RNA redistribution driven by alterations in transcription during early embryogenesis of rainbow trout

In many species, the differential localization of RNAs along the animal-vegetal axis is established during oogenesis. The resulting asymmetry is essential for axis formation, germ layer patterning, and cell fate determination, especially in fish and amphibians. In recent years, research in this field has focused mainly on zebrafish, which raises the question about the conservation of localization processes across all teleost species. Although extant teleost species utilize meroblastic cleavage only, there are extreme differences in their oocyte size. These differences are fundamentally linked to each species' life history. Some have rapid embryonic development, while embryos of other species, like salmonids, take weeks to develop. This might have consequences on the spatial distribution of biomolecules during oogenesis and their relocalization during early embryogenesis. Yet, our knowledge is based on data from small-sized oocyte species with rapid development only (e.g. zebrafish). In this study, we performed a spatially resolved TOMO-seq method on early embryos of the rainbow trout, a species characterized by prolonged embryonic development and large oocytes, and compared it with zebrafish. We revealed that the maternal pre-patterned localization of transcripts can be disrupted in the early embryo by two main mechanisms: de novo transcription and degradation. The most prominent change can be seen in the emerging blastodisc in the animal pole, where there is a significant increase in localized transcripts. In contrast with research suggesting active relocalization of RNAs by ooplasmic streaming in zebrafish, we hypothesized that the change in RNA localization is caused by regionalized zygotic transcription in trout. Regardless of these differing mechanisms, the cross-species comparison revealed a conservation of many transcripts involved in germ cell development and cell proliferation. Moreover, using hybrid trout embryos, we were able to reveal the early onset of de novo transcription. Altogether, these findings indicate how species with large oocytes and prolonged development utilize unique RNA localization strategies. This knowledge expands our understanding of early development across teleost species.