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RNA polymerase V targets transcriptional silencing components to promoters of protein-coding genes

Authors

  • Qi Zheng,

    1. Department of Biology, Penn Genomes Frontier Institute, University of Pennsylvania, Philadelphia, PA 19104, USA
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    • These authors contributed equally to this work.
  • M. Jordan Rowley,

    1. Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI 48109 , USA
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    • These authors contributed equally to this work.
  • Gudrun Böhmdorfer,

    1. Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI 48109 , USA
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  • Davinder Sandhu,

    1. Department of Biology, Penn Genomes Frontier Institute, University of Pennsylvania, Philadelphia, PA 19104, USA
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  • Brian D. Gregory,

    Corresponding author
    • Department of Biology, Penn Genomes Frontier Institute, University of Pennsylvania, Philadelphia, PA 19104, USA
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  • Andrzej T. Wierzbicki

    Corresponding author
    1. Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, MI 48109 , USA
    • Department of Biology, Penn Genomes Frontier Institute, University of Pennsylvania, Philadelphia, PA 19104, USA
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(e-mails bdgregor@sas.upenn.edu; wierzbic@umich.edu).

Summary

Transcriptional gene silencing controls transposons and other repetitive elements through RNA-directed DNA methylation (RdDM) and heterochromatin formation. A key component of the Arabidopsis RdDM pathway is ARGONAUTE4 (AGO4), which associates with siRNAs to mediate DNA methylation. Here, we show that AGO4 preferentially targets transposable elements embedded within promoters of protein-coding genes. This pattern of AGO4 binding cannot be simply explained by the sequences of AGO4-bound siRNAs; instead, AGO4 binding to specific gene promoters is also mediated by long non-coding RNAs (lncRNAs) produced by RNA polymerase V. lncRNA-mediated AGO4 binding to gene promoters directs asymmetric DNA methylation to these genomic regions and is involved in regulating the expression of targeted genes. Finally, AGO4 binding overlaps sites of DNA methylation affected by the biotic stress response. Based on these findings, we propose that the targets of AGO4-directed RdDM are regulatory units responsible for controlling gene expression under specific environmental conditions.

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