A heterochromatin-dependent transcription machinery drives piRNA expression

TY - JOUR

T1 - A heterochromatin-dependent transcription machinery drives piRNA expression

AU - Andersen, Peter Refsing

AU - Tirian, Laszlo

AU - Vunjak, Milica

AU - Brennecke, Julius

PY - 2017/9/7

Y1 - 2017/9/7

N2 - Nuclear small RNA pathways safeguard genome integrity by establishing transcription-repressing heterochromatin at transposable elements. This inevitably also targets the transposon-rich source loci of the small RNAs themselves. How small RNA source loci are efficiently transcribed while transposon promoters are potently silenced is not understood. Here we show that, in Drosophila, transcription of PIWI-interacting RNA (piRNA) clusters-small RNA source loci in animal gonads-is enforced through RNA polymerase II pre-initiation complex formation within repressive heterochromatin. This is accomplished through Moonshiner, a paralogue of a basal transcription factor IIA (TFIIA) subunit, which is recruited to piRNA clusters via the heterochromatin protein-1 variant Rhino. Moonshiner triggers transcription initiation within piRNA clusters by recruiting the TATA-box binding protein (TBP)-related factor TRF2, an animal TFIID core variant. Thus, transcription of heterochromatic small RNA source loci relies on direct recruitment of the core transcriptional machinery to DNA via histone marks rather than sequence motifs, a concept that we argue is a recurring theme in evolution.

AB - Nuclear small RNA pathways safeguard genome integrity by establishing transcription-repressing heterochromatin at transposable elements. This inevitably also targets the transposon-rich source loci of the small RNAs themselves. How small RNA source loci are efficiently transcribed while transposon promoters are potently silenced is not understood. Here we show that, in Drosophila, transcription of PIWI-interacting RNA (piRNA) clusters-small RNA source loci in animal gonads-is enforced through RNA polymerase II pre-initiation complex formation within repressive heterochromatin. This is accomplished through Moonshiner, a paralogue of a basal transcription factor IIA (TFIIA) subunit, which is recruited to piRNA clusters via the heterochromatin protein-1 variant Rhino. Moonshiner triggers transcription initiation within piRNA clusters by recruiting the TATA-box binding protein (TBP)-related factor TRF2, an animal TFIID core variant. Thus, transcription of heterochromatic small RNA source loci relies on direct recruitment of the core transcriptional machinery to DNA via histone marks rather than sequence motifs, a concept that we argue is a recurring theme in evolution.

KW - Animals

KW - Chromosomal Proteins, Non-Histone/metabolism

KW - DNA Transposable Elements/genetics

KW - Drosophila Proteins/metabolism

KW - Drosophila melanogaster/genetics

KW - Female

KW - Gene Silencing

KW - Heterochromatin/chemistry

KW - Multigene Family/genetics

KW - Promoter Regions, Genetic/genetics

KW - RNA Polymerase II/chemistry

KW - RNA, Small Interfering/biosynthesis

KW - Telomeric Repeat Binding Protein 2/metabolism

KW - Transcription Factor TFIIA/metabolism

KW - Transcription Initiation, Genetic

KW - Transcription, Genetic

U2 - 10.1038/nature23482

DO - 10.1038/nature23482

M3 - Journal article

C2 - 28847004

SN - 0028-0836

VL - 549

SP - 54

EP - 59

JO - Nature

JF - Nature

IS - 7670

ER -