Distribution of short interstitial telomere motifs in two plant genomes: putative origin and function

Abstract

BackgroundShort 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.ResultsOur 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.ConclusionsThe 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.

Complementary Activities of TELOMERE REPEAT BINDING Proteins and Polycomb Group Complexes in Transcriptional Regulation of Target Genes

“…Consistent with previous reports on the coincidence of site II motifs and teloboxes (Tremousaygue et al, 2003;Gaspin et al, 2010), we found ribosomal protein genes overrepresented among direct TRB1 target genes ( Figure 4B). In addition, while tRNA and snoRNA genes were marginally enriched among the targets, a subset of intron-containing tRNA genes was strongly overrepresented ( Figure 4B).…”

“…Teloboxes (AAACCCTA) are related to telomeric repeats (CCCTAAA 3 n; n = 2-1000+), which were previously shown to bind TRB1 in vitro (Schrumpfova et al, 2004;Hofr et al, 2009). The presence of teloboxes enhances the effect conferred by site II motifs but is not sufficient to drive expression from a minimal promoter on its own (Tremousaygue et al, 2003;Gaspin et al, 2010). Cluster 5 was indeed enriched for ribosomal genes, corroborating the previous link to site II motifs.…”

“…It has been speculated that these evolve rapidly from interstitial telomere repeats, which form by the invasion of chromosomal ends into extratelomeric regions (Gaspin et al, 2010). In any case, it seems that the connection of telomere-derived cis-elements and cognate transcription factors with genes encoding proteins involved in primary cellular functions is an ancient one, although the outcome on gene regulation can be quite different from the one reported in plants (Ye et al, 2014).…”

“…Cluster 5 was indeed enriched for ribosomal genes, corroborating the previous link to site II motifs. However, teloboxes, although present, were not overrepresented in the corresponding promoter set, which could be due to the high incidence of teloboxes among all Arabidopsis promoters used as a background in the enrichment analysis (Tremousaygue et al, 2003;Gaspin et al, 2010). Cluster 5 contained the most highly expressed gene set ( Figure 3A), which was expressed at lower levels in the trb1-1 and trb1-1 lhp1 background.…”

Chromosome Evolution in Dendropsophini (Amphibia, Anura, Hylinae)

“…However, there are diverse mechanisms that explain the origin of ITSs other than chromosomal rearrangements and need to be briefly considered here. These include the amplification of the oligonucleotide (TTTAGGG) n associated to heterochromatin extension, mutations, transposition or unequal crossing-over, or the acquisition of ITSs related to transcriptional processes associated to the DNA repair machinery [Tsipouri et al, 2008;Carvalho et al, 2009 and references therein;Ventura et al, 2009;Gaspin et al, 2010].…”