Drosophila melanogaster embryonic development starts with thirteen nuclear divisions without cytokinesis (syncytial blastoderm), being these divisions among the fastest known for any animal embryonic system. Drosophila syncytial blastoderm relies on maternally encoded gene products, loaded into the egg during oogenesis. After fertilization, and as nuclei enter interphase 14, there is a maternal to zygotic transition (MZT) in which the soma suddenly becomes transcriptionally active and many of the maternally encoded products are rapidly degraded. Whilst the major burst of zygotic transcription only occurs once the nuclei arrest in interphase 14, there is an initial wave of zygotic expression during the syncytial nuclear divisions 8-13.
Drosophila syncytial nuclear divisions limit transcription unit size of early zygotic genes. As mitosis inhibits not only transcription, but also pre-mRNA splicing, we reasoned that constraints on splicing were likely to exist in the early embryo, being splicing avoidance a possible explanation why most early zygotic genes are intronless. We isolated two mutant alleles for a subunit of the NTC/Prp19 complexes, which specifically impaired pre-mRNA splicing of early zygotic but not maternally encoded transcripts. We hypothesized that the requirements for pre-mRNA splicing efficiency were likely to vary during development. Ectopic maternal expression of an early zygotic pre-mRNA was sufficient to suppress its splicing defects in the mutant background. Furthermore, a small early zygotic transcript with multiple introns was poorly spliced in wild-type embryos. Our findings demonstrate for the first time the existence of a developmental pre-requisite for highly efficient splicing during Drosophila early embryonic development and suggest in highly proliferative tissues a need for coordination between cell cycle and gene architecture to ensure correct gene expression and avoid abnormally processed transcripts.