Genome wide analysis of Arabidopsis core promoters
© Molina and Grotewold; licensee BioMed Central Ltd. 2005
Received: 11 November 2004
Accepted: 25 February 2005
Published: 25 February 2005
Core promoters are the gene regulatory regions most proximal to the transcription start site (TSS), central to the formation of pre-initiation complexes and for combinatorial gene regulation. The DNA elements required for core promoter function in plants are poorly understood. To establish the sequence motifs that characterize plant core promoters and to compare them to the corresponding sequences in animals, we took advantage of available full-length cDNAs (FL-cDNAs) and predicted upstream regulatory sequences to carry out the analysis of 12,749 Arabidopsis core promoters.
Using a combination of expectation maximization and Gibbs sampling methods, we identified several motifs overrepresented in Arabidopsis core promoters. One of them corresponded to the TATA element, for which an in-depth analysis resulted in the generation of robust TATA Nucleotide Frequency Matrices (NFMs) capable of predicting Arabidopsis TATA elements with a high degree of confidence. We established that approximately 29% of all Arabidopsis promoters contain TATA motifs, clustered around position -32 with respect to the TSS. The presence of TATA elements was associated with genes represented more frequently in EST collections and with shorter 5' UTRs. No cis-elements were found over-represented in TATA-less, compared to TATA-containing promoters.
Our studies provide a first genome-wide illustration of the composition and structure of core Arabidopsis promoters. The percentage of TATA-containing promoters is much lower than commonly recognized, yet comparable to the number of Drosophila promoters containing a TATA element. Although several other DNA elements were identified as over-represented in Arabidopsis promoters, they are present in only a small fraction of the genes and they represent elements not previously described in animals, suggesting a distinct architecture of the core promoters of plant and animal genes.
In eukaryotes, many cellular processes are regulated at the level of transcription. Initiation of transcription by RNA polymerase II requires the assembly of the basal transcription apparatus at the core promoter, a region of about 70 bp flanking the transcription start site (TSS) . Interactions mediated by components of the basal machinery and transcription factors that recognize specific cis-regulatory elements, frequently located upstream of the core promoter, ensure efficient and regulated transcription by RNA polymerase II at Class II promoters . Class II core promoters often contain conserved DNA elements recognized by components of the basal transcription machinery, the general transcription factors. The best-described core promoter DNA element is the TATA box, which is recognized by TATA-binding protein (TBP). The TATA box is a T/A-rich sequence usually located 25–35 base pairs upstream of the TSS . Recruitment of TBP and TBP-associated factors, all part of the TFIID complex, directs assembly of the pre-initiation complex (PIC), a highly regulated process that ensures precise initiation of transcription. The directionality of the PIC is likely to be provided by the presence of another conserved element, present in a large fraction of Class II promoters, the BRE (IIB recognition element) [4, 5]. In addition, Initiator (Inr) elements are often present at the site of initiation of transcription in a number of eukaryotic core promoters. The Inr is a loosely conserved element containing an adenosine at the TSS and a C as the nucleotide preceding it (position -1), surrounded by a few pyrimidines . The function of the Inr and the components of the basal transcription machinery that recognize this element remain poorly defined.
In spite of the availability of a large number of computational programs that predict the presence of plant genes and their architecture (reviewed in ), accurately identifying core promoters solely based on genome sequence analysis remains a daunting task. Although no known DNA-sequence motif is present in all plant core promoters, TATA and Inr motifs represent two elements that are often present . A main limitation in the analysis of plant core promoters is the insufficient amount of information available regarding TSSs, and hence the location of core promoters in genomic sequences. Over the past few years, several efforts have initiated the high-throughput production and analysis of full-length (FL) Arabidopsis cDNAs [8, 9]. These FL-cDNAs have dramatically improved the annotation of the Arabidopsis genome , providing a powerful tool for the identification and analysis of core promoter elements.
Here, we describe the analysis of core promoters of ca. 12,750 Arabidopsis genes, using publicly available FL-cDNA sequences. Our objectives for this study were to i) identify motifs characteristic of Arabidopsis core promoters; ii) determine how often Arabidopsis core promoters contain a TATA box, and iii) compare the architecture of Arabidopsis core promoters with those of Drosophila, the only higher eukaryote for which such a genome-wide analysis has been performed. We examined the presence, distribution and consensus sequence of conserved motifs proximal to the TSS. In addition to TATA elements, we identified several other motifs, primarily representing microsatellite elements, some of them overrepresented in particular regions of core promoters. Using Nucleotide Frequency Matrices (NFM), we carried out a genome-wide analysis for the presence and position of TATA-box elements. Our studies show that only about 29% of all Arabidopsis genes contain a recognizable TATA element. The position of the TATA motif with respect to the TSS and correlations between the presence of a TATA with EST abundance and 5' UTR lengths are discussed.
Results and discussion
Obtaining core promoter and 5' UTR sequences for 12,749 Arabidopsis genes
As a first step towards identifying core Arabidopsis promoters, we queried TAIR's Gene Search with the condition of a FL-cDNA entry. We retrieved a total of 13,964 non-redundant hits, derived from over 28,000 total FL-cDNAs deposited at TAIR. The locus Ids for these 13,964 FL-cDNAs was used to retrieve the 5' UTR corresponding to 12,749 genes. The remaining 1,215 genes for which a 5' UTR was not retrieved corresponded to FL-cDNAs that differed between the annotations at TAIR and TIGR, sequences for which no 5'UTR was annotated or sequences with 5' UTR regions corresponding to alternative gene models.
The [-500, -1] and [-50, -1] regions of all 12,749 genes was directly retrieved from the TAIR 500 bp upstream dataset. To obtain the [+1, +50] regions, we first checked the length of the 5' UTRs, which was shorter than 50 bp for 2,649 genes and which was interrupted by introns in 2,179 genes. To include into our analyses these cases, three different strategies were followed. If the 5' UTR was longer than 50 bp, and no introns were present in the corresponding [-50, -1] region (10,100 genes), a direct retrieval of the [+1, +50] region was performed from the TAIR 5' UTR dataset. If the 5' UTR was shorter than 50 bp and no intron interrupted this region (2,617 genes), we extended the 5' UTR to 50 nt with a fragment of the immediately adjacent downstream coding sequence using the TIGR cDNA dataset. Finally, if the 5' UTR was shorter than 50 nt and an intron interrupted this region (32 genes), we manually retrieved the [+1, +50] region from the genomic sequence using TAIR's SeqViewer. After these analyzes, we were able to generate datasets corresponding to the [-500, -1], [-50, -1] and [+1, +50] regions from a total of 12,749 genes. These datasets were used for all the subsequent analyzes in this study.
Identification of conserved motifs in core promoters
Overrepresentation of motifs in the [-50, -1] or [+1, +50] regions
Motif frequency in the [-50, -1] and [+1, +50] regions of 12,749 Arabidopsis genes compared to background models
Motifs 3 and Motifs 7 showed a clear Overrepresentation in the [-50, -1] interval. Motif 3 has all the characteristics of a TATA box (Figure 1), and was detected in 1,899 genes using the NFM, representing approximately 15% of all the genes investigated. A more detailed characterization of this motif is described below. Motif 7 was detected in a much smaller number of genes (153), and the corresponding motif with the A A/G GCCCA T/A consensus was shown before to be overrepresented in upstream regions versus coding regions of Arabidopsis genes . Consistent with our findings that show an increased accumulation of this motif towards the left border of the [-50, -1] interval (Figure 1), this motif was previously shown to have a strong positional preference for the [-250, -50] interval . Interestingly, in Arabidopsis this motif is associated with dark-induced genes and is over-represented in genes under circadian regulation .
Three motifs were also found to be overrepresented in the [+1, +50] region. Motif 10 resembles the (GAA)n microsatellite represented at least two fold higher in the [+1, +50] region, compared to the [-50, -1] or the [-500, -450] regions (Table 1). This overrepresentation cannot be explained by the modest difference in nucleotide composition between these regions, consistent with the comparable distribution in the randomly simulated datasets (Table 1). As described above, 2,649 of the [+1, +50] regions contain coding regions in addition to short 5' UTRs. To investigate whether the coding sequences contributed to the overrepresentation of this motif, we analyzed the presence of this motif in the 10,100 [+1, +50] "clean" 5'UTR regions, which do not contain any coding or intron sequences (shown between brackets in Table 1 under [+1, +50] Real). In these 10,100 sequences, Motif 10 was found in 340 [+1, +50] sequences, the same frequency as in the original dataset (519/12,749). Thus, this (GAA)n microsatellite is overrepresented in the [+50, +1] region, irrespective of whether it is coding or 5' UTR. (GAA)n microsatellites have been extensively researched in humans , but not yet associated with any functional role in Arabidopsis.
Motif 13, with the consensus T/A CCGGCGA (Figure 1), was detected by both MEME and AlignACE only in the [+1, +50] region (Table 1). This motif, however, was not identified as the binding site for any known transcription factor, as deduced from searching the PLACE , TRANSFAC  and AGRIS  databases (not shown).
Finally, Motif 11, present in a significant number of sequences (Figure 1), fits the Kozak consensus (ACCATGG) for a translation start ATG codon . Consistently, 1,139 out of the 1,352 sequences in which we found Motif 11 have a short 5' UTR, reflected in that this motif is present in just 213 5' UTR [+1, +50] sequences (Table 1). While this motif is irrelevant to our analysis, it provides a good internal control regarding the sensitivity and comprehensiveness of our search for motifs in the [-50, -1] and [+1, +50] regions.
Motifs 1, 2, 4, 6, and 9 correspond to microsatellites commonly found in Arabidopsis , displaying similar frequency distributions in the [-50, -1] and [+1, +50] regions. From these 5 motifs, only Motif 2 does not seem to be significantly overrepresented in these two regions, when compared to the [-500, -450] sequences (Table 1). The potential participation of microsatellites in the control of gene expression is unclear, but according to recent studies in rice and Arabidopsis, their distribution may follow a gradient in the direction of transcription . Motif 8 conforms to a (CG)n microsatellite, frequent in monocots such as rice, but not often found in Arabidopsis , which is consistent with a low but comparable frequency in all three regions studied here (Table 1). The apparent higher frequency of Motif 8 in the [+1, +50] region, compared to the [-50, -1] (421 versus 282, respectively), is likely to correspond to an increased G/C content of the 5' UTR (see Methods), as reflected by the increased distribution of this motif in a random simulation of sequences with the same nucleotide composition of the corresponding [+1, +50] region (Table 1). Motif 9, corresponding to a (CA)n microsatellite (with n = 5), was found to be only slightly overrepresented in the [-50, -1] region, compared to the [-500, -450] background model (Table 1). Interestingly, however, this motif is significantly clustered in the [-35, -10] region (Figure 1). A similar clustering was not observed in the [+1, +50] region, where this motif is significantly overrepresented, compared to the background models (Table 1).
Motif 5, with the consensus sequence AAACCCTA (Fig. 1), and similarly overrepresented in the [-50, -1] and [+1, +50] regions, compared to the random or [-500, -450] background models (Table 1), does not conform to a typical microsatellite sequence. Interestingly, however, the sequence of Motif 5 is precisely the reverse complement of Motif 12, which with the TAGGGTTT DNA-consensus fits the sequence of the Arabidopsis telomeric sequence , and of the telobox, the binding site for a MYB-related telomeric DNA-binding protein previously described in proteins from yeast, plants and animals . This element, present in the 5' UTR or promoter region of many genes encoding products associated with the translational apparatus , was also shown to participate in the expression of Arabidopsis root meristem genes . Our analysis suggests that the number of sequences containing the telobox motif in either the forward or reverse-complement configuration is much larger than previously reported . Consistent with previous studies , only a few genes (8) contain Motif 5 or 12 in both the [-50, -1] and [+1, +50] regions.
We also investigated for the presence of motifs previously shown to be overrepresented in the [-60, +40] regions of Drosophila core promoters . Using the corresponding NFMs, we searched our databases for DRE (DNA-replication related element) and DPE (downstream promoter element), usually found ~30 nt downstream of the TSS [25, 26]. Although the [-60, +40] region is shifted 10 bp towards the 5' end from our selection, the positional clustering of the DRE and DPE motifs  still falls under the [-50, +50] region investigated here. In our analyses, neither one of the two motifs was represented at a level significantly higher than in the random models (not shown). A CCAAT box NFM  did not result in any significant distribution change between real and randomly generated datasets for both regions (not shown). This was expected because CCAAT boxes usually cluster around the -75 position , which is outside of the [-50, +50] interval investigated here, corresponding to what is generally recognized as the core promoter region. Similarly, none of the motifs identified here appeared to correspond to Inr elements. We conclude that, with the exception of the TATA box, the elements involved in the architecture of core promoter in Arabidopsis and Drosophila are overall different.
Distribution of TATA motifs in core Arabidopsis promoters
Frequency of TATA frequency in the [-50, -1] and [+1, +50] regions of 12,749 Arabidopsis genes compared to background models
TATA NFM derived from 1,899 motifs.
Derived from MEME
TATA NFM derived from 3,679 motifs.
Derived from PlantProm
The new NFMs were used to scan the [-500, -1] region and establish where each of them localized a TATA with the highest probability. As shown in Figure 2A, both NFMs showed a significant peak in the [-50, -25] region, consistent with the position expected for TATA elements. To establish the average distance of TATA elements to the TSS, the MEME and PlantProm TATA NFMs were used to scan the 12,749 [-50, -1] regions and the positions of the corresponding TATA boxes were recorded and graphed (Figure 2B). The average distance of a TATA (position 1 in Tables 3 and 4) to the TSS is 31.7 nt (indicated with a green line in Figure 2B). Thus, the position of the TATA box in Arabidopsis is more similar to what is typically the case in animal promoters, usually 25–30 nt from the TSS  than what is found in yeast, where the TATA box has a variable position in the [-100, -40] region .
Understanding the architecture of core promoters is central to establishing the mechanisms by which the basal transcriptional machinery assembles and facilitates formation of the pre-initiation complex. We provide here the first genome-wide analysis of Arabidopsis core promoters. We have identified several motifs overrepresented in core promoters, with respect to background models consisting of random sequences of identical nucleotide composition or intergenic regions. With the exception of microsatellites similarly distributed in the [-50, +1] and [+1, +50] regions and the TATA element, for which an in-depth analysis was carried out, most other overrepresented motifs were present in only a small subset of the sequences analyzed. Our studies provide robust NFMs corresponding to TATA elements and other conserved motifs, and show that only 29% of all Arabidopsis promoters contain a TATA element located in average approximately 32 nt upstream of the TSS. The absence of a TATA correlates with a lower representation of the corresponding gene in public EST collections as well as with longer 5' UTR sequences. However, the absence of a TATA is not compensated for by the overrepresentation of any one of several motifs present in Drosophila core promoters, suggesting significant differences in the organization of core promoters from animals and plants.
Retrieval of core promoter and 5' UTR sequences
To obtain the sequences of the region of promoters spanning the first 500 nt upstream of the TSS [-500, -1] and the corresponding 5' UTRs, we used the TAIR Gene Search web tool . The TAIR database was queried for all genes having a full-length cDNA (FL-cDNA) entry. The corresponding 5' UTR and the [-500, -1] regions datasets were downloaded from TAIR , last updated on February 28, 2004. The FL-cDNA sequences were obtained from the June 10, 2004 realese of the TIGR's cDNA dataset . The locus Ids of the gene queries were checked against the 5' UTR, [-500, -1] and FL-cDNA files to reject erroneous annotations. We divided the 100 bp region flanking the TSS in upstream [-50, -1] and downstream [+1, +50] sub-regions of 50 bp each. The [-50, -1] and [+1, +50] intervals of the confirmed genes were directly retrieved from the downloaded TAIR files, when possible. In those cases when the 5' UTR region was shorter than 50 bp, the TIGR file was used to extend the region to the necessary length by appending a fragment of the immediately adjacent coding sequence. When an intron interrupted the 5' UTR, we manually extracted the 50 bp region from the Arabidopsis genomic sequences using the SeqViewer tool at TAIR.
Motif discovery and motif search
To characterize core promoters, we first investigated features represented by conserved regions or motifs. From several algorithms available , we chose the expectation maximization method MEME (version 3.0.8)  and the Gibbs Sampling method AlignACE . MEME and AlignACE were run for the [-50, -1] and [+1, +50] regions separately for the entire set of genes. For MEME, a fixed minimum motif length of 5 and a maximum of 10 was set and 20 motifs were requested using the zero or one occurrence per sequence model. For AlignACE, only the background fractional GC content of the input sequences was supplied, and all the other parameters were left at default values. MEME and AlignACE were run in the Itanium 2 Cluster at the Ohio Supercomputer Center. The results obtained with MEME were compared with those obtained with AlignACE. Motifs consisting of single nucleotide repeats (i.e. An) were manually parsed out independent of the number of occurrences or positional preferences. The obtained motifs were plotted according to their positions within the regions and their consensus sequences were graphed using WebLogo version 2.7 .
To find pre-defined motifs in the [-50, -1] and [+1, +50] regions, we used the higher order probabilistic model MotifScanner from MotifSampler version 3.0 . The searches were fed with the nucleotide frequency matrices (NFMs) of the selected motifs obtained from the MEME search, and a background model of order 1 accounting for single- and di-nucleotide distributions for each set. The prior probability of finding one instance of the motif was left to the default value of 0.2. We also ran the motif search with elements conserved in core promoters of other organisms. The first two corresponded to the TATA and CCAAT elements obtained as NFMs from PlantProm . The other two corresponded to the Downstream Promoter Element (DPE) and the DNA-replication Related Element (DRE) described for Drosophila core promoters . For these new four elements, we performed the same analysis as described before, using the [-50, -1] and [+1, +50] region datasets and the corresponding randomly generated dataset.
Generation of random sequence models
After establishing that the distribution of nucleotides in the Arabidopsis [-50, -1] and [+1, +50] regions are ~65% A/T to ~35% C/G and ~61% A/T to ~39% C/G, respectively, a pseudo-random set of 50 bp sequences was generated for each region to be tested with the matrices as a way of determining the chances of finding the motifs candidates in a stochastic environment. This information was then used together with the search results obtained from the real data to support the confidence of the findings.
Analysis of TATA elements
For the analysis of the TATA motif, the TATA NFM previously described  was used against the NFM reported by our own motif search. Using MotifScanner, the distribution of TATA elements in the upstream vicinity of the TSS was investigated. After determining the location of the putative TATA motifs in the [-50, -1] region, the NFMs were retrained with the new retrieved TATA motifs.
Analysis of gene ontology and expression level based on EST abundance
To determine whether the occurrences of the discovered motifs were associated with specific gene functions or products we retrieved the Arabidopsis Gene Ontology Database  (last update July 20, 2004) and correlated the annotated molecular function, biological process or cellular component of Arabidopsis genes with the ones found in the motif clusters. Under the assumption that the contribution of a gene to transcription activity is related to the number of its detected ESTs, we downloaded a dataset from TAIR that accounts for the number of ESTs submissions per locus  (last update July 23, 2004). With this, we then established the relative expression levels based on the ratio of the genes containing a particular motif and the overall EST frequency per gene.
List of abbreviations
expressed sequence tag
nucleotide frequency matrix
translations start site 5' UTR, 5' untranslated region
The analysis of plant promoters is supported in part by grants MCB-0210413 and MCB-0418891 (to E.G.) from the National Science Foundation and by a seed grant from the Ohio Supercomputer Center. We appreciate helpful comments on this manuscript by Nicole Matthews, Ralf Bundschuh, George Heine, Marcela Hernandez and Rebecca Lamb. We thank Uwe Ohler for sharing with us the position probability matrices for motifs overrepresented in Drosophila core promoters.
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