TBPL2/TFIIA complex establishes the maternal transcriptome through oocyte-specific promoter usage

Changwei Yu,Nevena Cvetesic,Luc Negroni,Vincent Hisler,Tao Ye,Stéphane D Vincent,László Tora,Petra Hajkova,Boris Lenhard,Ferenc Müller,Emese Gazdag,Imre Berger,Kapil Gupta

doi:10.1038/s41467-020-20239-4

Abstract

During oocyte growth, transcription is required to create RNA and protein reserves to achieve maternal competence. During this period, the general transcription factor TATA binding protein (TBP) is replaced by its paralogue, TBPL2 (TBP2 or TRF3), which is essential for RNA polymerase II transcription. We show that in oocytes TBPL2 does not assemble into a canonical TFIID complex. Our transcript analyses demonstrate that TBPL2 mediates transcription of oocyte-expressed genes, including mRNA survey genes, as well as specific endogenous retroviral elements. Transcription start site (TSS) mapping indicates that TBPL2 has a strong preference for TATA-like motif in core promoters driving sharp TSS selection, in contrast with canonical TBP/TFIID-driven TATA-less promoters that have broader TSS architecture. Thus, we show a role for the TBPL2/TFIIA complex in the establishment of the oocyte transcriptome by using a specific TSS recognition code.

Highlights

During oocyte growth, transcription is required to create RNA and protein reserves to achieve maternal competence
We show that a unique basal transcription machinery composed of TBPL2 associated with TFIIA is controlling transcription initiation during oocyte growth, orchestrating a transcriptome change prior to fertilisation using an oocyte-specific TTS usage
TBPL1 (TRF2) expression is enriched during spermatogenesis, and male germ cells lacking

Summary

Introduction

Transcription is required to create RNA and protein reserves to achieve maternal competence During this period, the general transcription factor TATA binding protein (TBP) is replaced by its paralogue, TBPL2 (TBP2 or TRF3), which is essential for RNA polymerase II transcription. All three vertebrate TBP-related factors can interact with the GTFs TFIIA and TFIIB, and can mediate Pol II transcription initiation in vitro[12,13,18,19,20]. Transcription initiation within a narrow region, called “sharp” (or focused) TSS-type, is common in highly active, tissue-specific gene promoters containing TATA boxes. TATA-like, AT-rich (W-box) upstream elements guiding TSS selection, while embryonically active broad promoter architectures of the same genes appear to be regulated by nucleosome positioning. A number of germ cell-specific, as well as somatic transcriptional regulators, have been well characterised during folliculogenesis (reviewed in ref. 24), the exact actors and mechanisms required for setting up the oocyte-specific transcriptome have not yet been identified in vertebrates

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