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An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation
Zhihuan Gao1,10, Hai-Liang Liu1,2,10, Lucia Daxinger3,10,11, Olga Pontes4,10, Xinjian He1,5, Weiqiang Qian1, Huixin Lin1, Mingtang Xie1, Zdravko J. Lorkovic6, Shoudong Zhang1,5, Daisuke Miki1, Xiangqiang Zhan1,5, Dominique Pontier7, Thierry Lagrange7, Hailing Jin8, Antonius J. M. Matzke3, Marjori Matzke3, Craig S. Pikaard9 & Jian-Kang Zhu1,5
Institute for Integrative Genome Biology and Department of Botany and Plant Sciences, University of California, Riverside, California 92521, USA
School of life science and technology, Tongji University, Shanghai 200092, China
Gregor Mendel Institute of Molecular Plant Biology, Austrian Academy of Sciences, 1030 Vienna, Austria
Biology Department, Washington University, St Louis, Missouri 63130, USA
Center for Plant Stress Genomics and Technology, 4700 King Abdullah University of Science and Technology, Thuwal 23955-6900, Kingdom of Saudi Arabia
Max F. Perutz Laboratory, Medical University of Vienna, 1030 Vienna, Austria
LGDP, CNRS/IRD/Université de Perpignan, UMR 5096, 66860 Perpignan, France
Institute for Integrative Genome Biology and Department of Plant Pathology and Microbiology, University of California, Riverside, California 92521, USA
Department of Biology and Department of Molecular and Cellular Biochemistry, Indiana University, Bloomington, Indiana 47405, USA
These authors contributed equally to this work.
DNA methylation is an important epigenetic mark in many eukaryotes1, 2, 3, 4, 5. In plants, 24-nucleotide small interfering RNAs (s) bound to the effector protein, Argonaute 4 (AGO4), can direct de novo DNA methylation by the methyltransferase DRM2 (refs 2, 4–6). Here we report a new regulator of RNA-directed DNA methylation (RdDM) in Arabidopsis: RDM1. Loss-of-function mutations in the RDM1 gene impair the accumulation of 24-nucleotide siRNAs, reduce DNA methylation, and release transcriptional gene silencing at RdDM target loci. RDM1 encodes a small protein that seems to bind single-stranded methyl DNA, and associates and co-localizes with RNA polymerase II (Pol II, also known as NRPB), AGO4 and DRM2 in the nucleus. Our results indicate that RDM1 is a component of the RdDM effector complex and may have a role in linking siRNA production with pre-existing or de novo cytosine methylation. Our results also indicate that, although RDM1 and Pol V (also known as NRPE) may function together at some RdDM target sites in the peri-nucleolar siRNA processing centre, Pol II rather than Pol V is associated with the RdDM effector complex at target sites in the nucleoplasm.
