- Email: [email protected]
The Dof family of plant transcription factors
Review
TRENDS in Plant Science Vol.7 No.12 December 2002
555
The Dof family of plant transcription factors Shuichi Yanagisawa Dof proteins are members of a major family of plant transcription factors. The proteins have similar DNA-binding properties because of the highly conserved DNA-binding domain. However, recent studies are disclosing their diverse roles in gene expression when associated with plant-specific phenomena including light, phytohormone and defense responses, seed development and germination. Based on the structural diversity indicated by the complete catalog of Arabidopsis Dof proteins, Dof genes appear to have evolved multiple times, preceding and paralleling the diversification of angiosperms. Such gene multiplication might have led to the functional diversification of Dof proteins proceeding differently in distinct plant species.
Plant gene expression involves classes of transcription factors that have specifically evolved to regulate plant-specific genes and/or to mediate a variety of plant-specific signals. The Dof family is a typical example of such transcription factors. Many Dof proteins have already been discovered in both monocots and dicots. Currently, we know only a fraction of their biological roles. However, it is evident that Dof proteins play vital roles in plant gene expression. In the complete Arabidopsis genome sequence, 37 putative Dof genes are discernible [1]. The presence of so many Dof genes suggests that multiplication of Dof genes might be linked with the formation of sophisticated transcriptional control in higher plants. What are Dof proteins?
Shuichi Yanagisawa Dept of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Komaba, Meguro, Tokyo 153-8902, Japan. e-mail: csyanag@ mail.ecc.u-tokyo.ac.jp
The first Dof protein (ZmDof1) was found as a DNA-binding protein of maize [2]. The DNA-binding domain in ZmDof1 includes a C2C2-type zinc-fingerlike motif, although the amino acid sequence of this domain is largely different from those of other zinc-finger domains (Fig. 1a). The divalent metal chelators, 1, 10-o-phenanthroline and EDTA, inhibited the DNA-binding of ZmDof1, and mutations on cysteine residues that had been expected to coordinate to a zinc ion also prevented the DNA-binding activity [3]. This suggested that the DNA binding domain contained a variant of zinc fingers, and it was therefore referred to as the Dof (DNA-binding with one finger) domain [3,4]. During recent years, >20 cDNAs encoding a Dof domain have been isolated from maize and other plant species, including Arabidopsis, tobacco, pumpkin, potato, barley, wheat and rice [3,5–13]. Dof proteins, which are typically composed of 200–400 amino acids, are now defined as DNA-binding proteins that have a highly conserved Dof domain. In spite of intensive homology in the Dof domain, the rest of the amino http://plants.trends.com
acid sequences in the proteins are divergent, coinciding with their expected diverse functions. The inhibitory effects of the metal chelators and the absolute requirement of cysteine residues for putative zinc coordination were repeatedly demonstrated in studies of the DNA interaction of several Dof proteins [6,8,11,14]. Furthermore, two aromatic amino acid residues (Tyr and Trp) conserved among all Dof domains are necessary for sufficient DNA-binding of a pumpkin Dof protein [15]. However, whether the Dof domain includes a zinc finger has still to be determined. By contrast, the assumption that Dof proteins are unique to plants has been verified in a recent comparative study using the complete genome information from Arabidopsis, Drosophila, Caenorhabditis elegans and yeast [1]. Dof proteins as transcription factors
Co-transfection experiments with expression vectors for Dof proteins and their putative target promoters fused to reporter genes have provided direct evidence that Dof proteins function as transcriptional activators or repressors through direct interaction with DNA. For instance, ZmDof1 enhanced reporter gene expression depending on the binding sites in the promoters, whereas co-expression of another maize protein (ZmDof2) suppressed the positive effect of ZmDof1 in maize mesophyll protoplasts [16]. A barley Dof protein (BPBF) also activated the transcription from a putative target promoter in particle-bombarded endosperm, but BPBF with mutations on the cysteine residues for putative zinc coordination did not [9]. In accordance with its activity as a transcription factor, nuclear localization of ZmDof1 was also shown [16,17]. Interestingly, the transcriptional activation domain of ZmDof1 can function not only in plant cells but also in animal cells and in yeast [17]. Like aromatic residues in the transcriptional activation domains of animal factors GATA-4 and VP16, a tryptophan residue in the transcriptional activation domain of ZmDof1 is of particular importance for the function [17]. In addition, the C-terminal part of BPBF also functions as a transcriptional activation domain in yeast [18]. Therefore, although Dof proteins are unique to plants, some Dof proteins might regulate transcription through a mechanism evolutionarily conserved among all eukaryotes.
1360-1385/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S1360-1385(02)02362-2
Review
556
TRENDS in Plant Science Vol.7 No.12 December 2002
Table 1. A variety of putative roles for Dof proteins in plants
(a) CPRCASRDTKFCYYNNYNTSQPRHFCKGCRRYWTKGGTLRNVPVGGGTRK
Activation
Dof 1
(b)
100
NLS
200
238 amino acids
+1
Arabidopsis GST6 promoter
–450 TGACGACCTCCTCTACACTTTT
OBF
OBP1
Refs
ZmDof1 PBF BPBF WPBF OBP1 DAG1 DAG2 NtBBF1 AOBP OsDof3 StDof1
Maize Maize Barley Wheat Arabidopsis Arabidopsis Arabidopsis Tobacco Pumpkin Rice Potato
Light response Endosperm specificity Orthologs of PBF Orthologs of PBF Defense response Seed germination Seed germination Auxin response Auxin response Gibberellin response Guard cell specificity
[16,21] [7] [9] [9] [5,14] [31] [13] [6,32] [8] [11] [12]
Dual function of the Dof domain
The strong similarity among Dof DNA-binding domains suggested that all Dof proteins display similar DNA-binding specificity. Indeed, an AAAG sequence or its reversibly orientated sequence, CTTT, is always found in the binding sequences of individual Dof proteins [2,5–7,9–12,14,16,21], except a pumpkin Dof protein (AOBP) that recognizes an AGTA motif [8]. Furthermore, binding- site selection experiments with four maize Dof proteins established an (A/T)AAAG sequence as the recognition core [22]. A different preference of each protein on the sequence flanking the core motif was also shown, but it affected the DNA recognition only to a limited extent [22]. Similar to the many cases of other transcription factors, precise selection of target promoters by each Dof protein in vivo might require other factors in addition to the DNA sequence. Dual activity of the Dof domain might be a clue to understanding why each Dof protein can act on correct target promoters in vivo. Like other zinc fingers [23], the Dof domain is known to be a bi-functional domain that mediates not only DNA-binding but also protein–protein interactions. The first protein–protein interaction was reported by Bei Zhang et al. [5]. An Arabidopsis Dof protein (OBP1), which was isolated as a protein specifically interacting with basic leucine zipper (bZIP) proteins (OBF4 and 5), promoted the binding of the bZIP proteins to DNA through its Dof domain [5,10]. An OBP1-binding site in close vicinity to an OBF-binding site was indeed found on a target promoter, Arabidopsis GST6 promoter (Fig. 1b) [14]. Another example of the Dof–bZIP interaction can be seen in the interaction of PBF (a maize endospermspecific Dof protein) with O2 (a maize bZIP protein involved in endosperm-specific gene expression) [7]. The physiological significance of the PBF–O2 interaction is shown by the requirement of the PBF-binding site for O2-dependent activation [24,25] and conservation of the set of PBF- and O2-binding sites in many promoters of cereal storage-protein genes [26,27]. Furthermore, another target promoter of O2 in the endosperm (the maize cyPPDK promoter)
+1
TGTCACATGTGTAAAGGTGAAGAGATCATGCATGTCATTCCACGTAG
O2
O2
TRENDS in Plant Science
Fig. 1. (a) Scheme of ZmDof 1 as an example of the Dof protein domain structure. The Dof domain, a nuclear localization signal (NLS) and the transcriptional activation domain are indicated in yellow, pink and purple, respectively. A serine-stretch is indicated in green. The cysteine residues for putative coordination of zinc are shown in red letters in the Dof domain amino acid sequence. (b) Examples of Dof-binding sites in plant promoters. The binding sites for Dof proteins and bZIP proteins are indicated in red and blue, respectively. Dof–bZIP interactions and transcription start sites are indicated by bi-directional arrows and bent arrows, respectively.
Domain structure
Transcription factors sometimes contain multiple DNA-binding domains. For example, some plant MYB proteins have a single MYB DNA-binding domain, but others contain imperfect repeats of the MYB domain [19]. In addition, single MYB-domain proteins and two- or three-repeat MYB proteins have been suggested to bind DNA in different ways [19]. Similarly, plant-specific WRKY transcription factors possess different numbers of WRKY DNA-binding domains, which allows the proteins to be classified into subgroups [20]. However, in the case of Dof proteins, only a single copy of the Dof domain can always be found in their N-terminal regions. By contrast, the minimal transcriptional activation domain of ZmDof1 has been mapped in 44 amino acid residues of the C-termini [17]. The C-terminal regions of other Dof proteins (Arabidopsis OBP1, 2 and 3, and barley BPBF) also include transcriptional activation domains [10,18]. Taken together, Dof proteins usually appear to consist of two major domains: an N-terminal conserved DNA-binding domain and a C-terminal domain for transcriptional regulation (Fig. 1a). Serine-stretches that are frequently located immediately downstream of the Dof domains might be the molecular hinges linking the two domains. http://plants.trends.com
Putative role
OBP1 OBP1
–250
PBF
Species
AAAAGGAAAG
Maize 22-kDa zein promoter
O2
Dof protein
Review
TRENDS in Plant Science Vol.7 No.12 December 2002
Table 2. List of Arabidopsis Dof genes a
b
c
Dof gene
Gene code
Clone
EST
Synonymous
AtDof1.1 AtDof1.2 AtDof1.3 AtDof1.4 AtDof1.5 d AtDof1.6 AtDof1.7 AtDof1.8 AtDof1.9 AtDof1.10 AtDof2.1 AtDof2.2 AtDof2.3 AtDof2.4 AtDof2.5 AtDof3.1 AtDof3.2 AtDof3.3 AtDof3.4 AtDof3.5 AtDof3.6 AtDof3.7 AtDof4.1 AtDof4.2 AtDof4.3 AtDof4.4 AtDof4.5 AtDof4.6 AtDof4.7 AtDof5.1 AtDof5.2 AtDof5.3 AtDof5.4 AtDof5.5 AtDof5.6 AtDof5.7 AtDof5.8
At1 g07640 At1 g21340 At1 g26790 At1 g28310 At1 g29160 At1 g47650 At1 g51700 At1 g64620 At1 g65935 At1 g69570 At2 g28510 At2 g28810 At2 g34140 At2 g37590 At2 g46590 At3 g21270 At3 g45610 At3 g47500 At3 g50410 At3 g52440 At3 g55370 At3 g61850 At4 g00940 At4 g21030 At4 g21040 At4 g21050 At4 g21080 At4 g24060 At4 g38000 At5 g02460 At5 g39660 At5 g60200 At5 g60850 At5 g62430 At5 g62940 At5 g65590 At5 g66940
F24B9 F24J8 T24P13 F3H9 F28N24 F16N3 F19C24 F1N19 F12P19 F10D13 T17D12 F8N16 T14G11 F13M22 F13A10 MXL8 F9K21 F1P2 F11C1 F22O6 T22E16 F21F14 T18A10 T13K14 T13K14 T13K14 F7J7 T19F6 F20D10 T22P11 MIJ24 F15L12 MAE1 K19B1 MQB2 K21L13 K8A10
AV540721 – – – – – BE038318 T14116 – AV564595 – AI999028 AA395802 – AI993066 BE038318 AV442796 AV559509 AW004398 – T22381 AV543166 H77029 – – – – AV537390 AV531601 AV560727 T88559 N38019 AI995889 AV519437 – T43764 –
OBP2 – – – – – ADOF1 – – – – – – – DAG2 ADOF2 – – OBP1 – OBP3 DAG1 and BBFa – – – – – – – – – – OBP4 – – – –
a
Nomenclature giving first the chromosome numbers and then orders on the chromosome. GenBank accession numbers. Even if multiple ESTs were found, only one is shown. '–' indicates no GenBank accession number. c The original names used in publication or for registration in a database. '–' indicates no other name. d The open reading frame (ORF) for AtDof1.6 was estimated using a Met codon that was different from the putative translational start Met codon for the ORF, At1 g47650. b
is also a target of ZmDof1 in leaf mesophyll cells, although no Dof–bZIP interaction associated with the activity of the cyPPDK promoter has been identified [21]. These examples reveal an interesting character of the Dof domains, but it still uncertain whether every Dof protein interacts with a bZIP protein. The Dof domain also mediates other types of protein–protein interactions. The Dof domain showed a specific affinity to distinct Dof domains, although the biochemical and biological meanings of this affinity have not been clarified yet [28]. In addition, Dof domains interacted with maize HMG (chromatin-associated high mobility group) proteins and different HMG proteins enhanced DNA-binding of Dof proteins to different extents [28,29]. http://plants.trends.com
557
Combinatorial regulation by distinct classes of transcription factors is a persuasive explanation for seeming discrepancies between DNA-binding in vitro and the action in vivo of transcription factors [30]. It is likely that the dual function of the Dof domain contributes to correct choice and/or selective activation or repression of target genes in vivo. However, the exact meanings of these protein–protein interactions in transcriptional control still remain to be evaluated in vivo. Also, it is still unknown what determines the specificity of these interactions in spite of the conserved amino acid sequence within the Dof domain. In a recent report, the Dof–MYB interaction was mediated through the C-terminal of BPBF but not through the Dof domain [18]. Analogous to the case of O2 protein, both the MYB-binding and the Dof binding sites were necessary for the MYB protein to activate the transcription from a target promoter [18]. Divergent roles of Dof proteins
Divergent physiological roles of Dof proteins have been suggested to date (Table 1). The suggested roles do not have anything in common apart from all being linked to plant-specific gene expression. Maize Dof1 was suggested to be a regulator for the light-responsive expression of multiple genes, including the C4 photosynthetic phosphoenolpyruvate carboxylase gene [16,21]. Maize PBF and its orthologs of wheat and barley appear to be transcription factors controlling endosperm-specific expression of storage proteins [7,9]. Arabidopsis OBP1 might regulate defense gene expression in response to salicylic acid and oxidative stress signals [5,14]. Arabidopsis DAG1 and DAG2 have been shown to act on a maternal switch controlling seed germination by isolating mutants with a T-DNA insertion in their respective genes [13,31]. Dof proteins are probably also involved in phytohormone-regulated expression. A tobacco Dof protein, NtBBF1, is a candidate for the activator of auxin-inducible expression of a plant oncogene rolB in apical meristems and vascular tissues [6,32]. Participation of Dof proteins in gene silencing has also been suggested from the binding of a pumpkin Dof protein (AOBP) to the silencer region of the auxin-inducible ascorbate-oxidase gene promoter [8]. Some gibberellin (GA) responses might involve Dof proteins as well. A rice Dof protein, OsDof3, might be a mediator for GA signaling during germination [11]. Recently, another function of Dof proteins was suggested in the regulation of guard cell-specific gene expression in potato [12]. Although every role has not been confirmed conclusively, Dof proteins apparently function in the regulation of various processes. Transcriptional and post-transcriptional regulations matching the suggested physiological functions have also been reported on expression of several Dof proteins. For example, expression of PBF gene is strictly restricted to certain developmental stages in the endosperm [7,9], and
558
Review
TRENDS in Plant Science Vol.7 No.12 December 2002
AtDof4.2 AtDof4.4 AtDof4.3 AtDof4.5
DNEMN--VMPPP--RV Dof DNQVNGLKRPPPS-RV Dof DNQVNDVKPPPPPPRV Dof DNQVNDVKPPPPPPRV Dof
OsDof5 AtDof3.3 AtDof5.5 AtDof5.2 AtDof1.5 AtDof2.3 AtDof1.3 AtDof1.10 AOBP
QPSVAQMVSVGIQPGSHKPF QPSVARMVSVETQRGNNQPF
KTLKKPTKILP Dof NK KTLKKPTKILP Dof NK LKKPDKILP Dof NK
LSANPAALSR
DLTAEKRPDKIIP Dof SK DLTAEKRPDKIIA Dof SK EKTTELKKPDKILP Dof NK EKSTALKKPDKLIP Dof NK LKKPDKILP Dof NK
LQANPAAMAR LQANPAAMSR LQANPAALSR
Dof RSR Dof SRR PEQSLR Dof HKR PPELALR Dof NKR
AtDof3.7 AtDof4.1 NtBBF1 NtBBF2a OsDof1 OsDof2
PTERKPRP-QKEQAIN HIERKIRPHQKDQALN STERRARP-QKEKALN GTERRARP-QKEKALN
AtDof1.8
AtDof3.4 AtDof5.8 AtDof1.6 AtDof1.7 AtDof3.1 AtDof4.7 AtDof5.7 AtDof1.4 AtDof2.4 AtDof5.1
MPSEFSESR MPSEPNQTR MQDLTSAA MQDP--AA
Dof Dof Dof Dof
IDLAAVFA LRTTPEP LRTTPEP
IDLALVYA MELGLAYA IDLSLAFA
LPDLNP
QDLNLGFS KDLNLAFS QDLNLLSF
LPDLNP LPDLNP
KDLNLLSF NDLSLSFS
Group III
IDLNLAFA
NKR SKK NKR NKR
HDLNLAFN QDLNLGFS QDLNLAFP QDLNLAFP
QEQLP Dof QEQLS Dof AEPLP Dof QEQLK Dof QEQLK Dof QPVLK Dof
PLQTTPVLFPQ PLQATPVLFPQ
QQNLK Dof QPQLK Dof
SSIETLSCLNQDLHWRLQQQR
Group IV
SSIESLSSFNQDLHQKLQQQR
AtDof3.6 AtDof1.1
RARQA-NVALPEAALK Dof RNRRTKS RARLA-NIPLPETALK Dof RNKRTKN RARIAKV-PLPEAALN Dof RNKRSKS RARQA-NIPPLAGPLK Dof RNNKKGK
AtDof2.2 StDof1 ZmDof3
RARLAKNSQPPEGALK Dof RN-KKGK RARLAKV-PLPEAALN Dof RNKRSKS RARLAR-IPLPEPGLK Dof RHAKRAK
AtDof5.4 ZmDof1 ZmDof2 OsDof4
Dof A KRS APAPAVGEGDP Dof APG-----GDP Dof Dof TKRS
AtDof5.6 ZmPBF BPBF WPBF
Dof GERKPRPQLPEALK- Dof AEKKSRPK-PEQKVE Dof PKRP AEKKPRPK-PEQKVE Dof PKRS Dof SKRS
OsDof3
Group II
LCANPAALSR LQANPAALSR
LGGEAQN Dof NKR GGERKARP-EKDQAVN Dof NKR PVERKARP-EKDQALN Dof NKR VA ERKARP-Q-EK-LN Dof NKR MET RKARP-Q-EK-VN Dof NKR MTTMSTRP-Q-EP-RN Dof NKK
AtDof2.5
Group I
Dof
AtDof1.2 AtDof3.5 AtDof3.2 AtDof5.3 AtDof2.1 AtDof4.6
QSSVSQMILAEIQQGNHQPF QSSISEMVSVENQPINHQSF
QQSSM QQHQ
VKVED Group V VKMEDSNNQLNLSR
QQAQQFPFL
NLSR VKMEEQPNLANLSR VKMEDN-HLGNISR
QQMQSFPFL
VDHAYW PP--YW PPAAYW
DQDQS--GLYLPstop DPDPACIFLNLPstop DTDPA-LFLNLPstop VPDPN---VYLPstop
TMGLFPNVLPTLMPTGGG TGMNFANVLPTFMSGGFD TGMNFANVLPTFMSVGFE
Group VI
Group VII
PCADFPNVLPTFVSTGFE TRENDS in Plant Science
DAG1 gene is expressed in flowers but not in embryos in accordance with its maternal role [13,31,33]. In addition, OBP1 mRNA is induced by plant defense http://plants.trends.com
signals [10,14]. OsDof3 expression is induced by GA, but an antagonistic phytohormone of GA, abscisic acid, prevents the GA effect on OsDof3 expression [11].
Review
TRENDS in Plant Science Vol.7 No.12 December 2002
Fig. 2. Dof protein relationships. The phylogenetic tree was created using full sequences of Arabidopsis Dof proteins, using the ClustalW program. Dof proteins from other species (indicated in red) are also classified into subgroups. The first one or two letters of the names indicate the initials of the species (except that of pumpkin, which is AOBP): At, Arabidopsis thaliana; B, barley; Nt, Nicotiana tabacum; Os, Oryza sativa; St, Solanum tuberosum; W, wheat, Zm, Zea mays. The signature motifs conserved among members of the same group are shown in blue. Examples of motifs conserved in only some members are shown in green. Non-homologous sequences between motifs are indicated by bars. Although no conserved motifs are found in AtDof5.6 or OsDof5, they were suggested to form subgroups with others on the basis of the calculation using the ClustalW program.
A recent study using the Arabidopsis GeneChip system also showed that the expression of Dof genes were controlled differently in various environmental conditions [34]. However, the ZmDof1 activity appears to be modulated in a post-translational manner in response to light [16,17]. A protein kinase inhibitor was recently observed to activate ZmDof1, suggesting that protein phosphorylation–dephosphorylation might be included in the regulation for Dof proteins (S. Yanagisawa, unpublished). Evolutionary diversification
Acknowledgements I would like to thank Hiroshi Akanuma and Terunao Takahara for their critical reading of the manuscript, and Cheri Chen for assistance in surveying Arabidopsis Dof proteins. Research support was provided in part by the Ministry of Education, Culture, Sports, Science and Technology, Japan (no. 13780549 and no. 13039006).
The complete catalog of Dof proteins in a single plant species is useful for viewing the structural and functional diversity among Dof proteins as a whole. In a survey of the complete Arabidopsis genome sequence, 37 putative Dof genes have been found [1]. Because several Arabidopsis Dof proteins and their genes have been named in a non-systematic manner, they are listed in Table 2 in the order of their chromosomal positions. Although, at this stage, it is impossible to evaluate the expression of these genes exactly, ESTs corresponding to the genes in the database suggest that most of the genes are expressed, whereas the AtDof1.9 gene appears to be a pseudogene owing to a stop codon within the Dof domain. A phylogenetic tree categorizes Arabidopsis Dof proteins into seven subgroups (Fig. 2). Although the primary structures, except the Dof domain, are largely divergent among all Dof proteins, detailed comparison revealed small structural motifs that could become hallmarks, substantiating the validity of the classification. Amino acid substitutions within the Dof domain were also in accord with the classification. A recent genome-wide analysis suggested that the Arabidopsis genome had been generated by four different large-scale genome duplications 100 million to 200 million years ago (during the formative period in the diversification of angiosperms) [35]. Obviously, such genome duplications caused multiplication of Dof genes. For instance, generation of the AtDof3.2 and AtDof5.3 genes, which are located close to one another in the phylogenetic tree, is a result of genome duplication that was estimated to have occurred 100 million years ago. The same genome duplication also gave rise to the divergence of the AtDof2.5 and AtDof3.7 genes in Group III, and the divergence of the AtDof1.1 and AtDof2.2 genes in Group V. By contrast, other close relationships between the AtDof1.7 and http://plants.trends.com
559
AtDof3.1 genes and between the AtDof4.7 and AtDof5.7 genes reflect different genome duplications, which were estimated to have occurred 140 million years ago and 170 million years ago, respectively. Accordingly, the formation of subgroups appears to be originated from the multiplication of a Dof gene from a much older period, presumably before the divergence of monocots and dicots, which was estimated to have occurred between 180 million and 220 million years ago [36,37]. This is further supported because the same subgroups include both monocot and dicot Dof proteins. Thus, the complete catalog of Arabidopsis Dof proteins might disclose both the diversity common to all higher plants (represented by subgroups) and the diversity specific to dicots or species (represented by each member in the same subgroup). There is limited information about the relationship between functional diversification and gene multiplication. However, it is not unexpected that members in the same subgroup show redundant, overlapping or related functions. Indeed, OsDof3, which is specifically expressed in the scutellum and the endosperm of rice in response to GA during germination, forms a subgroup together with other Dof proteins associated with endosperm development (PBF, BPBF and WPBF). In addition, recent studies revealed that two closely related Arabidopsis Dof genes in Group III [DAG1 (AtDof3.7) and DAG2 (AtDof2.5)] are maternal genes involved in the control of seed germination, although their actions are opposite [13,31]. Furthermore, the phylogenetic tree of Dof proteins suggests that the branching of Dof genes after the divergence of monocots and dicots might produce further functional diversity in a dicot- or monocotspecific, or species-specific manner. For example, Group VI (Fig. 2) includes only a single Arabidopsis Dof protein but two maize Dof proteins (ZmDof1 and ZmDof2). These maize proteins display different expression patterns and related but different functions [16]. Many roles have already been suggested for Dof proteins. However, more roles should come to light in the future because the complete list of Arabidopsis Dof proteins suggests that most Dof proteins have yet to be characterized. Although further analyses should establish the function of each Dof protein, including gain-of-function and loss-of-function experiments, it is apparent that Dof proteins are involved in diverse plant physiology. This is not surprising because the structural and functional diversification of Dof proteins appears to have occurred at an early stage of higher plant evolution. Comparative studies with lower plants, such as mosses and algae, might reveal the origin and the primary role of Dof proteins, and also the evolutionary linkage between the functional diversification of Dof proteins and the emergence of higher plants in the world.
560
Review
References 1 Riechmann, J.L. et al. (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290, 2105–2110 2 Yanagisawa, S. and Izui, K. (1993) Molecular cloning of two DNA-binding proteins of maize that are structurally different but interact with the same sequence motif. J. Biol. Chem. 268, 16028–16036 3 Yanagisawa, S. (1995) A novel DNA binding domain that may form a single zinc finger motif. Nucleic Acids Res. 23, 3403–3410 4 Yanagisawa, S. (1996) Dof DNA binding domains contain a novel zinc finger motif. Trends Plant Sci. 1, 213–214 5 Zhang, B. et al. (1995) Interactions between distinct types of DNA binding proteins enhance binding to ocs element promoter sequences. Plant Cell 7, 2241–2252 6 de Paolis, A. et al. (1996) A rolB regulatory factor belongs to a new class of single zinc finger plant proteins. Plant J. 10, 215–223 7 Vicente-Carbajosa, J. et al. (1997) A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator. Proc. Natl. Acad. Sci. U. S. A. 94, 7685–7690 8 Kisu, Y. et al. (1998) Characterization and expression of a new class of zinc finger protein that binds to silencer region of ascorbate oxidase gene. Plant Cell Physiol. 39, 1054–1064 9 Mena, M. et al. (1998) An endosperm-specific DOF protein from barley, highly conserved in wheat, binds to and activates transcription from the prolamin-box of a native b-hordein promoter in barley endosperm. Plant J. 16, 53–62 10 Kang, H-G. and Singh, K. (2000) Characterization of salicylic acid-responsive, Arabidopsis Dof domain proteins: overexpression of OBP3 leads to growth defects. Plant J. 21, 329–339 11 Washio, K. (2001) Identification of Dof proteins with implication in the gibberellin-regulated expression of a peptidase gene following the germination of rice grains. Biochim. Biophys. Acta 1520, 54–62 12 Plesch, G. et al. (2001) Involvement of TAAAG elements suggests a role for Dof transcription factors in guard cell-specific gene expression. Plant J. 28, 455–464
TRENDS in Plant Science Vol.7 No.12 December 2002
13 Gualberti, G. et al. (2002) Mutations in the Dof zinc finger genes DAG2 and DAG1 influence with opposite effects the germination of Arabidopsis seeds. Plant Cell 14, 1253–1263 14 Chen, W. et al. (1996) The promoter of an H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBFand OBP1-binding sites. Plant J. 10, 955–966 15 Shimofurutani, N. et al. (1998) Functional analyses of the Dof domain, a zinc-finger DNA-binding domain, in a pumpkin DNA-binding protein AOBP. FEBS Lett. 430, 251–256 16 Yanagisawa, S. and Sheen, J. (1998) Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression. Plant Cell 10, 75–89 17 Yanagisawa, S. (2001) The transcriptional activation domain of the plant-specific Dof1 factor functions in plant, animal, and yeast cells. Plant Cell Physiol. 42, 813–822 18 Diaz, I. et al. (2002) The GAMYB protein from barley interacts with the DOF transcription factor BPBF and activates endosperm-specific genes during seed development. Plant J. 29, 453–464 19 Jin, H. and Martin, C. (1999) Mutifunctionality and diversity within the plant MYB gene family. Plant Mol. Biol. 41, 577–585 20 Eulgem, T. et al. (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199–206 21 Yanagisawa, S. (2000) Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J. 21, 281–288 22 Yanagisawa, S. and Schmidt, R.J. (1999) Diversity and similarity among recognition sequences of Dof transcription factors. Plant J. 17, 209–214 23 Mackay, J.P. and Crossley, M. (1998) Zinc fingers are sticking together. Trends Biochem. Sci. 23, 1–4 24 Albani, D. et al. (1997) The wheat transcriptional activator SPA: a seed-specific bZIP protein that recognizes that GCN4-like motif in the bifactorial endosperm box of prolamin genes. Plant Cell 9, 171–184 25 Vicente-Carbajosa, J. et al. (1998) Barley BLZ1: a bZIP transcriptional activator that interacts with endosperm-specific gene promoters. Plant J. 13, 629–640
26 Aukerman, M.J. and Schmidt, R.J. (1994) Regulation of α-zein gene expression during maize endosperm development. In Results and Problems in Cell Diferentiation Vol. 20 (Nover, L., ed.), pp. 209–233, Springer 27 Muller, M. et al. (1995) Regulation of storage protein synthesis in cereal seeds: developmental and nutritional aspects. J. Plant Physiol. 145, 606–613 28 Yanagisawa, S. (1997) Dof DNA binding domains of plant transcription factors contribute to multiple protein-protein interactions. Eur. J. Biochem. 250, 403–410 29 Krohn, N.M. et al. (2002) Specificity of the stimulatory interaction between chromosomal HMGB proteins and the transcription factor Dof2 and its negative regulation by protein kinase CK2-mediated phosphorylation. J. Biol. Chem. 277, 32438–32444 30 Singh, K.B. (1998) Transcriptional regulation in plants: the importance of combinatorial control. Plant Physiol. 118, 1111–1120 31 Papi, M. et al. (2000) Identification and disruption of an Arabidopsis zinc finger gene controlling seed germination. Genes Dev. 14, 28–33 32 Baumann, K. et al. (1999) The DNA binding site of the Dof protein NtBBF1 is essential for tissue-specific and auxin-regulated expression of the rolB oncogene in plants. Plant Cell 11, 323–333 33 Papi, M. et al. (2002) Inactivation of the phloem-specific Dof zinc finger gene DAG1 affects response to light and integrity of the testa of Arabidopsis seeds. Plant Physiol. 128, 411–417 34 Chen, W. et al. (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14, 559–574 35 Vision, T.J. et al. (2000) The orgin of genomic duplications in Arabidopsis. Science 290, 2114–2117 36 Soltis, P. et al. (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402, 402–404 37 Yang, Y-W. et al. (1999) Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and other angiosperm lineages. J. Mol. Evol. 48, 597–604
Managing your references and BioMedNet Reviews Did you know that you can now download selected search results on BioMedNet Reviews directly into your chosen reference managing software? After performing a search, simply click to select the articles you wish, choose the format required (e.g. EndNote 3.1), and the bibliographic details, the abstract and the link to the full-text article will download into your desktop reference manager database. BioMedNet Reviews is available on an institute-wide subscription. If you do not have access to the full-text articles in BioMedNet Reviews, ask your librarian to contact us at [email protected]
http://plants.trends.com
TRENDS in Plant Science Vol.7 No.12 December 2002
555
The Dof family of plant transcription factors Shuichi Yanagisawa Dof proteins are members of a major family of plant transcription factors. The proteins have similar DNA-binding properties because of the highly conserved DNA-binding domain. However, recent studies are disclosing their diverse roles in gene expression when associated with plant-specific phenomena including light, phytohormone and defense responses, seed development and germination. Based on the structural diversity indicated by the complete catalog of Arabidopsis Dof proteins, Dof genes appear to have evolved multiple times, preceding and paralleling the diversification of angiosperms. Such gene multiplication might have led to the functional diversification of Dof proteins proceeding differently in distinct plant species.
Plant gene expression involves classes of transcription factors that have specifically evolved to regulate plant-specific genes and/or to mediate a variety of plant-specific signals. The Dof family is a typical example of such transcription factors. Many Dof proteins have already been discovered in both monocots and dicots. Currently, we know only a fraction of their biological roles. However, it is evident that Dof proteins play vital roles in plant gene expression. In the complete Arabidopsis genome sequence, 37 putative Dof genes are discernible [1]. The presence of so many Dof genes suggests that multiplication of Dof genes might be linked with the formation of sophisticated transcriptional control in higher plants. What are Dof proteins?
Shuichi Yanagisawa Dept of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Komaba, Meguro, Tokyo 153-8902, Japan. e-mail: csyanag@ mail.ecc.u-tokyo.ac.jp
The first Dof protein (ZmDof1) was found as a DNA-binding protein of maize [2]. The DNA-binding domain in ZmDof1 includes a C2C2-type zinc-fingerlike motif, although the amino acid sequence of this domain is largely different from those of other zinc-finger domains (Fig. 1a). The divalent metal chelators, 1, 10-o-phenanthroline and EDTA, inhibited the DNA-binding of ZmDof1, and mutations on cysteine residues that had been expected to coordinate to a zinc ion also prevented the DNA-binding activity [3]. This suggested that the DNA binding domain contained a variant of zinc fingers, and it was therefore referred to as the Dof (DNA-binding with one finger) domain [3,4]. During recent years, >20 cDNAs encoding a Dof domain have been isolated from maize and other plant species, including Arabidopsis, tobacco, pumpkin, potato, barley, wheat and rice [3,5–13]. Dof proteins, which are typically composed of 200–400 amino acids, are now defined as DNA-binding proteins that have a highly conserved Dof domain. In spite of intensive homology in the Dof domain, the rest of the amino http://plants.trends.com
acid sequences in the proteins are divergent, coinciding with their expected diverse functions. The inhibitory effects of the metal chelators and the absolute requirement of cysteine residues for putative zinc coordination were repeatedly demonstrated in studies of the DNA interaction of several Dof proteins [6,8,11,14]. Furthermore, two aromatic amino acid residues (Tyr and Trp) conserved among all Dof domains are necessary for sufficient DNA-binding of a pumpkin Dof protein [15]. However, whether the Dof domain includes a zinc finger has still to be determined. By contrast, the assumption that Dof proteins are unique to plants has been verified in a recent comparative study using the complete genome information from Arabidopsis, Drosophila, Caenorhabditis elegans and yeast [1]. Dof proteins as transcription factors
Co-transfection experiments with expression vectors for Dof proteins and their putative target promoters fused to reporter genes have provided direct evidence that Dof proteins function as transcriptional activators or repressors through direct interaction with DNA. For instance, ZmDof1 enhanced reporter gene expression depending on the binding sites in the promoters, whereas co-expression of another maize protein (ZmDof2) suppressed the positive effect of ZmDof1 in maize mesophyll protoplasts [16]. A barley Dof protein (BPBF) also activated the transcription from a putative target promoter in particle-bombarded endosperm, but BPBF with mutations on the cysteine residues for putative zinc coordination did not [9]. In accordance with its activity as a transcription factor, nuclear localization of ZmDof1 was also shown [16,17]. Interestingly, the transcriptional activation domain of ZmDof1 can function not only in plant cells but also in animal cells and in yeast [17]. Like aromatic residues in the transcriptional activation domains of animal factors GATA-4 and VP16, a tryptophan residue in the transcriptional activation domain of ZmDof1 is of particular importance for the function [17]. In addition, the C-terminal part of BPBF also functions as a transcriptional activation domain in yeast [18]. Therefore, although Dof proteins are unique to plants, some Dof proteins might regulate transcription through a mechanism evolutionarily conserved among all eukaryotes.
1360-1385/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S1360-1385(02)02362-2
Review
556
TRENDS in Plant Science Vol.7 No.12 December 2002
Table 1. A variety of putative roles for Dof proteins in plants
(a) CPRCASRDTKFCYYNNYNTSQPRHFCKGCRRYWTKGGTLRNVPVGGGTRK
Activation
Dof 1
(b)
100
NLS
200
238 amino acids
+1
Arabidopsis GST6 promoter
–450 TGACGACCTCCTCTACACTTTT
OBF
OBP1
Refs
ZmDof1 PBF BPBF WPBF OBP1 DAG1 DAG2 NtBBF1 AOBP OsDof3 StDof1
Maize Maize Barley Wheat Arabidopsis Arabidopsis Arabidopsis Tobacco Pumpkin Rice Potato
Light response Endosperm specificity Orthologs of PBF Orthologs of PBF Defense response Seed germination Seed germination Auxin response Auxin response Gibberellin response Guard cell specificity
[16,21] [7] [9] [9] [5,14] [31] [13] [6,32] [8] [11] [12]
Dual function of the Dof domain
The strong similarity among Dof DNA-binding domains suggested that all Dof proteins display similar DNA-binding specificity. Indeed, an AAAG sequence or its reversibly orientated sequence, CTTT, is always found in the binding sequences of individual Dof proteins [2,5–7,9–12,14,16,21], except a pumpkin Dof protein (AOBP) that recognizes an AGTA motif [8]. Furthermore, binding- site selection experiments with four maize Dof proteins established an (A/T)AAAG sequence as the recognition core [22]. A different preference of each protein on the sequence flanking the core motif was also shown, but it affected the DNA recognition only to a limited extent [22]. Similar to the many cases of other transcription factors, precise selection of target promoters by each Dof protein in vivo might require other factors in addition to the DNA sequence. Dual activity of the Dof domain might be a clue to understanding why each Dof protein can act on correct target promoters in vivo. Like other zinc fingers [23], the Dof domain is known to be a bi-functional domain that mediates not only DNA-binding but also protein–protein interactions. The first protein–protein interaction was reported by Bei Zhang et al. [5]. An Arabidopsis Dof protein (OBP1), which was isolated as a protein specifically interacting with basic leucine zipper (bZIP) proteins (OBF4 and 5), promoted the binding of the bZIP proteins to DNA through its Dof domain [5,10]. An OBP1-binding site in close vicinity to an OBF-binding site was indeed found on a target promoter, Arabidopsis GST6 promoter (Fig. 1b) [14]. Another example of the Dof–bZIP interaction can be seen in the interaction of PBF (a maize endospermspecific Dof protein) with O2 (a maize bZIP protein involved in endosperm-specific gene expression) [7]. The physiological significance of the PBF–O2 interaction is shown by the requirement of the PBF-binding site for O2-dependent activation [24,25] and conservation of the set of PBF- and O2-binding sites in many promoters of cereal storage-protein genes [26,27]. Furthermore, another target promoter of O2 in the endosperm (the maize cyPPDK promoter)
+1
TGTCACATGTGTAAAGGTGAAGAGATCATGCATGTCATTCCACGTAG
O2
O2
TRENDS in Plant Science
Fig. 1. (a) Scheme of ZmDof 1 as an example of the Dof protein domain structure. The Dof domain, a nuclear localization signal (NLS) and the transcriptional activation domain are indicated in yellow, pink and purple, respectively. A serine-stretch is indicated in green. The cysteine residues for putative coordination of zinc are shown in red letters in the Dof domain amino acid sequence. (b) Examples of Dof-binding sites in plant promoters. The binding sites for Dof proteins and bZIP proteins are indicated in red and blue, respectively. Dof–bZIP interactions and transcription start sites are indicated by bi-directional arrows and bent arrows, respectively.
Domain structure
Transcription factors sometimes contain multiple DNA-binding domains. For example, some plant MYB proteins have a single MYB DNA-binding domain, but others contain imperfect repeats of the MYB domain [19]. In addition, single MYB-domain proteins and two- or three-repeat MYB proteins have been suggested to bind DNA in different ways [19]. Similarly, plant-specific WRKY transcription factors possess different numbers of WRKY DNA-binding domains, which allows the proteins to be classified into subgroups [20]. However, in the case of Dof proteins, only a single copy of the Dof domain can always be found in their N-terminal regions. By contrast, the minimal transcriptional activation domain of ZmDof1 has been mapped in 44 amino acid residues of the C-termini [17]. The C-terminal regions of other Dof proteins (Arabidopsis OBP1, 2 and 3, and barley BPBF) also include transcriptional activation domains [10,18]. Taken together, Dof proteins usually appear to consist of two major domains: an N-terminal conserved DNA-binding domain and a C-terminal domain for transcriptional regulation (Fig. 1a). Serine-stretches that are frequently located immediately downstream of the Dof domains might be the molecular hinges linking the two domains. http://plants.trends.com
Putative role
OBP1 OBP1
–250
PBF
Species
AAAAGGAAAG
Maize 22-kDa zein promoter
O2
Dof protein
Review
TRENDS in Plant Science Vol.7 No.12 December 2002
Table 2. List of Arabidopsis Dof genes a
b
c
Dof gene
Gene code
Clone
EST
Synonymous
AtDof1.1 AtDof1.2 AtDof1.3 AtDof1.4 AtDof1.5 d AtDof1.6 AtDof1.7 AtDof1.8 AtDof1.9 AtDof1.10 AtDof2.1 AtDof2.2 AtDof2.3 AtDof2.4 AtDof2.5 AtDof3.1 AtDof3.2 AtDof3.3 AtDof3.4 AtDof3.5 AtDof3.6 AtDof3.7 AtDof4.1 AtDof4.2 AtDof4.3 AtDof4.4 AtDof4.5 AtDof4.6 AtDof4.7 AtDof5.1 AtDof5.2 AtDof5.3 AtDof5.4 AtDof5.5 AtDof5.6 AtDof5.7 AtDof5.8
At1 g07640 At1 g21340 At1 g26790 At1 g28310 At1 g29160 At1 g47650 At1 g51700 At1 g64620 At1 g65935 At1 g69570 At2 g28510 At2 g28810 At2 g34140 At2 g37590 At2 g46590 At3 g21270 At3 g45610 At3 g47500 At3 g50410 At3 g52440 At3 g55370 At3 g61850 At4 g00940 At4 g21030 At4 g21040 At4 g21050 At4 g21080 At4 g24060 At4 g38000 At5 g02460 At5 g39660 At5 g60200 At5 g60850 At5 g62430 At5 g62940 At5 g65590 At5 g66940
F24B9 F24J8 T24P13 F3H9 F28N24 F16N3 F19C24 F1N19 F12P19 F10D13 T17D12 F8N16 T14G11 F13M22 F13A10 MXL8 F9K21 F1P2 F11C1 F22O6 T22E16 F21F14 T18A10 T13K14 T13K14 T13K14 F7J7 T19F6 F20D10 T22P11 MIJ24 F15L12 MAE1 K19B1 MQB2 K21L13 K8A10
AV540721 – – – – – BE038318 T14116 – AV564595 – AI999028 AA395802 – AI993066 BE038318 AV442796 AV559509 AW004398 – T22381 AV543166 H77029 – – – – AV537390 AV531601 AV560727 T88559 N38019 AI995889 AV519437 – T43764 –
OBP2 – – – – – ADOF1 – – – – – – – DAG2 ADOF2 – – OBP1 – OBP3 DAG1 and BBFa – – – – – – – – – – OBP4 – – – –
a
Nomenclature giving first the chromosome numbers and then orders on the chromosome. GenBank accession numbers. Even if multiple ESTs were found, only one is shown. '–' indicates no GenBank accession number. c The original names used in publication or for registration in a database. '–' indicates no other name. d The open reading frame (ORF) for AtDof1.6 was estimated using a Met codon that was different from the putative translational start Met codon for the ORF, At1 g47650. b
is also a target of ZmDof1 in leaf mesophyll cells, although no Dof–bZIP interaction associated with the activity of the cyPPDK promoter has been identified [21]. These examples reveal an interesting character of the Dof domains, but it still uncertain whether every Dof protein interacts with a bZIP protein. The Dof domain also mediates other types of protein–protein interactions. The Dof domain showed a specific affinity to distinct Dof domains, although the biochemical and biological meanings of this affinity have not been clarified yet [28]. In addition, Dof domains interacted with maize HMG (chromatin-associated high mobility group) proteins and different HMG proteins enhanced DNA-binding of Dof proteins to different extents [28,29]. http://plants.trends.com
557
Combinatorial regulation by distinct classes of transcription factors is a persuasive explanation for seeming discrepancies between DNA-binding in vitro and the action in vivo of transcription factors [30]. It is likely that the dual function of the Dof domain contributes to correct choice and/or selective activation or repression of target genes in vivo. However, the exact meanings of these protein–protein interactions in transcriptional control still remain to be evaluated in vivo. Also, it is still unknown what determines the specificity of these interactions in spite of the conserved amino acid sequence within the Dof domain. In a recent report, the Dof–MYB interaction was mediated through the C-terminal of BPBF but not through the Dof domain [18]. Analogous to the case of O2 protein, both the MYB-binding and the Dof binding sites were necessary for the MYB protein to activate the transcription from a target promoter [18]. Divergent roles of Dof proteins
Divergent physiological roles of Dof proteins have been suggested to date (Table 1). The suggested roles do not have anything in common apart from all being linked to plant-specific gene expression. Maize Dof1 was suggested to be a regulator for the light-responsive expression of multiple genes, including the C4 photosynthetic phosphoenolpyruvate carboxylase gene [16,21]. Maize PBF and its orthologs of wheat and barley appear to be transcription factors controlling endosperm-specific expression of storage proteins [7,9]. Arabidopsis OBP1 might regulate defense gene expression in response to salicylic acid and oxidative stress signals [5,14]. Arabidopsis DAG1 and DAG2 have been shown to act on a maternal switch controlling seed germination by isolating mutants with a T-DNA insertion in their respective genes [13,31]. Dof proteins are probably also involved in phytohormone-regulated expression. A tobacco Dof protein, NtBBF1, is a candidate for the activator of auxin-inducible expression of a plant oncogene rolB in apical meristems and vascular tissues [6,32]. Participation of Dof proteins in gene silencing has also been suggested from the binding of a pumpkin Dof protein (AOBP) to the silencer region of the auxin-inducible ascorbate-oxidase gene promoter [8]. Some gibberellin (GA) responses might involve Dof proteins as well. A rice Dof protein, OsDof3, might be a mediator for GA signaling during germination [11]. Recently, another function of Dof proteins was suggested in the regulation of guard cell-specific gene expression in potato [12]. Although every role has not been confirmed conclusively, Dof proteins apparently function in the regulation of various processes. Transcriptional and post-transcriptional regulations matching the suggested physiological functions have also been reported on expression of several Dof proteins. For example, expression of PBF gene is strictly restricted to certain developmental stages in the endosperm [7,9], and
558
Review
TRENDS in Plant Science Vol.7 No.12 December 2002
AtDof4.2 AtDof4.4 AtDof4.3 AtDof4.5
DNEMN--VMPPP--RV Dof DNQVNGLKRPPPS-RV Dof DNQVNDVKPPPPPPRV Dof DNQVNDVKPPPPPPRV Dof
OsDof5 AtDof3.3 AtDof5.5 AtDof5.2 AtDof1.5 AtDof2.3 AtDof1.3 AtDof1.10 AOBP
QPSVAQMVSVGIQPGSHKPF QPSVARMVSVETQRGNNQPF
KTLKKPTKILP Dof NK KTLKKPTKILP Dof NK LKKPDKILP Dof NK
LSANPAALSR
DLTAEKRPDKIIP Dof SK DLTAEKRPDKIIA Dof SK EKTTELKKPDKILP Dof NK EKSTALKKPDKLIP Dof NK LKKPDKILP Dof NK
LQANPAAMAR LQANPAAMSR LQANPAALSR
Dof RSR Dof SRR PEQSLR Dof HKR PPELALR Dof NKR
AtDof3.7 AtDof4.1 NtBBF1 NtBBF2a OsDof1 OsDof2
PTERKPRP-QKEQAIN HIERKIRPHQKDQALN STERRARP-QKEKALN GTERRARP-QKEKALN
AtDof1.8
AtDof3.4 AtDof5.8 AtDof1.6 AtDof1.7 AtDof3.1 AtDof4.7 AtDof5.7 AtDof1.4 AtDof2.4 AtDof5.1
MPSEFSESR MPSEPNQTR MQDLTSAA MQDP--AA
Dof Dof Dof Dof
IDLAAVFA LRTTPEP LRTTPEP
IDLALVYA MELGLAYA IDLSLAFA
LPDLNP
QDLNLGFS KDLNLAFS QDLNLLSF
LPDLNP LPDLNP
KDLNLLSF NDLSLSFS
Group III
IDLNLAFA
NKR SKK NKR NKR
HDLNLAFN QDLNLGFS QDLNLAFP QDLNLAFP
QEQLP Dof QEQLS Dof AEPLP Dof QEQLK Dof QEQLK Dof QPVLK Dof
PLQTTPVLFPQ PLQATPVLFPQ
QQNLK Dof QPQLK Dof
SSIETLSCLNQDLHWRLQQQR
Group IV
SSIESLSSFNQDLHQKLQQQR
AtDof3.6 AtDof1.1
RARQA-NVALPEAALK Dof RNRRTKS RARLA-NIPLPETALK Dof RNKRTKN RARIAKV-PLPEAALN Dof RNKRSKS RARQA-NIPPLAGPLK Dof RNNKKGK
AtDof2.2 StDof1 ZmDof3
RARLAKNSQPPEGALK Dof RN-KKGK RARLAKV-PLPEAALN Dof RNKRSKS RARLAR-IPLPEPGLK Dof RHAKRAK
AtDof5.4 ZmDof1 ZmDof2 OsDof4
Dof A KRS APAPAVGEGDP Dof APG-----GDP Dof Dof TKRS
AtDof5.6 ZmPBF BPBF WPBF
Dof GERKPRPQLPEALK- Dof AEKKSRPK-PEQKVE Dof PKRP AEKKPRPK-PEQKVE Dof PKRS Dof SKRS
OsDof3
Group II
LCANPAALSR LQANPAALSR
LGGEAQN Dof NKR GGERKARP-EKDQAVN Dof NKR PVERKARP-EKDQALN Dof NKR VA ERKARP-Q-EK-LN Dof NKR MET RKARP-Q-EK-VN Dof NKR MTTMSTRP-Q-EP-RN Dof NKK
AtDof2.5
Group I
Dof
AtDof1.2 AtDof3.5 AtDof3.2 AtDof5.3 AtDof2.1 AtDof4.6
QSSVSQMILAEIQQGNHQPF QSSISEMVSVENQPINHQSF
QQSSM QQHQ
VKVED Group V VKMEDSNNQLNLSR
QQAQQFPFL
NLSR VKMEEQPNLANLSR VKMEDN-HLGNISR
QQMQSFPFL
VDHAYW PP--YW PPAAYW
DQDQS--GLYLPstop DPDPACIFLNLPstop DTDPA-LFLNLPstop VPDPN---VYLPstop
TMGLFPNVLPTLMPTGGG TGMNFANVLPTFMSGGFD TGMNFANVLPTFMSVGFE
Group VI
Group VII
PCADFPNVLPTFVSTGFE TRENDS in Plant Science
DAG1 gene is expressed in flowers but not in embryos in accordance with its maternal role [13,31,33]. In addition, OBP1 mRNA is induced by plant defense http://plants.trends.com
signals [10,14]. OsDof3 expression is induced by GA, but an antagonistic phytohormone of GA, abscisic acid, prevents the GA effect on OsDof3 expression [11].
Review
TRENDS in Plant Science Vol.7 No.12 December 2002
Fig. 2. Dof protein relationships. The phylogenetic tree was created using full sequences of Arabidopsis Dof proteins, using the ClustalW program. Dof proteins from other species (indicated in red) are also classified into subgroups. The first one or two letters of the names indicate the initials of the species (except that of pumpkin, which is AOBP): At, Arabidopsis thaliana; B, barley; Nt, Nicotiana tabacum; Os, Oryza sativa; St, Solanum tuberosum; W, wheat, Zm, Zea mays. The signature motifs conserved among members of the same group are shown in blue. Examples of motifs conserved in only some members are shown in green. Non-homologous sequences between motifs are indicated by bars. Although no conserved motifs are found in AtDof5.6 or OsDof5, they were suggested to form subgroups with others on the basis of the calculation using the ClustalW program.
A recent study using the Arabidopsis GeneChip system also showed that the expression of Dof genes were controlled differently in various environmental conditions [34]. However, the ZmDof1 activity appears to be modulated in a post-translational manner in response to light [16,17]. A protein kinase inhibitor was recently observed to activate ZmDof1, suggesting that protein phosphorylation–dephosphorylation might be included in the regulation for Dof proteins (S. Yanagisawa, unpublished). Evolutionary diversification
Acknowledgements I would like to thank Hiroshi Akanuma and Terunao Takahara for their critical reading of the manuscript, and Cheri Chen for assistance in surveying Arabidopsis Dof proteins. Research support was provided in part by the Ministry of Education, Culture, Sports, Science and Technology, Japan (no. 13780549 and no. 13039006).
The complete catalog of Dof proteins in a single plant species is useful for viewing the structural and functional diversity among Dof proteins as a whole. In a survey of the complete Arabidopsis genome sequence, 37 putative Dof genes have been found [1]. Because several Arabidopsis Dof proteins and their genes have been named in a non-systematic manner, they are listed in Table 2 in the order of their chromosomal positions. Although, at this stage, it is impossible to evaluate the expression of these genes exactly, ESTs corresponding to the genes in the database suggest that most of the genes are expressed, whereas the AtDof1.9 gene appears to be a pseudogene owing to a stop codon within the Dof domain. A phylogenetic tree categorizes Arabidopsis Dof proteins into seven subgroups (Fig. 2). Although the primary structures, except the Dof domain, are largely divergent among all Dof proteins, detailed comparison revealed small structural motifs that could become hallmarks, substantiating the validity of the classification. Amino acid substitutions within the Dof domain were also in accord with the classification. A recent genome-wide analysis suggested that the Arabidopsis genome had been generated by four different large-scale genome duplications 100 million to 200 million years ago (during the formative period in the diversification of angiosperms) [35]. Obviously, such genome duplications caused multiplication of Dof genes. For instance, generation of the AtDof3.2 and AtDof5.3 genes, which are located close to one another in the phylogenetic tree, is a result of genome duplication that was estimated to have occurred 100 million years ago. The same genome duplication also gave rise to the divergence of the AtDof2.5 and AtDof3.7 genes in Group III, and the divergence of the AtDof1.1 and AtDof2.2 genes in Group V. By contrast, other close relationships between the AtDof1.7 and http://plants.trends.com
559
AtDof3.1 genes and between the AtDof4.7 and AtDof5.7 genes reflect different genome duplications, which were estimated to have occurred 140 million years ago and 170 million years ago, respectively. Accordingly, the formation of subgroups appears to be originated from the multiplication of a Dof gene from a much older period, presumably before the divergence of monocots and dicots, which was estimated to have occurred between 180 million and 220 million years ago [36,37]. This is further supported because the same subgroups include both monocot and dicot Dof proteins. Thus, the complete catalog of Arabidopsis Dof proteins might disclose both the diversity common to all higher plants (represented by subgroups) and the diversity specific to dicots or species (represented by each member in the same subgroup). There is limited information about the relationship between functional diversification and gene multiplication. However, it is not unexpected that members in the same subgroup show redundant, overlapping or related functions. Indeed, OsDof3, which is specifically expressed in the scutellum and the endosperm of rice in response to GA during germination, forms a subgroup together with other Dof proteins associated with endosperm development (PBF, BPBF and WPBF). In addition, recent studies revealed that two closely related Arabidopsis Dof genes in Group III [DAG1 (AtDof3.7) and DAG2 (AtDof2.5)] are maternal genes involved in the control of seed germination, although their actions are opposite [13,31]. Furthermore, the phylogenetic tree of Dof proteins suggests that the branching of Dof genes after the divergence of monocots and dicots might produce further functional diversity in a dicot- or monocotspecific, or species-specific manner. For example, Group VI (Fig. 2) includes only a single Arabidopsis Dof protein but two maize Dof proteins (ZmDof1 and ZmDof2). These maize proteins display different expression patterns and related but different functions [16]. Many roles have already been suggested for Dof proteins. However, more roles should come to light in the future because the complete list of Arabidopsis Dof proteins suggests that most Dof proteins have yet to be characterized. Although further analyses should establish the function of each Dof protein, including gain-of-function and loss-of-function experiments, it is apparent that Dof proteins are involved in diverse plant physiology. This is not surprising because the structural and functional diversification of Dof proteins appears to have occurred at an early stage of higher plant evolution. Comparative studies with lower plants, such as mosses and algae, might reveal the origin and the primary role of Dof proteins, and also the evolutionary linkage between the functional diversification of Dof proteins and the emergence of higher plants in the world.
560
Review
References 1 Riechmann, J.L. et al. (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290, 2105–2110 2 Yanagisawa, S. and Izui, K. (1993) Molecular cloning of two DNA-binding proteins of maize that are structurally different but interact with the same sequence motif. J. Biol. Chem. 268, 16028–16036 3 Yanagisawa, S. (1995) A novel DNA binding domain that may form a single zinc finger motif. Nucleic Acids Res. 23, 3403–3410 4 Yanagisawa, S. (1996) Dof DNA binding domains contain a novel zinc finger motif. Trends Plant Sci. 1, 213–214 5 Zhang, B. et al. (1995) Interactions between distinct types of DNA binding proteins enhance binding to ocs element promoter sequences. Plant Cell 7, 2241–2252 6 de Paolis, A. et al. (1996) A rolB regulatory factor belongs to a new class of single zinc finger plant proteins. Plant J. 10, 215–223 7 Vicente-Carbajosa, J. et al. (1997) A maize zinc-finger protein binds the prolamin box in zein gene promoters and interacts with the basic leucine zipper transcriptional activator. Proc. Natl. Acad. Sci. U. S. A. 94, 7685–7690 8 Kisu, Y. et al. (1998) Characterization and expression of a new class of zinc finger protein that binds to silencer region of ascorbate oxidase gene. Plant Cell Physiol. 39, 1054–1064 9 Mena, M. et al. (1998) An endosperm-specific DOF protein from barley, highly conserved in wheat, binds to and activates transcription from the prolamin-box of a native b-hordein promoter in barley endosperm. Plant J. 16, 53–62 10 Kang, H-G. and Singh, K. (2000) Characterization of salicylic acid-responsive, Arabidopsis Dof domain proteins: overexpression of OBP3 leads to growth defects. Plant J. 21, 329–339 11 Washio, K. (2001) Identification of Dof proteins with implication in the gibberellin-regulated expression of a peptidase gene following the germination of rice grains. Biochim. Biophys. Acta 1520, 54–62 12 Plesch, G. et al. (2001) Involvement of TAAAG elements suggests a role for Dof transcription factors in guard cell-specific gene expression. Plant J. 28, 455–464
TRENDS in Plant Science Vol.7 No.12 December 2002
13 Gualberti, G. et al. (2002) Mutations in the Dof zinc finger genes DAG2 and DAG1 influence with opposite effects the germination of Arabidopsis seeds. Plant Cell 14, 1253–1263 14 Chen, W. et al. (1996) The promoter of an H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBFand OBP1-binding sites. Plant J. 10, 955–966 15 Shimofurutani, N. et al. (1998) Functional analyses of the Dof domain, a zinc-finger DNA-binding domain, in a pumpkin DNA-binding protein AOBP. FEBS Lett. 430, 251–256 16 Yanagisawa, S. and Sheen, J. (1998) Involvement of maize Dof zinc finger proteins in tissue-specific and light-regulated gene expression. Plant Cell 10, 75–89 17 Yanagisawa, S. (2001) The transcriptional activation domain of the plant-specific Dof1 factor functions in plant, animal, and yeast cells. Plant Cell Physiol. 42, 813–822 18 Diaz, I. et al. (2002) The GAMYB protein from barley interacts with the DOF transcription factor BPBF and activates endosperm-specific genes during seed development. Plant J. 29, 453–464 19 Jin, H. and Martin, C. (1999) Mutifunctionality and diversity within the plant MYB gene family. Plant Mol. Biol. 41, 577–585 20 Eulgem, T. et al. (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci. 5, 199–206 21 Yanagisawa, S. (2000) Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J. 21, 281–288 22 Yanagisawa, S. and Schmidt, R.J. (1999) Diversity and similarity among recognition sequences of Dof transcription factors. Plant J. 17, 209–214 23 Mackay, J.P. and Crossley, M. (1998) Zinc fingers are sticking together. Trends Biochem. Sci. 23, 1–4 24 Albani, D. et al. (1997) The wheat transcriptional activator SPA: a seed-specific bZIP protein that recognizes that GCN4-like motif in the bifactorial endosperm box of prolamin genes. Plant Cell 9, 171–184 25 Vicente-Carbajosa, J. et al. (1998) Barley BLZ1: a bZIP transcriptional activator that interacts with endosperm-specific gene promoters. Plant J. 13, 629–640
26 Aukerman, M.J. and Schmidt, R.J. (1994) Regulation of α-zein gene expression during maize endosperm development. In Results and Problems in Cell Diferentiation Vol. 20 (Nover, L., ed.), pp. 209–233, Springer 27 Muller, M. et al. (1995) Regulation of storage protein synthesis in cereal seeds: developmental and nutritional aspects. J. Plant Physiol. 145, 606–613 28 Yanagisawa, S. (1997) Dof DNA binding domains of plant transcription factors contribute to multiple protein-protein interactions. Eur. J. Biochem. 250, 403–410 29 Krohn, N.M. et al. (2002) Specificity of the stimulatory interaction between chromosomal HMGB proteins and the transcription factor Dof2 and its negative regulation by protein kinase CK2-mediated phosphorylation. J. Biol. Chem. 277, 32438–32444 30 Singh, K.B. (1998) Transcriptional regulation in plants: the importance of combinatorial control. Plant Physiol. 118, 1111–1120 31 Papi, M. et al. (2000) Identification and disruption of an Arabidopsis zinc finger gene controlling seed germination. Genes Dev. 14, 28–33 32 Baumann, K. et al. (1999) The DNA binding site of the Dof protein NtBBF1 is essential for tissue-specific and auxin-regulated expression of the rolB oncogene in plants. Plant Cell 11, 323–333 33 Papi, M. et al. (2002) Inactivation of the phloem-specific Dof zinc finger gene DAG1 affects response to light and integrity of the testa of Arabidopsis seeds. Plant Physiol. 128, 411–417 34 Chen, W. et al. (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14, 559–574 35 Vision, T.J. et al. (2000) The orgin of genomic duplications in Arabidopsis. Science 290, 2114–2117 36 Soltis, P. et al. (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402, 402–404 37 Yang, Y-W. et al. (1999) Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and other angiosperm lineages. J. Mol. Evol. 48, 597–604
Managing your references and BioMedNet Reviews Did you know that you can now download selected search results on BioMedNet Reviews directly into your chosen reference managing software? After performing a search, simply click to select the articles you wish, choose the format required (e.g. EndNote 3.1), and the bibliographic details, the abstract and the link to the full-text article will download into your desktop reference manager database. BioMedNet Reviews is available on an institute-wide subscription. If you do not have access to the full-text articles in BioMedNet Reviews, ask your librarian to contact us at [email protected]
http://plants.trends.com