Distribution of short interstitial telomere motifs in two plant genomes: putative origin and function
© Gaspin et al; licensee BioMed Central Ltd. 2010
Received: 23 December 2009
Accepted: 20 December 2010
Published: 20 December 2010
Short interstitial telomere motifs (telo boxes) are short sequences identical to plant telomere repeat units. They are observed within the 5' region of several genes over-expressed in cycling cells. In synergy with various cis-acting elements, these motifs participate in the activation of expression. Here, we have analysed the distribution of telo boxes within Arabidopsis thaliana and Oryza sativa genomes and their association with genes involved in the biogenesis of the translational apparatus.
Our analysis showed that the distribution of the telo box (AAACCCTA) in different genomic regions of A. thaliana and O. sativa is not random. As is also the case for plant microsatellites, they are preferentially located in the 5' flanking regions of genes, mainly within the 5' UTR, and distributed as a gradient along the direction of transcription. As previously reported in Arabidopsis, a conserved topological association of telo boxes with site II or TEF cis-acting elements is observed in almost all promoters of genes encoding ribosomal proteins in O. sativa. Such a conserved promoter organization can be found in other genes involved in the biogenesis of the translational machinery including rRNA processing proteins and snoRNAs. Strikingly, the association of telo boxes with site II motifs or TEF boxes is conserved in promoters of genes harbouring snoRNA clusters nested within an intron as well as in the 5' flanking regions of non-intronic snoRNA genes. Thus, the search for associations between telo boxes and site II motifs or TEF box in plant genomes could provide a useful tool for characterizing new cryptic RNA pol II promoters.
The data reported in this work support the model previously proposed for the spreading of telo boxes within plant genomes and provide new insights into a putative process for the acquisition of microsatellites in plants. The association of telo boxes with site II or TEF cis-acting elements appears to be an essential feature of plant genes involved in the biogenesis of ribosomes and clearly indicates that most plant snoRNAs are RNA pol II products.
Regulatory sequences constitute a small fraction of eukaryotic genomes that determine the level, location and chronology of gene expression. In parallel to functional studies, computational analysis provides different approaches for scanning genomic sequence to identify those regions predicted to participate in gene regulation [1, 2]: (i) sequence analysis of co-regulated genes within a given species, (ii) inter-species sequence comparison of orthologous genes and (iii), database construction and analysis of known transcription-factor binding sites.
Functional studies conducted to identify trans and cis-acting elements controlling the expression of translation factors and ribosomal proteins (rp) in Arabidopsis allowed us to characterize several cis-acting elements. One of them, the telo box (AAACCCTA), was first observed within the promoter of the four Arabidopsis genes encoding the translation elongation factor EF1αpromoters [3, 4] and subsequently within a few plant rp promoters . This short motif is identical to the repeat (AAACCCT)n of plant telomeres  but differs from long interstitial telomere repeats (ITRs) which are found at discrete intrachromosomal sites in many eukaryotic species [7, 8] and probably result from chromosomal rearrangements such as end-fusions and segmental duplications. In contrast to the limited number of ITRs observed in pericentromeric and subtelomeric regions in Arabidopsis , a preliminary computational analysis suggested that short telomere repeats (telo boxes) were over-represented at the 5' end of Arabidopsis ESTs . More recently, with the achievement of the Arabidopsis sequencing project, we showed that the occurrence of telo boxes within rp promoters is the rule rather than the exception [10, 11]. Telo boxes were also observed in promoters of several protein-encoding genes which, as is the case for rp, are expected to be over-expressed in cycling cells, suggesting that it could be involved in the coordinated expression of this class of genes. Experimental data indicated that the telo box was indeed involved in the expression in cycling cells [11–13]. However, by itself this motif is not able to activate the transcription by RNA pol II but acts in synergy with various cis-acting elements to increase the expression. These cis-acting elements include the TEF1 box identified in promoters of the translation elongation factor EF1α, the Trap1 box in the promoter of a rp gene  and redundant site II motifs initially characterized in the promoter of the proliferating cellular nuclear antigen gene (PCNA)  and subsequently in most Arabidopsis rp genes .
In this study, we analysed the distribution of telo boxes within A. thaliana and O. sativa genomes and their association with genes involved in the biogenesis of the translational apparatus. In addition, this analysis revealed a striking analogy with the genomic distribution of telo boxes and plant microsatellites.
Definition of the telo box and distribution in different genomic regions
Distribution of telo boxes in A. thaliana and O. sativa genomes
Telo Freq. (nb/Mb)
Comparative distribution of telo boxes and microsatellites
Distribution of telo boxes, microsatellites and Y Patch in 5' and 3' UTR in A. thaliana and O. sativa
3' UTR (number)
5' UTR frequency counts/Mb
3' UTR frequency counts/Mb
Telo boxes in the promoters of plant genes involved in ribosome biogenesis
In addition to ribosomal proteins, the biogenesis of cytoplasmic ribosomes also requires the biosynthesis of 5.8 S, 18 S and 25/26 S rRNAs, a process which is achieved by the transcription of rDNA and by endo- and exonucleolytic cleavages and extensive modifications of an rRNA precursor (pre-rRNA). Small nucleolar RNAs (snoRNAs), in association with specific nucleolar proteins (SnRNP), are involved in this process.
Summary of the analysis of 5' flanking regions of A. thaliana and O. sativa snoRNA genes
telo box - sites II
telo box - TEF
Intronic snoRNA clusters
Intronic orphan snoRNAs
Intergenic snoRNA clusters
Intergenic orphan snoRNAs
Intronic snoRNA clusters
Intronic orphan snoRNAs
Intergenic snoRNA clusters
Intergenic orphan snoring
Identification of cryptic promoters by using the conserved topological association of telo boxes with cis-acting elements
Biogenesis of ribosomes is a crucial process requiring the coordinate expression of hundreds of genes. In the yeast Saccharomyces cerevisiae this synchronized expression is primarily accomplished at the transcriptional level and mediated through common upstream activating sequences including in most cases Rap1p binding sites (rpg boxes) and, in a small subset of rp genes, Abf1p binding sites [38, 39]. In higher eukaryotes little is known about the transcriptional network controlling this regulon . Studies conducted in our group over the last two decades have led to the identification of several transcriptional trans and cis-acting elements which participate in the over-expression of translational factor and rp genes in dividing plant cells [3, 11, 12, 14, 41]. The data reported in the present work suggest that the occurrence of telo boxes in the 5' flanking regions of rp genes is the rule not only in Arabidopsis but in angiosperms in general and therefore extend this observation to genes involved in the maturation of pre-rRNA. In agreement with data coming from a genome-wide analysis suggesting that the sequences AAACCCTA and TAGGGTTT are Arabidopsis core promoter elements , the majority of telo boxes observed in 5' flanking regions of plant translation-related genes are located within a narrow window located -50 to +50 relative to the transcription start site (TSS). The conservation of a topological association between telo boxes and site II motifs or TEF box cis-acting elements provides insights into the transcriptional regulation process required for the coordinate expression of plant genes involved in ribosome biogenesis. For several aspects, a parallel can be drawn between the putative role of telo boxes in plants and those achieved by the rpg cis-acting element in the yeast S. cerevisiae: (i) the rpg boxes (ACACCCAYACAY) show an homology with yeast telomere repeats (C(1-3)A)n and are both targets for the Rap1p pleiotropic protein involved in telomere metabolism and gene expression ; (ii) a common characteristic of yeast genes under the control of rpg boxes is their very high transcription rate during exponential growth. Up to now, the effect of telo boxes on expression was only observed in exponentially-growing cell cultures or in cycling cells of root primordia and young leaves [11–13]; (iii) among the yeast genes up-regulated in an rpg-dependent manner during exponential growth, genes involved in the biogenesis of ribosomes constitute a major class [38, 43, 44]; (iv) the interaction of Rap1p with the rpg box does not directly act as transcriptional activator but instead as a synergistic element that allows the activation by other regulatory proteins in participating in their recruitment in protein-protein interactions or in destabilizing the DNA duplex [38, 45, 46]. Similarly, in gain-of-function experiments, the telo box is not able by itself to activate gene expression in transgenic plants but acts in synergy with other cis-acting elements like site II motifs or TEF boxes [11, 12]. Taken together, these observations support the hypothesis that there are functional similarities between the roles played by interstitial telomere motifs in plant promoters and those of the rpg box in yeast. We have estimated at about 10% the number of Arabidopsis genes harbouring a telo box within their 5' flanking regions suggesting that this element plays a much more general role than solely in the ribosome biogenesis. An intriguing question which might consequently be addressed concerns the meaning of the involvement in both yeast and angiosperms of interstitial telomere motifs in the expression of a set of genes whose expression is, at least for translation-related genes, correlated to cellular proliferation.
In contrast to that observed in vertebrates, many plant snoRNA genes are found in polycistronic clusters composed of homologous or heterologous snoRNAs . Intronic snoRNA genes are frequently found in the genome of rice [26, 27] whereas they are the exception in Arabidopsis . There is currently little information on how the expression of plant snoRNA genes is coordinated with the expression of other components involved in the biogenesis of the translational apparatus. When nested within introns of genes involved in ribosome biogenesis such as fibrillarin SnRNP genes in Arabidopsis or several rp genes in O. sativa the co-expression process appears to be obvious. This co-expression process is much less clear when snoRNAs are expressed from independent promoters in non-intronic genes. Some plant non-intronic snoRNAs are RNA polymerase III products as suggested in Arabidopsis and rice by the characterization of dicistronic tRNA-snoRNA genes [47, 49]. However, it remains to assess the proportion of non-intronic snoRNAs that are transcribed by pol III in plants. Our data suggest that, at least in Arabidopsis, this is probably the exception rather than the rule. The remarkable conservation of the topological association of telo boxes with site II motifs or TEF boxes observed in promoters of genes encoding ribosomal proteins or proteins required for pre-rRNA processing as well as within sequences found upstream of non-intronic snoRNA genes, strongly suggests that the association of these cis-acting elements and their interaction with related trans-acting factors might play a fundamental role in their coordinated transcription by RNA pol II. Moreover, we took advantage of the availability of TIGR-CERES data on the sequencing of full length Arabidopsis cDNAs to map the 5' end of several snoRNA precursors (Additional Files 3 and 4). These full-length cognate cDNAs were obtained by the "cap-trapping" method indicating that the identified RNA precursor molecules harbouring snoRNAs are indeed capped and polyadenylated RNA pol II transcripts. Once again, and as for rp genes, a parallel can be drawn between the putative role played by the telo box in plants and those achieved by the yeast rpg box in snoRNA gene expression. In S. cerevisiae the promoters of non-intronic snoRNA genes contain rpg boxes which are required for their full expression . Thus, the analysis of conserved associations of telo boxes with site II motifs or TEF boxes allowed us to characterize new RNA pol II promoters involved in the biosynthesis of snoRNA precursors. A first analysis suggest that such an approach could be generalized to identify unexpected cryptic RNA pol II promoters within plant genomes (Figure 7). It would be of interest to investigate to what extent such promoters participate in the activation of expression in meristematic cycling cells, as is the case for plant rp or pre-rRNA processing genes showing a similar promoter configuration.
The data reported in this work support the model previously proposed for the way telo boxes spread within plant genomes and provide new insights into a putative process for the acquisition of microsatellites in plants. The conserved topological association of telo boxes with site II or TEF1 cis-acting elements appears to be an essential feature of plant genes involved in the biogenesis of ribosomes and clearly indicates that most plant snoRNAs are RNA pol II products. This conserved association could provide a powerful tool to improve genome annotation in characterizing new cryptic RNA pol II promoters.
Sequence data sources
Analysis of Arabidopsis sequences was carried out using the TAIR9 datasets http://www.arabidopsis.org. The analysis conducted by using the TAIR9 5'UTR (DNA) and the TAIR9 3' UTR (DNA) datasets does not include the sequences of putative introns within the 5' or 3' flanking non coding regions. The Arabidopsis rRNA processing protein and snoRNA genes were obtained from TAIR.
The O. sativa genome annotation data version 5 was downloaded from the Rice Genome Annotation Project database http://rice.plantbiology.msu.edu/. The "all.UTR" file containing the UTR sequences for 34793 gene models of the 12 pseudomolecules was used. The sequence of 5' flanking regions of rice ribosomal protein gene were extracted from the Ribosomal Protein Gene database http://ribosome.miyazaki-med.ac.jp/. The list of putative rice snoRNA and accession numbers were obtained from the literature . For each rice snoRNA, we extracted the Genbank sequence by using its accession number. All the snoRNA were searched for in the complete genomic sequence of Oryza sotiva by using NCBI Blastn with default parameters. Some of the clusters of snoRNA were obtained from the NCBI nucleotides database and were used to assign snoRNA to clusters. Others were assigned by using their chromosomic location and their positions on the chromosome. 60 clusters (instead of 68 given in Chen et al. ) were assigned to chromosomic loci thanks to the list of snoRNA given for each cluster. We also proposed some new clusters. For clusters 35, 36 and 37, it was not possible to assign snoRNA to clusters precisely. Nor was it possible to assign each sequence to a chromosomic region in the complete sequence of Oryza sotiva. Indeed, for some of the snoRNA we did not find significant similarities to anything in the entire genome of Oryza. sativa.
The command line version of the PatMatch software  was used to scan the different compartments of the genome for the presence of several nucleotide patterns: telo box (AAACCCTA) and 6 associated permutations of the telo box motif (AACCCTAA, ACCCTAAA, CCCTAAAC, CCTAAACC, CTAAACCC and TAAACCCT); a control sequence (AAACCTCA), and 6 associated permutations (AACCTCAA, ACCTCAAA, CCTCAAAC, CTCAAACC, TCAAACCT and CAAACCTC); the site II motifs (TGGGCY); the TEF1 box (ARGGRYNNNNNGYA); the (GCC)6 and (GAA)6 microsatellite motifs; and the (Y)18 pyrimidine block.
For protein coding genes, a region of 500 nt was scanned upstream of the translation initiation codon. In the case of snoRNA genes, for each cluster found in an ORF, a region of 1000 nt was extracted in the 5' region before the ATG of the host gene. For each cluster found in an intergenic region, 1000 nt were extracted before the beginning of the first snoRNA of the cluster. For individual snoRNA, a region of 1000 nt was extracted just before the beginning of the 5' region of the mature snoRNA.
The expected frequency of telo-box motif in each genome compartment under the assumption of a uniform distribution in the genome was determined as the ratio of each compartment size to the genome size. For each compartment, a chi-square test was performed between observed and expected counts of telo-box motif as compared to observed and expected counts in the rest of the genome. A combined chi-square test was performed as the sum over compartments of the square of the difference between observed and expected counts divided by expected count.
Mapping of cDNA
Putative transcripts located downstream of associations of telo boxes with site II motifs or TEF1 boxes were characterized by using sequences located downstream of these associations, Blastn and A. thaliana GB experimental cDNA/EST or Green Plant GB experimental cDNA/EST datasets.
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