The TATA-binding protein regulates maternal mRNA degradation and differential zygotic transcription in zebrafish

Abstract

Early steps of embryo development are directed by maternal gene products and trace levels of zygotic gene activity in vertebrates. A major activation of zygotic transcription occurs together with degradation of maternal mRNAs during the midblastula transition in several vertebrate systems. How these processes are regulated in preparation for the onset of differentiation in the vertebrate embryo is mostly unknown. Here, we studied the function of TATA-binding protein (TBP) by knock down and DNA microarray analysis of gene expression in early embryo development. We show that a subset of polymerase II-transcribed genes with ontogenic stage-dependent regulation requires TBP for their zygotic activation. TBP is also required for limiting the activation of genes during development. We reveal that TBP plays an important role in the degradation of a specific subset of maternal mRNAs during late blastulation/early gastrulation, which involves targets of the miR-430 pathway. Hence, TBP acts as a specific regulator of the key processes underlying the transition from maternal to zygotic regulation of embryogenesis. These results implicate core promoter recognition as an additional level of differential gene regulation during development.

The maternal-to-zygotic transition: a play in two acts

“…Genomescale transcript analyses in zebrafish (Fig. 2C) (Ferg et al, 2007;Mathavan et al, 2005) and C. elegans (Baugh et al, 2003) also show destabilization profiles that are consistent with maternal and zygotic degradation activities.…”

“…For example, the zygotic expression of miR-430 in zebrafish embryos is responsible for the clearance of several hundred maternal messages (Giraldez et al, 2006). miR-430 requires additional, zygotically produced, nonmiRNA factors to degrade a subset of its targets (Ferg et al, 2007). The D. melanogaster miR-309 family of miRNAs, which are synthesized zygotically in a SMG-dependent manner, participate in the destabilization of several hundred maternal mRNAs in a manner analogous to that of zebrafish miR-430 (Benoit et al, 2009;Bushati et al, 2008).…”

TBP, Mot1, and NC2 establish a regulatory circuit that controls DPE-dependent versus TATA-dependent transcription

“…Second, there may be an essential DPE-directed transcription factor that is inhibited by TBP. It is possible that DPE-mediated transcription does not directly involve TBP, as there is substantial evidence of RNA polymerase II-mediated transcription occurring in the absence of TBP (for example, see Veenstra et al 2000;Müller et al 2001;Martianov et al 2002;Paulson et al 2002;Deato and Tjian 2007;Ferg et al 2007). …”

Glucocorticoid receptor activation following elevated oocyte cortisol content is associated with zygote activation, early embryo cell division, and IGF system gene responses in rainbow trout

“…It is not clear at this point how that may occur, and it would appear to contradict the currently held view that the zygotic transcriptome is relatively stable and necessary for the regulation of the first cell division. However, there is evidence in several species for differential destabilization of a subset of mRNAs (Bashirulla et al 1999, Tandros et al 2003, 2007, Ferg et al 2007, Shiokawa et al 2008, Tandros & Lipshitz 2009). Therefore, the data presented in this paper may reflect an involvement of RU486 in destabilizing of some components of the zygotic transcriptome.…”