Transcription factor families in Arabidopsis: major progress and
outstanding issues for future research
Commentary
Li-Jia Qu and Yu-Xian Zhu
Transcription factors (TFs) are a group of proteins that control
cellular processes by regulating the expression of downstream
target genes. Recent progress has been made in the cloning
and characterization of Arabidopsis TFs on the genome scale,
especially on the cloning of open reading frames (ORFs),
sequence analysis and the expression profiling of different TF
families. Huge difference in numbers of subfamily members
were found for Arabidopsis MYB, C2H2 (Zn), C3H-type 1 (Zn),
C3H-type 2 (Zn) TFs by independent research groups, mainly
because of differences in bioinformatic search stringency.
However, the Arabidopsis and rice genomes contain very
different numbers of TFs in the WRKY, NAC, bZIP, MADS,
ALFIN-like, GRAS and C2C2 (Zn)-dof families, indicating a
possible divergence of biological functions from dicots to
monocots. TFs have also been found to play key roles in the
biosynthesis and signaling of plant hormones, in cell growth
and differentiation, and in photomorphogenesis.
Addresses
The National Laboratory of Protein Engineering and Plant Genetic
Engineering, College of Life Sciences, Peking University, Beijing
100871, China
frontier and identify several potential areas of future
research.
Major progress in recent years
ORF cloning and sequence analysis of Arabidopsis
TFs
Using InterPro and GenBank accessions as family identifier, it was initially estimated that the Arabidopsis genome contains 1533 TF genes [1]. Subsequent estimates of
Arabidopsis TF gene numbers by two independent groups
varies from 1510 to 1581, mainly because of differences in
bioinformatic search stringency and definitions of unclassified TFs ([2,3,4]; Table 1). A concerted large-scale
cloning effort cloned 1282 ORFs encoding Arabidopsis
TFs [2], and the expression profiles of over 1400 TFs
were analyzed using real-time quantitative reverse transcriptase (qRT)-PCR technology [5]. These ORF clones
and expression profiles have enriched our understanding
of the complexity of Arabidopsis TFs and their evolution.
The rice genome has been estimated to contain 1611 TF
genes [3] and a large number of full-length TF cDNAs
from rice were obtained as the result of a genome-wide
cloning project [6].
Current Opinion in Plant Biology 2006, 9:544–549
Available online 31st July 2006
1369-5266/$ – see front matter
# 2006 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2006.07.005
Introduction
By definition, transcription factors (TFs) implement their
functions by binding directly to the promoters of target
genes in a sequence-specific manner to either activate or
repress the transcription of downstream target genes.
With the completion of the Arabidopsis and rice genome
sequences, it became possible not only to study the
function of TFs on a genome-wide scale but also to
compare the structural and functional similarities and
differences between the TFs of monocots and dicots
plants. The necessity for genomics approaches becomes
clear as only about 10% of the TFs have been molecularly
or genetically characterized. Much important and exciting
progress has been made during the past a few years,
including the genome-wide cloning and characterization
of Arabidopsis TFs, real-time expression profiling, and
bioinformatic analysis of TFs in both Arabidopsis and
rice. We briefly summarize the recent progresses on this
Current Opinion in Plant Biology 2006, 9:544–549
Expression profiling of individual TF families
The Arabidopsis genome contains several large TF
families that include more than 100 members, such as
MYB, MADS, basic helix-loop-helix (bHLH) and APETALA2 (AP2)/ETHYLENE RESPONSE ELEMENT
BINDING PROTEIN (EREBP) [7–10]. Several of these
large TF families have been chosen for expression profiling analysis in recent years.
MYB superfamily
The MYB superfamily is the largest TF family known in
plants, consisting of approximately one-eighth of the TFs
in Arabidopsis. It is divided into three families, the R2R3,
R1R2R3 and MYB-related families, on the basis of the
number and position of the MYB repeats. Different studies
have predicted the total number MYB TFs to be 189 [3],
190 [1] and 258 [2]. Recently, 163 of the more reliable
Arabidopsis MYBs were cloned and studied systematically
[11]. Compared with mammalian MYB genes, these
plant MYB genes are more complex and diverse, and only
a few of them exhibited constitutive and ubiquitous
expression in Arabidopsis [2,12]. MYB TFs were typically
involved in a multitude of physiological processes, and
accordingly, they were induced by one or more developmental signals or by environmental stimuli [11].
www.sciencedirect.com
Transcription factor families in Arabidopsis Qu and Zhu 545
Table 1
Predicted number of genes in different TF families in the Arabidopsis genome.
TF families
InterPro or GenBank
Accession Access
ABI3/VP1
ALFIN-like
AP2/EREBP
ARF
ARID
AS2
AUX/IAA
bHLH
bZIP
C2C2 (Zn)-co-like
C2C2 (Zn)-dof
C2C2 (Zn)-gata
C2C2 (Zn)-yabby
C2H2 (Zn)
C3H-type1 (Zn)
C3H-type (Zn)
CCAAT
CAA48241
AAA20093
IPR001471
AAC49751
IPR001606
CPP (Zn)
E2F/DP
EIL
GARP
GRAS
HB
HMG-box
HSF
JUMONJI
LFY
MADS
MYB
NAC
Nin-like
PCG
SBP
TCP
Trihelix
TUB
WRKY (Zn)
Others
Totals
AAC39440
IPR001092
IPR001871
A56133
CAA66600
IPR000679
AAD30526
IPR000822
IPR000232
CAA65242
26771/P13434/
Q02516/AAB513
CAA09028
O00716/Q64163
AAC49750
AAD55941/BAA74528
AAB06318
IPR001356
IPR000910
IPR000232
T30254
AAA32826
IPR002100
IPR001005/IPR000818
BAB10725
CAB61243
CAB56581
AAC26786
S39484
IPR000007
S72443
Riechmann
et al. [1]
a
Gong
et al. [2]
Xiong
et al. [3]
14
7
144
23
4
0
26
139
81
33
37
28
6
105
17
16
36
17 (4)
7 (7)
118 (142)
23 (11)
5 (3)
0 (30)
28 (26)
108 (81)
82 (54)
32 (24)
35 (32)
22 (33)
5 (3)
152 (92)
46 (32)
26 (10)
36 (34)
6
7
146
23
3
30
26
164
76
87
8
8
6
56
32
89
10
26
9
1
82
190
109
15
4
16
25
28
11
72
20
1533
8 (5)
8 (1)
6 (5)
53 (24)
32 (26)
83 (56)
13 (10)
16 (12)
8 (4)
1 (0)
91 (70)
258 (244)
106 (93)
14 (2)
4 (2)
16 (14)
21 (19)
21 (1)
9 (7)
70 (54)
20 (16)
1581 (1282)
8
8
6
53
32
90
10
23
4
0
106
189
105
14
2
16
23
38
11
72
85
1510
66
11
9
36
Guo
et al. [4]
13
7
146
23
7
42
29
162
75
31
36
29
5
130
33
b
RIKEN
database
c
Arabidopsis
GRIS
11
7
149
24
7
0
0
161
73
30
36
30
6
211
165
36
112
60
145
119
6
0
49
157
75
51
33
37
5
177
38
10
37
8
8
6
55
32
94
10
24
13
3
107
203
113
14
4
16
24
28
11
72
178
1827
11
8
6
57
32
101
15
27
15
3
106
238
106
14
3
17
24
31
11
72
400
1968
8
8
6
56
33
91
0
21
5
0
109
133
96
9
0
16
26
29
10
72
105
1778
35
a
Numbers of TFs predicted/number of TFs whose ORFs have been cloned.
Number of TFs reported in RIKEN Arabidopsis Transcription Factor database (http://rarge.gsc.riken.jp/rartf/).
c
Number of TFs predicted by Arabidopsis Gene Regulatory Information Server at Ohio State University (http://arabidopsis.med.ohio-state.edu/
AtTFDB/).
b
bHLH family
A total of 162 AtBHLH genes have been identified, making
it the second largest TF family in the Arabidopsis genome
[10]. Members of this TF family are known to be involved
in controlling cell proliferation and in the development of
specific cell lineages [13]. Their mechanism for regulating
transcription often involves the formation of homo- or
hetero-dimeric configurations that can bind specifically
to the G-box DNA sequence motif CACGTG [14].
successfully amplified and cloned from various types of
Arabidopsis tissues or organs or after different treatments;
hence, the AP2/EREBP family is the most completely
cloned Arabidopsis TF family to date [15]. Although
many AP2/EREBP members are expressed in a tissuespecific manner and/or expressed differentially in
response to different phytohormones [15], it is believed
that this gene family are mainly involved in responses to
different stresses: drought, freezing and pathogen invasion [16].
AP2/EREBP family
The Arabidopsis genome contains 147 members of the
AP2/EREBP family, which are divided into three subgroups [15]. A total of 145 AP2/EREBP TFs have been
www.sciencedirect.com
MADS family
The Arabidopsis MADS family is composed of about
100 members. Most Arabidopsis MADS TFs are involved
Current Opinion in Plant Biology 2006, 9:544–549
546 Commentary
in the regulation of flower-related physiological and
developmental processes [17]. Members of this superfamily were predominantly detected in flowers and fruits
[12].
indicator [23]. Also, quite a few TFs, such as ARFs, PIF1
and PIF3, are now known to be regulated mainly by a
proteosome-mediated protein degradation and turnover
pathway [24,25,26].
WRKY family
Evolution of TFs
There are more than 70 WRKY TFs in Arabidopsis. They
are involved in salicylic acid signaling and in responses to
pathogens [18]. WRKY genes were often detected preferentially in leaves with family members sharing concerted expression patterns [12].
There are two contradictory hypotheses regarding the
evolution of the MYB superfamily. The first hypothesis
states that R2R3 TFs are relatively new and probably
evolved from R1R2R3 members by losing the R1 domain.
The second hypothesis suggests that R2R3 members
could be ancestors of R1R2R3 members, which evolved
by gaining the extra R1 domain. A recent publication by
Chen et al. [11] found that the Arabidopsis MYB superfamily underwent a rapid expansion after divergence with
monocots but before its divergence from other dicots,
suggesting that MYB-related members were possibly
more ancient than R2R3 members.
Comparative genomic studies of TFs in
Arabidopsis and rice
In most cases, the TF family counterparts in the Arabidopsis and rice genomes are of similar sizes. There are,
however, a few exceptions in which the numbers of
members within a family differ substantially between
Arabidopsis and rice (Table 2). Phylogenetic analyses
showed that nearly half of the TF genes from these
two plants form clear orthologous pairs or groups, suggesting that they were derived from common ancestral genes.
Meanwhile, the duplication of large intragenomic segments accounted for about 60% of the TF gene duplication events in rice [3].
Regulation of TF expression
Among 49 predicted targets of 14 Arabidopsis microRNAs,
34 were found to be TFs [19]. For example, miR160directed regulation of AUXIN RESPONSE FACTOR 17
(ARF17) is essential for plant development, and miR166mediated cleavage of Arabidopsis thaliana HOMEOBOX15
(ATHB15) mRNA is a key step in the regulation of
vascular development [20,21]. The cleavage of NAC1
mRNA, governed by miR164, is involved in the downregulation of auxin signals for Arabidopsis lateral root
development [22]. The mechanism for microRNAmediated gene expression was found to be conserved
among distant lineages, such as gymnosperms and flowering plants, when the target site of miR172 was used an
Table 2
TF families show significantly different member numbers in the
Arabidopsis and the rice genomes.
MYB
WRKY
NAC
bZIP
MADS
ALFIN-like
GRAS
C2C2 (Zn)-dof
Arabidopsis
Rice
189
70
106
82
107
7
32
35
182
109
149
94
77
10
57
30
Most of the predicted Arabidopsis TFs, except that of MYB [12] and
MADS [17], were reported in [2], and all rice TFs were reported in
[3].
Current Opinion in Plant Biology 2006, 9:544–549
Similar studies showed that the AP2 subfamily of AP2/
EREBP TFs diverged into the AP2 and AINTEGUMENTA (ANT) groups before the last common ancestor
of all land plants but after Chlamydomonas reinhardtii
diverged from the land-plant lineage [27]. Surprisingly,
it has been suggested that the AP2/EREBP family originated from HNH-AP2 endonucleases of bacteria or
viruses [27]. The WRKY family was originally regarded
as a plant-specific TF family until several WRKY proteins
were identified in non-plant eukaryotes, including Giardialamblia and the slime mold Dictyostelium discoideum
[28]. This suggested that WRKY genes might have an
early origin in low eukaryotes. It is likely that the loss of
the WRKY genes from most non-plant eukaryotes happened before the divergence of fungi and animals but
after that of mycetozoa and fungi/animals.
TFs in brassinosteroid and abscisic acid
signaling
Brassinosteroid (BR) is important in regulating plant
growth and development, and the BR signaling pathway
is well defined in Arabidopsis. Two novel TFs, BRASSINAZOLE-RESISTANT 1 (BZR1) and its closely related
homolog Bri1-EMS-Suppressor 1 (BES1), are positive
regulators of the BR signaling pathway. In the presence
of BR, both BZR1 and BES1 accumulate in the nucleus
and promote cellular responses by regulating the activities of BR-responsive promoters [29]. Paradoxically,
BZR1 acts as a transcriptional repressor of BR-biosynthetic genes such as CONSTITUTIVE PHOTOMORPHOGENESIS AND DWARFISM (CPD), whereas BES1, in
combination with other transcription factors such as
BIM1, serves as a transcriptional activator of the BRresponsive gene SAUR-AC1 (Arabidopsis Columbia small
auxin upregulated RNA gene 1) [30,31]. These results
suggest that BZR1 and BES1 exert different regulatory
effects on different subsets of BR target genes, possibly
through interactions with different nuclear components.
www.sciencedirect.com
Transcription factor families in Arabidopsis Qu and Zhu 547
Recently, the first abscisic acid (ABA) receptor, FLOWERING TIME CONTROL LOCUS A (FCA), was
identified. FCA is a soluble protein that regulates the
transcription of a MADS-domain transcription factor,
FLOWERING LOCUS C (FLC), through RNA processing. Binding of ABA to FCA exerts direct control on the
FCA-mediated processing of precursor FLC mRNA
[32].
TFs in cell growth and differentiation
Many TFs are known to play key roles in various regulatory networks that govern the growth and differentiation of a plant cell. In Arabidopsis, a protein complex
composed of the bHLH TFs GLABRA3 (GL3) and
ENHANCER OF GLABRA3 (EGL3) and different
MYBs that are associated with a WD40-repeat protein
(TRANSPARENT TESTA GLABRA1 [TTG1]) controls epidermal cell identity. This complex differentiates
root hairs, stomata and trichomes by controlling the
expression of a downstream regulator, GL2 [33]. Three
MYB genes, WEREWOLF (WER), GL1 and AtMYB23, are
involved in these complexes [7,8]. A protein complex that
contains WER, an R2R3 MYB, triggered root-hair cell
fate, whereas a complex containing another R2R3, GL1,
controls trichome cell fate in the leaf. When the singledomain MYB proteins (CAPRICE [CPC], TRIPTYCHON [TRY] and ENHANCER OF TRY AND
CPC1 [ETC1]) were present in these complexes instead
of the R2R3s, the opposite cell-fate determinations were
observed [33]. AtMYB23 is functionally equivalent to
GL1 during trichome initiation but plays a different role
during trichome branching [34].
TFs in photomorphogenesis
TFs that regulate the photomorphogenic development
of plants have been extensively studied during the
past decade. PHYTOCHROME-INTERACTING
FACTOR3 (PIF3), an important TF from the bHLH
family, interacts directly with the photoreceptors Phytochrome A and B [35], and targets the phytochrome signals
directly to the promoters of light-inducible genes in
Arabidopsis [36]. CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1), a repressor of photomorphogenesis, is
downregulated upon receiving the light signal. Four TFs,
LONG HYPOCOTYL 5 (HY5) and its homologs LONG
HYPOCOTYL5-LIKE (HYH), LONG HYPOCOTYL
IN FAR-RED 1 (HFR1) and LONG AFTER FARRED LIGHT1 (LAF1), are direct targets of COP1.
The molecular interaction between COP1 and HY5, a
basic leucine zipper (bZIP) transcription factor that binds
directly to the promoters of light-responsive genes,
defines a regulatory switch for the light control of Arabidopsis development [37]. Both HFR1 (a bHLH TF) and
LAF1 (an R2R3-type MYB TF) are involved in phytochrome A-mediated far-red light signaling, whereas
HFR1 is also required for Cryptochrome 1-mediated
blue-light signaling [38,39].
www.sciencedirect.com
Outstanding issues for future research
Genome-wide analysis of DNA-binding target
sequences for different TF families
The identification of the downstream target genes of a
TF is an important part of its functional characterization.
With more and more ORFs encoding most TFs and
bioinformatic analysis software now available, we predict
a breakthrough using protein microarray techniques to
find the direct downstream target genes of a specified TF
family at the genome scale. Results obtained from work of
this type will undoubtedly add to our portfolio of candidate regulatory sequences that are important for the life of
a given plant cell.
TFs for metabolic engineering
Because of their ability to control both multiple pathway
steps and cellular processes that are necessary for metabolite accumulation, TFs were thought to offer much
promise for manipulating metabolic pathways in higher
plants [40,41]. However, a breakthrough in finding readily
controllable TFs that can regulate a given metabolic
pathway is yet to come.
Coordinated regulations
Some signaling pathways are regulated through the coordination of TFs from a single family, such as BZR1 and
BES1 [29,30]. Other signaling networks rely on the
coordination of TFs from different families, which function through the formation of regulatory protein complexes. For instance, a regulatory bHLH–MYB complex
is essential for Arabidopsis root-hair formation [33]. As
more protein complexes are purified in the future, we
anticipate that many more examples of coordination
among different members of the same TF subfamily or
among members of different subfamilies will be revealed.
Crystalization and structural determination
The three-dimensional structure of the WRKY domains
of Arabidopsis, WRKY4 and WRKY1, have been determined by NMR. Within this structure, the WRKYGQK
region was proposed to correspond directly to the DNAbinding site [42]. Recently, scientists from US and several
other countries have initiated a project aiming at the
high-throughput structural determination of Arabidopsis
proteins (http://mips.gsf.de/projects/structgenomics/). We
believe that TFs might be good candidates for large-scale
crystallization because they are soluble. In the future,
however, researchers might want to obtain the structures
of important TFs that co-crystalize with a cis-element on
the promoter of their target gene.
Concluding remarks
TFs play multi-faceted and pivotal roles in controlling the
biological processes of all living organisms. Since the
identification of the first TF, TF1, from a bacteriophage
SPO1 in 1972 [43], a total of 215 918 publications (sorry to
those authors that were not referred to in this commentary
Current Opinion in Plant Biology 2006, 9:544–549
548 Commentary
because of space confines!) were reported when searching
PubMed using ‘transcription factor’ as the sole search
term. The full complement of Arabidopsis TFs, together
with studies illustrating some of the challenges facing
their functional characterization, form the basic framework for future analyses of transcriptional regulation in
plants. The old question of ‘how TFs might be regulated’
is being answered or, at least, there are more clues
available to answer it now than ever before. With the
implementation of DNA and protein microarrays, genome-wide studies of TF expression and interaction might
soon be available to pin down key members in this
complex gene family, and to allow researchers to decipher
mechanisms that allow plant cells to cope with developmental, environmental and hormonal stimuli.
Acknowledgements
The authors would like to thank Xing Wang Deng and Peter H Quail for
critical reading and comments on the manuscript. We are grateful to the
Chinese National Natural Science Foundation for a grant (#30221120261)
that allowed us to carry out the work on genome-wide cloning and
characterization of Arabidopsis TFs.
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Transcription factor families in Arabidopsis Qu and Zhu 549
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