Early evolution of histone mRNA 3′ end processing

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 39 end of the mature RNA, and this 39 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 39 end processing is related to that of polyadenylation as protein components are shared between the systems. It is commonly believed that histone 39 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 39 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 39 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 39 end processing. These results provide further evidence that some histone genes are regulated at the level of 39 end processing to produce either polyadenylated RNAs or RNAs with the 39 end characteristic of replicationdependent histone mRNAs.

CstF-64 supports pluripotency and regulates cell cycle progression in embryonic stem cells through histone 3′ end processing

“…A similar alternative pathway to polyadenylation appears to be present in Drosophila replication-dependent histone mRNAs (51–53). Mammalian testis histone variants are also polyadenylated (54,55) as are histone mRNAs in yeast (56), demonstrating that this mechanism is ancient and conserved (57,58). …”

Birth and Death of Histone mRNAs

“…The structure of the SLBP–stem-loop RNA complex has been determined [5] (Box 1) and this complex at the 3′ end of the mRNA is involved in all steps of histone mRNA metabolism (i.e., processing, nuclear export, translation, and degradation of histone mRNA). There are no homologs of SLBP in species whose histone mRNAs are polyadenylated [6]. …”

“…Likely SLBP homologs have been identified in several single-cell eukaryotes including Volvox, Dictyostelium , and Chlamydomonas . These species also have stem-loops close to the 3′ end of their histone mRNAs, suggesting that histone mRNAs ending in stem-loops may have been present in some single-cell eukaryotes, and thus this property has been lost in evolution [6]. …”

“…This property is not essential for viability because plants and most single-cell eukaryotes have polyadenylated histone mRNAs, whose levels are also tightly cell cycle-regulated. The evolutionary analysis of Samuelsson and coworkers [6] strongly suggests that histone mRNAs may have differed from other mRNAs in some single-cell eukaryotic lineages, consistent with the stem-loop being ancient and having been lost from many lineages, together with SLBP, NPAT, FLASH, and U7 snRNP. In the immediate precursors of metazoans, histone mRNAs likely had stem-loops.…”

Genome-Wide Analysis and Functional Characterization of the Polyadenylation Site in Pigs Using RNAseq Data

“…In the process, multiple enzymes first recognize poly(A) signals, such as cleavage/polyadenylation specificity factor (CPSF), cleavage stimulation factor (CstF) and cleavage factor I (CFI), and then cleavage occurs at the 3′ ends of mRNAs123. Subsequently, poly(A) tail addition modifies mRNA at the cleavage site (also called the polyadenylation site, PAS), catalysed by CPSF, polyadenylated polymerase (PAP), polyadenylated binding protein II (PAB II) and RNA polymerase II (RNAP II)456.…”