A chromodomain protein mediates heterochromatin-directed piRNA expression

PIWI-interacting RNAs (piRNAs) play significant roles in suppressing transposons, maintaining genome integrity, and defending against viral infections. How piRNA source loci are efficiently transcribed is poorly understood. Here, we show that in Caenorhabditis elegans, transcription of piRNA cluster...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2021-07, Vol.118 (27), p.1-11
Main Authors: Huang, Xinya, Cheng, Peng, Weng, Chenchun, Xu, Zongxiu, Zeng, Chenming, Xu, Zheng, Chen, Xiangyang, Zhu, Chengming, Guang, Shouhong, Feng, Xuezhu
Format: Article
Language:English
Subjects:
Animals
Biological Sciences
Caenorhabditis elegans - genetics
Caenorhabditis elegans - metabolism
Caenorhabditis elegans Proteins - metabolism
Chromatin Assembly and Disassembly
Chromatin remodeling
Clusters
Deoxyribonucleic acid
DNA
Genetic screening
Genetic Testing
Genomes
Germ Cells - cytology
Germ Cells - metabolism
Heterochromatin
Heterochromatin - metabolism
Histones
Histones - metabolism
Loci
Lysine
Lysine - metabolism
Methylation
Microenvironments
Peptides - metabolism
Polycomb Repressive Complex 2 - metabolism
Protein Binding
Proteins
RNA, Small Interfering - metabolism
Temperature
Transcription
Transposons
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Summary:PIWI-interacting RNAs (piRNAs) play significant roles in suppressing transposons, maintaining genome integrity, and defending against viral infections. How piRNA source loci are efficiently transcribed is poorly understood. Here, we show that in Caenorhabditis elegans, transcription of piRNA clusters depends on the chromatin microenvironment and a chromodomain-containing protein, UAD-2. piRNA clusters form distinct focus in germline nuclei. We conducted a forward genetic screening and identified UAD-2 that is required for piRNA focus formation. In the absence of histone 3 lysine 27 methylation or proper chromatin-remodeling status, UAD-2 is depleted from the piRNA focus. UAD-2 recruits the upstream sequence transcription complex (USTC), which binds the Ruby motif to piRNA promoters and promotes piRNA generation. Vice versa, the USTC complex is required for UAD-2 to associate with the piRNA focus. Thus, transcription of heterochromatic small RNA source loci relies on coordinated recruitment of both the readers of histone marks and the core transcriptional machinery to DNA.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2103723118