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 -