specific manner4. These proteins are themselves subject
to regulation at different levels5 (Fig. 1).
assigned to one of several classes; these include basic regionleucine zipper (bZIP) proteins, MYB-like proteins, MADS-domain
proteins, helix–loop–helix proteins, zinc-finger proteins and homeobox proteins6,7. Within these classes, DNA-binding specificity is
brought about by subtle changes in the amino acid sequence of the
DNA-binding domain.
In sharp contrast to the DNA-binding domains of transcription factors, the amino acid sequences that comprise their activation and repression domains are not conserved, and consensus
sequences have yet to be derived from the many eukaryotic actiActivators and repressors
vation domains that have been functionally defined to date8,9. On
Transcriptional activators and repressors generally consist of several the basis of their amino acid composition, activation domains
functional modules with DNA-binding, activation and repression can only be classified as being rich in acidic amino acids, in
domains. On the basis of their usually highly conserved DNA- glutamines, prolines, or serine and threonine residues. Howbinding domains, most eukaryotic transcription factors can be ever, not all activation domains fit into these general categories,
and mutational analyses (also
carried out with plant transcription factors) have shown
that those amino acids that
Coactivator binding
predominate in activation doand other interactions
mains are not necessarily important for their function8,10,11.
Coact
DNA
Transcription
It may be that the precise
machinery
Transcription
molecular interactions that
TF
TF TF
lead to transcriptional actiDNA-binding
pre-mRNA
vation vary between different
Dimerization
Splicing
transcription factors in difPost-translational
P
mRNA
ferent promoter contexts, or
L modifications
that mechanisms other than
specific protein–protein interTF
TF
Nucleus
TF
actions govern transcriptional
activation.
mRNA export
The classification system of
Nuclear import
transcription
factor represmRNA
P
sion domains is poorly characL
Translation
terized9. This may be because
TF
TF
TF
research on repressors is comTF
plicated by the fact that it is
Post-translational
modifications
difficult to distinguish between
Dissociation
genuine effects of a repressor
Inhibitor binding
Cytoplasm
protein and the effects caused
IN
by a dominant negative form
TF
of the protein. It is thought that
IN
repressors act in one of three
ways:
Fig. 1. Regulatory mechanisms that can play a part in the regulation of transcription factor activity.
• By binding to a cognate proAbbreviations used TF, transcription factor; Coact, coactivator; IN, inhibitor; P, phosphate; L, ligand
moter site and blocking the
binding. Adapted from Ref. 5.
binding of general transcription factors or activators.
378
October 1998, Vol. 3, No. 10
Copyright © 1998 Elsevier Science Ltd. All rights reserved. 1360 - 1385/98/$19.00 PII: S1360-1385(98)01302-8
trends in plant science
reviews
(b)
Anthocyanins
A
B3
VP1
Light
ABA
GT Sph G-box
C1
Seed maturation
B2
ABA
VP1
EMBP1 (+ osZIP-1a)
osZIP-2a
osZIP-2b
RY
Fig. 2. (a) Two selfed maize ears segregating for Viviparous-1 (vp1).
The vp1 mutant seed germinate prematurely on the maize cob. In this
mutant, anthocyanin synthesis in the aleurone layer is suppressed (right
cob) because of the lack of VP1; VP1 activates Colourless-1 (C1) gene
expression, a transcriptional activator of genes that encode for enzymes
of the anthocyanin biosynthetic pathway. Light can activate C1 expression independently from VP1; this accounts for the anthocyanin pigmentation on the viviparous kernels of the left cob where the husks of the
ear have been removed to admit light. (b) VP1 participates in the activation of C1 and EM and the repression of a-amylase gene expression.
The schematic shows the different target genes, and factors that have
a positive or negative influence on gene expression. Domains of VP1
known to be involved in the particular processes are indicated above
the protein. Abbreviations: ABA, abscisic acid; GA, gibberellic acid.
• By blocking transcription by means of inhibitory interactions
with general transcription factors or activators.
• By altering the higher-order DNA structure in a way that inhibits transcription.
VIVIPAROUS-1, an activator and repressor of gene
expression
The complexities of transcriptional regulation have been elegantly
demonstrated in a series of studies on the maize transcription factor Viviparous-1 (VP1). VP1 is a key regulator of seed maturation
and germination and severe vp1 mutations cause premature germination of the seed on the maize cob12,13 (Fig. 2a). During seed
maturation, VP1 acts as transcriptional activator of the (wheat)
EM gene14 and the (maize) Colourless-1 (C1) genes15,16, but at the
same time it can mediate repression of (barley) a-amylase gene
expression17 (Fig. 2b). All vp1 mutants are insensitive to abscisic
acid (ABA), and as they do not express the C1 transcriptional regulator they are devoid of anthocyanin pigmentation in the seed in
the dark (Fig. 2a). However, there are colourless mutants of VP1
that do not express C1, but which undergo normal seed dormancy
and also express the EM gene18. This suggests that two different
mechanisms govern the activation of C1 and EM gene expression
during seed development.
Sph
1a
1b
EM
Seed germination
ABA
B1
VP1
?
GA
a-Amylase
VP1 activates C1 gene expression
The expression of C1 can be activated independently by three factors:
VP1 expression, ABA and light15,16 (Fig. 2a). The Sph-promoterelement of the C1 promoter has been shown to be sufficient and
necessary for VP1-mediated activation in transient expression
studies of maize vp1 embryos and suspension culture cells15,16. A
corresponding VP1 DNA-binding domain (B3 domain) was recently
identified that can bind to the Sph-element in vitro19. Transient expression experiments have revealed that this DNA-binding domain is
required for transcriptional activation of C1 in the absence of light20.
In addition, an activation domain (the A domain) was mapped to the
highly acidic N-terminus of VP1, which when deleted abolishes
transcriptional activation in transient expression assays14. The C1
promoter element that confers a response to ABA is tightly linked
to, but apparently distinct from, the VP1-responsive Sph-element16.
Light-inducibility of the C1 promoter is thought to be mediated
by a promoter region that comprises a light-responsive G-box element located downstream of the Sph-element16 (Fig. 2b). This latter finding is intriguing, because G-box binding factors (GBFs)
have been suggested to be important for the expression of lightregulated genes21. Synthesis of VP1 in organs other than seeds
cannot activate C1 expression, but light is sufficient to activate C1
expression in seeds and leaves (Fig. 2a).
October 1998, Vol. 3, No. 10
379
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VP1 activates expression of the EM gene
In the EM promoter, VP1 can activate transcription from several
promoter elements. VP1 is sufficient to activate transcription from
an Sph-like and an RY-promoter element and is necessary but not
sufficient for transcriptional activation from two G-box like motifs
(Em1a and Em1b)22,23 (Fig. 2b). The expression of EM from these
G-box elements is synergistically activated by VP1 and ABA. As
a tetramer, Em1a and Em1b can confer ABA-responsiveness to a
minimal promoter22. Studies using southwestern screening have
identified the bZIP transcription factor EMBP1 that binds the
Em1a promoter, and to a lesser extent the Em1b element23.
In contrast to its role on the C1 promoter, VP1 appears to act by
facilitating the binding of EMBP1 to the Em1a and Em1b elements.
Binding studies in vitro revealed that a basic region of VP1 (the BR2
domain) possessing a weak and non-specific DNA binding capacity
can greatly enhance the binding of EMBP1 to its target sites. Thus,
while VP1 activates the expression of C1 through direct promoter
binding and transcriptional activation, VP1 potentiates EM expression by encouraging binding of the transcription factor EMBP1.
mediated expression24. PvALF, a putative homolog of VP1, acts
as a transcriptional activator of the storage proteins phytohemagglutinin and b-phaseolin in cotyledons. In bombardment studies,
it was shown that the activation potential of PvALF can be further
enhanced by the addition of ABA – an effect similar to that observed with VP1. Transcriptional activation mediated by PvALF
appears to be counteracted by the two bZIP-like repressors ROM1
and ROM2, which are expressed at different stages during cotyledon development25,26 (Fig. 3). ROM1 represses transcription early
in seed maturation but its expression declines at the onset of
storage protein synthesis26, whereas the onset of ROM2 expression coincides with the decline of storage protein production25. A
reduction in storage protein concentrations has also been reported
for vp1 mutant maize plants27, and repressors similar to the ones
identified for PvALF may also control storage protein production
in maize.
Dimerization
Transcription factor activity is also affected by interactions with
other DNA-binding proteins or non DNA-binding accessory
VP1 is a repressor of a-amylase gene expression
proteins28. Dimerization increases the number of transcription
In contrast to its activating function, VP1 represses induction of factor complexes that can be formed from a smaller number of
a germination-specific a-amylase gene during seed maturation17 homeomeric components and can have a positive or negative in(Fig. 2b). Repression occurs even when the VP1 activation do- fluence on their DNA-binding characteristics, activation potenmain has been deleted. This suggests that the VP1 domain required tial, or nuclear localization. The dimerization process is regulated
for repression is distinct from the activation function, and that by the availability of their respective partners, their affinity for
VP1 is directly repressing a-amylase gene expression rather than each other and the affinity of the dimer for other components
activating the expression of another protein that in turn represses (such as DNA) – this sensitizes responses to minor fluctuations in
a-amylase gene expression. The repression domain on VP1 that is effector concentration.
responsible for this has yet to be determined. During seed germiThe bZIP and the MADS-domain class of transcription factors
nation, a-amylase production is induced by gibberellic acids, but are well characterized dimerizing proteins in plants. In the case of
VP1 overexpression can override hormone-induced activation dur- the wheat bZIP protein EMBP1, which acts together with VP1 on
ing seed germination.
the EM promoter, three bZIP proteins (osZIPs) that appear to
interact have been identified from rice using an in vitro interacPvALF-mediated gene expression
tion screen29. Gel retardation experiments have revealed that the
The regulation of storage protein expression during seed maturation heterodimer formed by EMBP1 and osZIP-1 shows enhanced
in cotyledons of Phaseolus vulgaris, has some similarities to VP1- binding to the Em-1a element in the EM-promoter, but the heterodimer formed by EMBP1
and osZIP-2a or osZIP-2b prevents binding of EMBP1 to
its cognate promoter binding
ROM1
PvALF
ROM2
site (Fig. 2b). In addition to
SPs
SPs
SPs
osZIP-1, histone H1 has also
been reported to enhance bindTranscription
Repression
Repression
Activation
status
ing of EMBP-1 to its promoter
> activation
> activation
> repression
binding sites in vitro30. This
suggests that the interplay
Days after
between inhibitory and stimu9
11
13
15
17
19 21
23
25
27 29 31
33
35
flowering
latory heterodimers is a reguROM1
Repressor
latory mechanism for EMBP-1
expression
activity, and DNA-binding in
ROM2
general. However, these difActivator
PvAlf
ferent proteins originate from
expression
different species, and further
Storage
b-Phaseolin
research will be needed to conprotein
firm these observations.
expression
The activity of the MybPhytohemagglutinin
like transcription factor C1 is
also regulated by heterodimerFig. 3. The activity of PvALF, a putative bean homologue of maize Viviparous-1 (VP1), is counteracted
ization31. Genetic studies and
by the repressor proteins ROM1 and ROM2, which are expressed at different stages during seed matutransient expression assays reration and germination. The three proteins together regulate the synthesis of the bean storage proteins
vealed that C1 is unable to acti(SPs) b-phaseolin and phytohemagglutinin.
vate expression of its target
genes (these encode enzymes
380
October 1998, Vol. 3, No. 10
trends in plant science
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of the anthocyanin biosynthetic pathway) in the absence of the
helix-loop-helix transcription factor B-Peru32–34. Using the yeast
two-hybrid system, it was found that B-Peru can interact with
the DNA-binding domain of C1 (Ref. 33) and that this interaction enhances the DNA-binding specificity of C1. However,
the extent to which the putative basic helix–loop–helix DNAbinding domain of B-Peru participates in this DNA-binding is
unclear.
Dimerization can also regulate nuclear localization. Evidence
from genetic analysis have suggested that the activities of the homeotic MADS-box proteins APETALA-3 (AP3) and PISTILLATA
(PI), which in Arabidopsis are responsible for the initiation of
petal and pistil formation, are interdependent35. DNA-binding studies in vitro have revealed that AP3 and PI can form a heterodimer.
By transforming AP3- and PI-GUS fusion constructs into an
ap3/pi mutant background, it was possible to demonstrate that the
interaction between AP3 and PI is crucial for the nuclear import
of the transcription factors. In these transgenic plants, GUS activity was detected solely in the cytoplasm when only one of
the two MADS-box proteins was present, whereas reporter gene
activity was localized to the nucleus in plants expressing both
proteins.
Cytosol
(a)
COP1
HY5
Nucleus
CHS1-promoter
(b)
Light signal
?
COP1
Cytosol
Nuclear
export?
?
COP1
Nuclear localization
The import and export of proteins to and from the nucleus is a
highly regulated process36. Entry of transcription factors into the
nucleus can occur by diffusion or it can be a regulated process
responsive to exogenous or endogenous signals. Also, as observed
with AP3/PI, there may be co-transport of two or more factors.
The nuclear import of large proteins is carried out by transporter
proteins that shuttle between the cytoplasm and the nucleus, or by
receptors at the nuclear pores. Import is mediated by nuclear localization signals (NLSs), short peptide sequences rich in arginine
and lysine residues, which have been found in several transcription factors36.
Two NLSs have been identified in the transcription factor
OPAQUE-2 (O2), which regulates the production of zein storage
proteins in the maize endosperm37. One of the NLS domains was
mapped to the basic DNA-binding domain of O2, suggesting that
the DNA-binding domain of this bZIP protein is identical to its
nuclear localization domain. However, using an o2 mutant deficient for DNA binding, it was shown that nuclear localization and
DNA binding are independent functions38. This mutant protein
still entered the nucleus but could no longer activate transcription
of O2 target genes. In tobacco, a protein complex located at the
nuclear pores strongly binds to the NLS of O2 and may be implicated in nuclear import of this transcription factor39.
An example of the control of transcription by dimerization and
nuclear localization is the interaction between COP1 and the bZIP
transcription factor HY5. The pleiotropic Arabidopsis cop1 mutants have the phenotype of light-grown seedlings when grown
in the dark. The COP1 protein has therefore been assigned the role
of a repressor of photomorphogenesis. By contrast, on the basis
of the light-insensitivity of hy5 seedlings, HY5 has been defined
as a positive regulator of photomorphogenesis. Using COP1-GUS
fusions, it has been shown that COP1 protein is localized in the
nucleus in the dark but that it leaves the nucleus after light irradiation40. Genetical evidence had already suggested that COP1 and
HY5 interact directly, and a direct interaction between the two has
now been established in vitro and in vivo41–43. This led to the
development of a model in which COP1 interacts with HY5 in the
dark to keep it in an inactive state. In the light, COP1 releases
HY5 and leaves the nucleus, allowing subsequent activation of
target genes by HY5 (Ref. 42; Fig. 4).
HY5
Dissociation
Nucleus
HY5
CHS1-promoter
Fig. 4. The activity of the Arabidopsis bZIP transcription factor
HY5 is regulated by COP1. (a) In the dark, COP1 is localized to
the nucleus where it binds HY5. (b) After light irradiation, COP1
releases HY5 and leaves the nucleus such that HY5 can then activate its target genes.
Post-translational events
Post-translational modification by protein phosphorylation activates the nuclear import of transcription factors and stimulates or
represses the DNA-binding affinity or the activation potential of
many transcription factors44. Different phosphorylation events are
not mutually exclusive, as phosphorylation events at several sites
could play a part in different aspects of the regulation of transcription factor activity. In plants, the predominant kinase used in
phosphorylation studies is casein kinase II (CKII)45,46. The bZIP
transcription factor GBF1 from Arabidopsis can be phosphorylated
by purified CKII from broccoli46 and by extracts from nuclei of
Arabidopsis45. This modification greatly enhances its DNA-binding
activity.
Phosphorylation is also crucial for regulation of the DNAbinding activity of O2 (Ref. 47). Up to seven distinct phosphorylated forms of O2 can be identified in protein extracts from maize
endosperm separated on two-dimensional protein gels. Only the
unphosphorylated O2 forms bind DNA with high affinity, and the
phosphorylated forms only bind DNA after dephosphorylation by
phosphatase treatment. The phosphorylation pattern of O2 is subject to diurnal changes: hypophosphorylated forms accumulate by
day and hyperphosphorylated forms in the dark. This pattern suggests a temporal regulation of O2 activity ensuring that storage proteins are synthesized at times of high energy supply. The specific
kinases that participate in this process have yet to be identified.
October 1998, Vol. 3, No. 10
381
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A link between a receptor kinase and
transcription has been established for the
plant disease resistance gene, Pto, which
confers resistance to bacterial speck disease in tomato. The Pto serine/threonine
kinase can interact directly not only with
the pathogenic elicitor avrPto, but also with
at least three transcription factors belonging
to the class of ethylene-responsive element
binding proteins (EREBP) from tobacco48.
The kinase activity of Pto and its interaction
with transcription factors suggests a direct
regulation of their activity through phosphorylation (Fig. 5), although their DNAbinding affinity was not influenced by
phosphorylation. Cognate promoter elements for EREBPs have been found in
several pathogenesis-related proteins and
upon infection with the pathogen the expression of some of these genes is upregulated.
Pseudomonas syringae
AvrPto
Secretion
P
?
Pto
Cytoplasm
Hypersensitive
response
Pto
?
?
?
P
P
P
Pti-6
Pti-4
Outlook
Pti-5
We have summarized some interesting
examples of the regulation of transcription
factors. The availability of large mutant collections, in particular from Arabidopsis and
maize, will lead to the isolation of more transcription factor mutants. Mutant analysis
will provide an important tool for the study
of these transcription factors. The inclusion
of genomics approaches in several plant
species combined with classical genetics
and improved in vitro techniques should
allow a more mechanistic understanding of
how plant transcription factors work. In this
respect, the development of reliable and
reproducible in vitro transcription systems
is an important objective49. In conjunction,
these tools will help us to decipher the
plant-specific regulatory networks and so
understand the process from signal transduction to transcriptional regulation.
Nucleus
Nuclear import?
P
PR-box
Fig. 5. The cytoplasmic receptor Pto-kinase interacts with the elicitor of Pseudomonas
syringae, AvrPto, and subsequently phosphorylates several Pti transcription factors belonging
to the class of ethylene-responsive element binding proteins (EREBPs). EREBP-promoter
binding sites have been found in several promoters of pathogenicity-related proteins. The role
of phosphorylation in regulating the activity of these transcription factors remains unclear.
Abbreviation: P, phosphate.
We thank Roderick Card for critical reading of the manuscript.
Our work is supported by the Ministry of Agriculture, Fisheries
and Food (MAFF).
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Claus Schwechheimer and Michael Bevan* are at the
Molecular Genetics Dept, John Innes Centre, Norwich, Norfolk,
UK NR4 7UH; Claus Schwechheimer is presently at the
Dept for Molecular, Cellular and Developmental Biology,
Yale University, New Haven, CT 06520-8140, USA.
*Author for correspondence (tel +44 1603 452571;
fax +44 1603 505725; e-mail bevan@bbsrc.ac.uk).
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