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Early evolution of histone mRNA 3' end processing - PubMed

Early evolution of histone mRNA 3' end processing

Marcela Dávila López et al. RNA. 2008 Jan.

Abstract

The replication-dependent histone mRNAs in metazoa are not polyadenylated, in contrast to the bulk of mRNA. Instead, they contain an RNA stem-loop (SL) structure close to the 3' end of the mature RNA, and this 3' end is generated by cleavage using a machinery involving the U7 snRNP and protein factors such as the stem-loop binding protein (SLBP). This machinery of 3' end processing is related to that of polyadenylation as protein components are shared between the systems. It is commonly believed that histone 3' end processing is restricted to metazoa and green algae. In contrast, polyadenylation is ubiquitous in Eukarya. However, using computational approaches, we have now identified components of histone 3' end processing in a number of protozoa. Thus, the histone mRNA stem-loop structure as well as the SLBP protein are present in many different protozoa, including Dictyostelium, alveolates, Trypanosoma, and Trichomonas. These results show that the histone 3' end processing machinery is more ancient than previously anticipated and can be traced to the root of the eukaryotic phylogenetic tree. We also identified histone mRNAs from both metazoa and protozoa that are polyadenylated but also contain the signals characteristic of histone 3' end processing. These results provide further evidence that some histone genes are regulated at the level of 3' end processing to produce either polyadenylated RNAs or RNAs with the 3' end characteristic of replication-dependent histone mRNAs.

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Figures

FIGURE 1.
FIGURE 1.

Phylogenetic distribution of components involved in histone 3′ end formation. The distribution of identified stem–loop motifs in regions downstream from histone coding sequences are shown as well as SLBP, U7 RNA, Lsm10, and Lsm11. In the case of histones, “H” indicates that a histone downstream sequence was identified but no stem–loop motif. Shaded boxes represent cases in which a histone downstream sequence including a stem–loop motif was identified, and empty boxes are cases in which no histone or histone downstream sequence at all could be identified. For the SLBP, a “P” indicates that the available protein sequence covers only the RNA-binding domain. In instances where a genus name only is indicated, multiple species were analyzed: C. elegans and Caenorhabditis briggsae; Phytophthora infestans and P. sojae; C. hominis and C. parvum; Plasmodium berghei, Plasmodium chabaudi, P. falciparum, and Plasmodium yoelii; T. annulata and T. parva; Leishmania infantum and Leishmania major; Trypanosoma brucei and T. cruzi; Candida albicans, Candida glabrata, and Candida tropicalis.

FIGURE 2.
FIGURE 2.

Selected stem–loop motifs of metazoa and protozoa. Selected stem–loop motifs of H3 and H4 histone genes were manually aligned. A more comprehensive collection of sequences are in the Supplemental Material Document 3. Potential HDE regions are shown in boldface, and the number following the species name is the distance between the stop codon and the first nucleotide of the conserved stem–loop motif. Regions in stem–loop motifs that are identical in a group of alveolates are shown with a shaded background. Full species names are in Figure 1.

FIGURE 3.
FIGURE 3.

Conserved features of histone stem–loop motifs. Sequence logos of histone SL motifs in (A) metazoa and in (B) protozoa. (C) Conserved bases in the stem–loop motif are shown in the context of the secondary structure; the most highly conserved positions are shown with a black background.

FIGURE 4.
FIGURE 4.

Conserved RNA-binding domain of SLBP homologs. Multiple alignment of stem–loop binding protein (SLBP) homologs was produced with T-Coffee (Notredame et al. 2000) and visualized with Jalview (Clamp et al. 2004). Full species names are in Figure 1.

FIGURE 5.
FIGURE 5.

Proposed secondary structure of U7 RNA orthologs and possible interaction with histone mRNA. Upper sequences are histone mRNA sequences, and lower sequences are U7 RNAs. The U7 RNA sequence from Homo sapiens (Mowry and Steitz 1987) is shown, as well as U7 sequences not previously reported from Gallus gallus, D. rerio, G. aculeatus, P. marinus, B. floridae, and S. purpuratus. Helices in the SL motif as well as in U7 RNA are shown with a bracket notation. Potential Sm sites in U7 RNA are shown in boldface. See Supplemental Figure 7 for more detailed information on the origin of U7 RNA sequences.

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