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Genes Dev. 2019 Jan 1;33(1-2):90-102. doi: 10.1101/gad.319293.118. Epub 2018 Dec 19.

The USTC co-opts an ancient machinery to drive piRNA transcription in C. elegans.

Author information

1
Hefei National Laboratory for Physical Sciences at the Microscale, School of Life Sciences, University of Science and Technology of China, Hefei, Anhui 230027, China.
2
Wellcome Cancer Research UK Gurdon Institute, University of Cambridge, Cambridge CB2 1QN, United Kingdom; Department of Genetics, University of Cambridge, Cambridge CB2 3EH, United Kingdom.
3
National Institute of Biological Sciences, Beijing 102206, China.
4
Structural and Computational Biology Unit, European Molecular Biology Laboratory (EMBL), 69117 Heidelberg, Germany.
5
Wellcome Sanger Institute, Cambridge CB10 1SA, United Kingdom.
#
Contributed equally

Abstract

Piwi-interacting RNAs (piRNAs) engage Piwi proteins to suppress transposons and nonself nucleic acids and maintain genome integrity and are essential for fertility in a variety of organisms. In Caenorhabditis elegans, most piRNA precursors are transcribed from two genomic clusters that contain thousands of individual piRNA transcription units. While a few genes have been shown to be required for piRNA biogenesis, the mechanism of piRNA transcription remains elusive. Here we used functional proteomics approaches to identify an upstream sequence transcription complex (USTC) that is essential for piRNA biogenesis. The USTC contains piRNA silencing-defective 1 (PRDE-1), SNPC-4, twenty-one-U fouled-up 4 (TOFU-4), and TOFU-5. The USTC forms unique piRNA foci in germline nuclei and coats the piRNA cluster genomic loci. USTC factors associate with the Ruby motif just upstream of type I piRNA genes. USTC factors are also mutually dependent for binding to the piRNA clusters and forming the piRNA foci. Interestingly, USTC components bind differentially to piRNAs in the clusters and other noncoding RNA genes. These results reveal the USTC as a striking example of the repurposing of a general transcription factor complex to aid in genome defense against transposons.

KEYWORDS:

PRDE-1; Ruby motif; SNPC; SNPC-4; TOFU-4; TOFU-5; U6 RNA; piRNA; snRNA

PMID:
30567997
DOI:
10.1101/gad.319293.118
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