Conservation, diversification and expansion of C2H2 zinc finger proteins in the Arabidopsis thaliana genome
© Englbrecht et al; licensee BioMed Central Ltd. 2004
Received: 16 March 2004
Accepted: 05 July 2004
Published: 05 July 2004
The classical C2H2 zinc finger domain is involved in a wide range of functions and can bind to DNA, RNA and proteins. The comparison of zinc finger proteins in several eukaryotes has shown that there is a lot of lineage specific diversification and expansion. Although the number of characterized plant proteins that carry the classical C2H2 zinc finger motifs is growing, a systematic classification and analysis of a plant genome zinc finger gene set is lacking.
We found through in silico analysis 176 zinc finger proteins in Arabidopsis thaliana that hence constitute the most abundant family of putative transcriptional regulators in this plant. Only a minority of 33 A. thaliana zinc finger proteins are conserved in other eukaryotes. In contrast, the majority of these proteins (81%) are plant specific. They are derived from extensive duplication events and form expanded families. We assigned the proteins to different subgroups and families and focused specifically on the two largest and evolutionarily youngest families (A1 and C1) that are suggested to be primarily involved in transcriptional regulation. The newly defined family A1 (24 members) comprises proteins with tandemly arranged zinc finger domains. Family C1 (64 members), earlier described as the EPF-family in Petunia, comprises proteins with one isolated or two to five dispersed fingers and a mostly invariant QALGGH motif in the zinc finger helices. Based on the amino acid pattern in these helices we could describe five different signature sequences prevalent in C1 zinc finger domains. We also found a number of non-finger domains that are conserved in these families.
Our analysis of the few evolutionarily conserved zinc finger proteins of A. thaliana suggests that most of them could be involved in ancient biological processes like RNA metabolism and chromatin-remodeling. In contrast, the majority of the unique A. thaliana zinc finger proteins are known or suggested to be involved in transcriptional regulation. They exhibit remarkable differences in the features of their zinc finger sequences and zinc finger arrangements compared to animal zinc finger proteins. The different zinc finger helix signatures we found in family C1 may have important implications for the sequence specific DNA recognition and allow inferences about the evolution of the members in this family.
C2H2 zinc finger proteins (ZFPs) constitute an abundant family of nucleic acid binding proteins in the genomes of higher and lower eukaryotes. The number of ZFPs identified by in silico analysis corresponds to ~2.3 and ~3% of all genes in diptera and mammalia, respectively [1, 2]. Approximately 0.8% of the proteins in Saccharomyces cerevisiae  have C2H2 zinc finger domains and about 0.7% in Arabidopsis thaliana (this paper). C2H2 zinc fingers (ZF) display a wide range of functions, from DNA or RNA binding to the involvement in protein-protein interactions. Therefore ZFPs not only act in transcriptional regulation, either directly or through site-specific modification and/or regulation of chromatin, but also participate in RNA metabolism and in other cellular functions that probably require specific protein contacts of the ZF domain. In addition, the comparison of the whole ZFP sets in major eukaryotic lineages has revealed a remarkable level of complexity through lineage specific diversification and expansion. These expansions often include ZFPs that contain conserved lineage specific non-finger domains like the vertebrate specific KRAB domain (reviewed in ) or the ZAD domain specific to diptera . These domains are protein interaction domains with known or suggested repressor functions. Several ZFPs in plants, e.g. Arabidopsis and Petunia, have already been functionally characterized. They are involved in a variety of processes such as the regulation of floral organogenesis, leaf initiation, lateral shoot initiation, gametogenesis and stress response. Former reviews on plant-ZFPs  have been limited to approximately 30 proteins. But the systematic analysis of a complete ZFP set of a plant genome with the aim to predict some basic molecular functions is lacking. The genome annotation of the model plant Arabidopsis thaliana has reached high quality and allows comprehensive computational analyses. Here we describe the classification of the full set of ZFPs in the Arabidopsis genome including a genome-wide comparative analysis based on the in silico analysis of the whole proteome of this plant.
General classification and characterization of ZFPs in the Arabidopsis genome
Overview of conserved and unique Arabidopsis ZFPs in different subsets. Maximum values are in boldface. Unique ZFPs are further classified into families, pairs and singletons. C1S and C2S belong to one family but contain ZFs both with HX3H and HX4H spacing, an asterisk marks a pair with the exceptional combination of ZFs with HX4H and HX3H spacing in the first and second finger, respectively. The most expanded families, A1 and C1 are in italics.
∑ all Sets
- ZFPs in families
- ZFPs in pairs
∑ all ZFPs
BLAST analysis against the non-redundant database of NCBI resulted in 33 AT-ZFPs that are conserved in other taxa. The proportion of conserved AT-ZFPs varies remarkably between the different subsets (Table 1), with minor proportions in sets A/B (6 of 33), C1 (2 of 77) and C2 (9 of 44), but a major proportion in set C3 (16 of 22). The 33 conserved AT-ZFPs and their assignment to 27 evolutionarily conserved ZFP families are highlighted in Table S1 [see Additional File 1]. The family names given in the table have either been published already (Table 2) or are proposed by us. About half of the ZFP families are new (SF1-SF13) and do not contain any functionally characterized members in any species. Only six of the 33 conserved AT-ZFPs have so far been functionally characterized in Arabidopsis or other plants. They will be discussed below together with our functional predictions for some of the conserved AT-ZFPs that have so far not been experimentally investigated.
Sets A and B
Description of acronyms: Description and Pfam/SMART accession numbers (if available) of acronyms used throughout the text and in Table S1 are given. Column "conserved" refers to classification in conserved ZF-families (ZF-fam) and/or non-finger domains (NFD).
C3H1 zinc finger
CHRomatin Organisation MOdifier
Dnaj molecular chaperone domain
Plant family of unknown function
Plant family of unknown function
Plant family of unknown function
E7cadherine binding protein family
New ZFP family FZF
IPP transferase family
Jumonji domain, C-terminal part
Jumonji domain, N-terminal part
Kyprides, Ouzounis, Woese motif
Methyl-CpG binding domain
OTU-like cysteine protease
PHD zinc finger
N-terminal to some SET domains
Ribosomal protein L11 methyl-transferase (PrmA)family
Domain in protein kinases
zf-C3HC4 or RING finger
RNA recognition motif
Splicosome associated protein 61/PRP9 family
Splicosome associated protein 62/PRP11 family
Transcription factor IIIA family
U1-like zinc finger
UBA/TS-N domain (ubiquitin associated domain)
Uncharacterized protein family
Ying Yang 1 family
AN1-like zinc finger
Subset C1 comprises 77 ZFPs containing ZFs with HX3H or HX3C spacing. Only two of them, At5g09740 and At5g64610, are also conserved in other kingdoms. They arose through duplication and belong to the SAS-MOZ family (Table 2). Both ZFPs contain the conserved combination of a single ZF with CHROMO and SAS domains (Table 2). Therefore we suggest that they have a function in histone acetylation (HAT), a key process in chromatin-remodeling (reviewed in ).
In subset C2, there are more ZFPs that are involved in chromatin-remodeling processes and are conserved between plants and animals. These are VERNALIZATION 2 (VRN2), EMBRYONIC FLOWER2 (EMF2) and FERTILIZATION-INDEPENDENT SEED (FIS2) [12–15]. They belong to the Polycomb group (PcG) and were given the name VEF family. As first described in  the ZF domains and other non-finger parts of these three AT-ZFPs are conserved in the Su(z)12 proteins of Drosophila and human. PcG proteins are required to maintain the transcriptionally repressed state of homeotic genes throughout development. The molecular function(s) of their single ZF are unknown, but data from Drosophila Su(z)12 suggest their involvement in specific protein contacts, but not DNA binding. FIS2 [12, 13], VRN2  and EMF2  act as repressors in different developmental stages of Arabidopsis (reviewed in ). Another conserved AT-ZFP in subset C2 is the protein SERRATE (SE, At2g27100) . The phenotype of the SE mutant reveals a role of the affected protein in the early steps of organ elaboration and a role in the regulation of gene expression via chromatin modification was also suggested . We assigned the proteins At5g01160 and At3g12270 to the evolutionarily conserved E7 and PRMT families (Table 2), respectively, based on their conserved combination of a single ZF with a RING and a PRMT3 domain.
16 out of the 22 ZFPs in subset C3 are conserved in other eukaryotes. There is no information available regarding the function of these proteins. Interestingly, we found that eleven of them are predicted to have a U1 type ZF (Table S1 [see Additional File 1], Table 2) that contains conserved extensions on both sides of the ZF which has a HX5H spacing. They are known or suggested to be involved in RNA binding and therefore we suggest that these conserved AT-ZFPs with U1 type ZFs could be involved in RNA metabolic processes, e.g. splicing like the splicosome associated proteins of the SAP62 family (Table 2), corresponding to At2g32600 in Arabidopsis. According to our prediction we found, that other conserved AT-ZFPs with U1 type ZFs are combined with domains, like DNAJ (At1g74250), KOW (At1g55460) or G-patch (At5g26610) (Table 2), which are also known to be involved in different RNA metabolic processes (reviewed in ). Like chromatin-remodeling, many pathways of the RNA metabolism are ancient, conserved processes in eukaryotes, which is reflected by our finding that several ZFPs that are described above are evolutionarily conserved in all eukaryotic taxa from Protozoa to Mammalia (data not shown).
AT-specific ZFPs and their families
BLAST analysis resulted in the assignment of the 143 AT-specific ZFPs to eight families, six pairs and to five single occurrences. This distribution reflects the high incidence of duplication events in the Arabidopsis genome. The two largest families, named A1 and C1, contain 24 and 64 members, respectively. Together they constitute about 60% of all AT-specific ZFPs. Additional data on other AT-specific ZFP families and pairs with uncharacterized members are given in Table S1 [see Additional File 1]. The C1 family is part of subset C1. We investigated the two biggest families in more detail.
The A1 family
ZF arrays and subgroups
Conserved non-finger regions in the A1 family
Using the expectation maximization search tool MEME (see Methods) we found additional conserved sequence parts in the regions outside of the ZF domains (Figure 3). These conserved regions vary in length and are not shared among the four subgroups, with the exception of a conserved N-terminal region of 29 residues that starts with an R/K rich stretch that is common to subgroups A1a and A1b. The basic amino acids could represent a nuclear localization signal . In addition, all members of subgroup A1a contain two other conserved sequences at their C-terminus. The consensus of the first is 'SATALLQKAAQMGS', the second is characterized by the pattern 'T [R/L]DFLG [L/V]' (Figure 3). These patterns could be necessary for protein interactions or localization.
The C1 family
The C1 family represents with 64 members by far the most expanded AT-ZFP family and includes about 85% of all ZFPs in subset C1. ZFPs in the C1 family are characterized by either a single finger or a varying number (2–5) of dispersed ZFs, most of them with the conserved QALGGH sequence in their alpha-helix positions 2–7. A part of this conserved plant family was investigated in petunia and named the EPF family . Based on 21 petunia-ZFPs with two, three or four dispersed ZFs, a first systematic classification of their ZF types was described in . About 20 members of the Arabidopsis C1 family have also been described regarding their biological functions and expression characteristics [25–28]. We have subdivided family C1 according to the varying numbers of fingers as subclasses C1-1i (N = 33), C1-2i (N = 20), C1-3i (N = 8), C1-4i (N = 2) and C1-5i (N = 1).
Representatives of the different C1 subclasses
Subclass C1-2i comprises 20 members (Table S1 [see Additional File 1]). Among them are a few with known biological functions. In  the expression of four proteins, namely STZ/ZAT10 (At1g27730), AZF1 (At5g67450), AZF2 (At3g19580) and AZF3 (At5g43170) was investigated. The authors showed that all four genes are involved in the plant's water-stress response. Our analysis assigned them into one subgroup (C1-2iD) as shown in Figure 5b. This subgroup contains two additional members, At3g49930 and At5g04340 that could be functionally related to ZAT10/AZF1-3. Other representatives of the C1-2i subclass are ZAT5, 7, 11 and 12 that were studied in . As shown in Figure 5b these ZFPs were assigned to three different subgroups C1-2iA (At2g37430, ZAT11), C1-2iB (At3g46070, ZAT7 and At5g59820, ZAT12) and C1-2iC (At2g28200, ZAT5). These three subgroups contain other yet uncharacterized members. Most of them are the result of duplications for example the segmentally duplicated ZAT11 and At3g53600 or the tandemly duplicated ZAT7 (At3g46090), At3g46070 and At3g46080 (Table S1 [see Additional File 1]).
Subclass C1-3i contains eight ZFPs with three dispersed ZFs (Table S1 [see Additional File 1]). They are assigned to four different subgroups C1-3iA to C1-3iD as illustrated in Figure 5c. This figure is for clarity restricted to the alignment of their ZF helices in positions -1 to 11. The only characterized ZFP of this subclass is ZAT1 (At1g02030), a member of subgroup C1-3iA . Its sequence is very similar to the segmentally duplicated At2g45120 and At3g60580.
The only two proteins we found with four dispersed ZFs (C1-4i), At1g49900 and At5g56200, are very different in length and in their sequences. The sequences of the ZF helices are also shown in Figure 5c. Only one protein with five dispersed zinc fingers (C1-5i), At3g29340, occurs in the Arabidopsis genome. Nothing is known about the function of the four and five fingered proteins.
Classification of C1 ZFPs and evaluation of different ZF helix types
Other conserved patterns
The motif search tool MEME revealed a number of other conserved patterns in family C1 (Figure 7). Most remarkable is a leucine rich stretch at the C-terminus of almost all ZFPs in this group. This was also described for homologs in petunia . This stretch is called ERF-associated amphiphilic repression motif and is essential for repression activity [34, 35]. We found a basic stretch adjacent to all Q2-1 ZF domains of subclass C1-1i. For SUP, RBE and ZFP11 this basic stretch was already described and suggested to be either involved in DNA binding or nuclear localization (see above). We suggest that it could have a dual function and may be important for both, as it was shown for other proteins [36, 37]. Furthermore we found the motifs 'CLMLL' and 'KRKSTKR' N-terminal of Q2-2 in C1-2i and in varying places in C1-3i. The conserved stretches of basic amino acids found in different positions in ZFPs of subclasses C1-2i, 3i and 4i may also serve as nuclear localization signal. The location of all conserved patterns is shown in Figure 7.
The majority of ZFPs in A. thaliana are plant specific and not conserved in other eukaryotes. Comparisons of pairwise distances revealed that ZF domains of subsets C2 and C3 show greater pairwise distances than those of the families C1 and A1. Therefore we can conclude that ZFPs of C2 and C3 are evolutionarily older than A1 and C1 which is supported by our finding that the proportion of conserved proteins is highest in subset C3 followed by subset C2 and that many of them are involved in ancient processes such as RNA metabolism and chromatin-remodeling. Families A1 and C1 are probably the result of a recent expansion. Both families almost exclusively contain plant and AT-specific proteins which supports the notion that they are younger families.
Kubo and coworkers  investigated members of the family C1 with two, three and four fingers and suggested, based on the distribution of domains, that multi-fingered proteins in petunia are probably older than those with two fingers. Based on our more comprehensive analysis of family C1 that includes also ZFPs with a single finger, we favor the alternative hypothesis that the single and two fingered proteins are older and the three and four fingered are derived. Q2-2 and Q2-3 are conserved between Arabidopsis and petunia (where so far only one single fingered protein has been reported) and Q2-1, Q2-2 and Q2-3 are highly conserved between single and two fingered ZFPs of rice and Arabidopsis. The K-types vary between rice and Arabidopsis which could indicate that there is less selective pressure on this type of zinc finger. We suggest the following scenario: the ancestor domains evolved to Q2-1 domains and duplicated to evolve into Q2-2 and Q2-3 domains, respectively, leading to the C1-2i ZFPs. Another duplication (probably Q2-3) led to three fingered ZFPs (C1-3i) and the domains K2-1 and K2-2. Recombination and also loss of domains could have led to the different three and four fingered types we see today, but can also explain the rare occurrence of one and two fingered proteins with K-type or similar domains (Figure 7). Based on the signatures of At1g49900 (Figure 5c and 6) we conclude that it arose from the duplication of a C1-2i protein. The second four fingered protein At5g56200 probably arose from recombining proteins of the subset C1-3i. The only five fingered ZFP we found is too diverged in sequence to allow inferences about its evolution. We think that the number of the members of the respective subgroups, the distribution of Q2-2 and Q2-3 as well as the distribution of non-finger conserved motifs (Figure 7) favor the assumption of evolution from a low number to a higher number of domains and not vice versa. All main signatures we found seem to be conserved in the plant kingdom. The conservation of the signatures, especially the Q-type implies that ZF types with the same signature may recognize similar DNA sites.
DNA recognition by C1 family zinc fingers
We showed that the minority of AT-ZFPs is evolutionarily conserved and our analysis further suggests that most of them could be involved in ancient biological processes like RNA metabolism and chromatin-remodeling. The majority of AT (plant)-specific ZFPs are known or suggested to be involved in transcriptional regulation and exhibit remarkable differences in the features of their ZF sequences and ZF arrangements compared to animal ZFPs. In A. thaliana we found two major families with recent expansions, one with zinc fingers arranged in tandem (A1), the other with a varying number of dispersed zinc fingers and the plant-specific invariant QALGGH motif in the alpha-helix (C1). However, our studies showed that most ZFPs of A. thaliana have their domains arranged in a dispersed manner and not in tandem. Additionally, novel plant specific ZFP-associated domains were detected that may be involved in DNA binding or repressor functions. Our results reflect the diversity of the transcriptional regulation guided by ZFPs in plants compared to animals. Our findings on signatures in zinc finger domains of the largest family C1, and on conserved non-finger motifs give insight into the evolution of the ZFPs and will help to understand their DNA binding function.
Identification of ZFPs and of conserved ZFP-associated motifs
For the identification of the ZFPs we searched the Arabidopsis proteome (MatDB_v110103) using the HMMer package 2.1.1  and the Pfam domain ZF-C2H2 (PF00096) . The minimal cut-off for the search was chosen at a score of 0. The choice of this rather low threshold permits the detection of all ZFs/ZFPs, but also results in the detection of many false-positives. Therefore all identified ZFs/ZFPs subsequently were checked for overlaps with other protein motifs by manual inspection with Pfam and SMART  search tools and by BLAST search . Putative C2H2 hits that overlapped with more significant hits of other motifs were eliminated. Usually, questionable C2H2 hits have very low scores and do not exactly fit the spacing of the Pfam C2H2 pattern. Pfam and SMART were also used for the identification of conserved non-finger domains in the AT-ZFPs. In addition, we have applied the program "Multiple Expectation Maximization for Motif Elicitation" (MEME)  for the detection of short conserved sequence parts that have not been described yet as Pfam and/or SMART motif. The program MEME detects conserved domains (with unknown sequence) in unaligned sequences. It starts with an initial alignment which provides an estimate of the amino acid composition at each position of the respective conserved stretch that is found. The two steps that follow, the expectation and maximization steps, are applied repeatedly to finally converge to a solution that offers the best location of the motif in each sequence and an estimate of the amino acid composition of each position of the motif.
Classification of AT-ZFPs into families and subgroups
The identified AT-ZFPs were compared to the NR protein database of the NCBI in order to find evolutionarily conserved proteins. Furthermore, all against all BLAST searches of the AT-ZFPs were performed to define families and subgroups and the number of their members. ZFPs in any genome can be classified first into a few main sets based on the number, types and arrangements of their fingers as proposed earlier by us for ZFPs of the yeast genome . All ZFPs containing tandem ZFs in one array or in more than one array are assigned accordingly to sets A and B, respectively, and all ZFPs containing a single ZF or dispersed ZFs are assigned to set C. Based on the results of our statistical analysis of linker lengths in ZFPs (S.B. unpublished data) we have defined tandem ZFs as fingers linked by zero to ten amino acid residues, with five residues as the most frequent (consensus) linker length. ZFs separated by longer spacers of eleven or more residues are considered as dispersed ZFs. Our choice of the upper and lower limits of ten and eleven linker/spacer residues for tandem and dispersed ZFs may seem somewhat arbitrary. However it reflects experimental data on DNA binding ZFPs from literature, where a range of two to seven residues for the linker is given, but most frequently a consensus linker with five residues and the conserved sequence 'TGEK/RP'. ZF domains of large subfamilies were also subjected to phylogenetic analyses using ClustalX  for alignments and the PHYLIP package  for pairwise sequence distance (PAM Dayhoff matrix) and neighbor-joining analyses.
List of abbreviations
- ZFPs C2H2:
zinc finger proteins
- ZF C2H2:
- AT-ZFPs C2H2:
zinc finger proteins found in A. thaliana
We would like to thank K. FX. Mayer, A. Facius and P. Pagel for technical support and A. D. Greenwood for helpful comments on the manuscript.
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