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 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.