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Metazoan replication-dependent histone mRNAs are not polyadenylated, and instead terminate in a conserved stem–loop structure generated by an endonucleolytic cleavage involving the U7 snRNP, which interacts with histone pre-mRNAs through base-pairing between U7 snRNA and a purine-rich sequence in the pre-mRNA located downstream of the cleavage site. Here we generate null mutations of the single  Drosophila U7  gene and demonstrate that U7 snRNA is required in vivo for processing all replication-associated histone pre-mRNAs. Mutation of  U7  results in the production of poly A +  histone mRNA in both proliferating and endocycling cells because of read-through to cryptic polyadenylation sites found downstream of each  Drosophila  histone gene. A similar molecular phenotype also results from mutation of  Slbp , which encodes the protein that binds the histone mRNA 3′ stem–loop.  U7  null mutants develop into sterile males and females, and these females display defects during oogenesis similar to germ line clones of  Slbp  null cells. In contrast to U7 mutants,  Slbp  null mutations cause lethality. This may reflect a later onset of the histone pre-mRNA processing defect in  U7  mutants compared to  Slbp  mutants, due to maternal stores of U7 snRNA. A double mutant combination of a viable, hypomorphic  Slbp  allele and a viable  U7  null allele is lethal, and these double mutants express polyadenylated histone mRNAs earlier in development than either single mutant. These data suggest that SLBP and U7 snRNP cooperate in the production of histone mRNA in vivo, and that disruption of histone pre-mRNA processing is detrimental to development.

U7 snRNA mutations in Drosophila block histone pre-mRNA processing and disrupt oogenesis