Abstract
BackgroundVertebrate development relies on the regulated translation of stored maternal mRNAs, but how these regulatory mechanisms may have evolved to control translational efficiency of individual mRNAs is poorly understood. We compared the translational regulation and polyadenylation of the cyclin B1 mRNA during zebrafish and Xenopus oocyte maturation. Polyadenylation and translational activation of cyclin B1 mRNA is well characterized during Xenopus oocyte maturation. Specifically, Xenopus cyclin B1 mRNA is polyadenylated and translationally activated during oocyte maturation by proteins that recognize the conserved AAUAAA hexanucleotide and U-rich Cytoplasmic Polyadenylation Elements (CPEs) within cyclin B1 mRNA's 3'UnTranslated Region (3'UTR).ResultsThe zebrafish cyclin B1 mRNA was polyadenylated during zebrafish oocyte maturation. Furthermore, the zebrafish cyclin B1 mRNA's 3'UTR was sufficient to stimulate translation of a reporter mRNA during zebrafish oocyte maturation. This stimulation required both AAUAAA and U-rich CPE-like sequences. However, in contrast to AAUAAA, the positions and sequences of the functionally defined CPEs were poorly conserved between Xenopus and zebrafish cyclin B1 mRNA 3'UTRs. To determine whether these differences were relevant to translation efficiency, we analyzed the translational activity of reporter mRNAs containing either the zebrafish or Xenopus cyclin B1 mRNA 3'UTRs during both zebrafish and Xenopus oocyte maturation. The zebrafish cyclin B1 3'UTR was quantitatively less effective at stimulating polyadenylation and translation compared to the Xenopus cyclin B1 3'UTR during both zebrafish and Xenopus oocyte maturation.ConclusionAlthough the factors that regulate translation of maternal mRNAs are highly conserved, the target sequences and overall sequence architecture within the 3'UTR of the cyclin B1 mRNA have diverged to affect translational efficiency, perhaps to optimize levels of cyclin B1 protein required by these different species during their earliest embryonic cell divisions.
Highlights
Vertebrate development relies on the regulated translation of stored maternal mRNAs, but how these regulatory mechanisms may have evolved to control translational efficiency of individual mRNAs is poorly understood
These quantitative differences were likely due distinctions between the 3'UnTranslated Region (3'UTR) of zebrafish and Xenopus cyclin B1 mRNAs. These findings suggest that Cytoplasmic Polyadenylation Elements (CPEs)-sequences and/or other aspects of 3'UTR sequence architecture evolved between species to modulate translational efficiency of maternal mRNAs, even those mRNAs that encode highly conserved proteins
Zebrafish cyclin B1 mRNA was polyadenylated during oocyte maturation and early embryogenesis Translation of the zebrafish cyclin B1 mRNA is activated during oocyte maturation but the underlying mechanisms have not been examined [22,23]
Summary
Vertebrate development relies on the regulated translation of stored maternal mRNAs, but how these regulatory mechanisms may have evolved to control translational efficiency of individual mRNAs is poorly understood. Early embryonic development is governed entirely by post-transcriptional mechanisms [1,2] During this period of development translational mechanisms dictate when and how efficiently each maternal mRNA is translated into protein [3,4]. Mechanisms that control maternal mRNA translation during Xenopus oocyte maturation are well studied and involve the regulated addition of 3' poly (A) to stored mRNAs [5,6]. It is unclear, how conserved these mechanisms are at the level of individual mRNAs. It is unclear, how conserved these mechanisms are at the level of individual mRNAs An understanding of such conservation should provide insights into how differences in target mRNA sequences could affect translational regulation during maternally controlled development
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