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An RNA-dependent RNA polymerase is required for paramutation in maize

Abstract

Paramutation is an allele-dependent transfer of epigenetic information, which results in the heritable silencing of one allele by another1. Paramutation at the b1 locus in maize is mediated by unique tandem repeats that communicate in trans to establish and maintain meiotically heritable transcriptional silencing2. The mop1 (mediator of paramutation1) gene is required for paramutation3, and mop1 mutations reactivate silenced Mutator elements4. Plants carrying mutations in the mop1 gene also stochastically exhibit pleiotropic developmental phenotypes3. Here we report the map-based cloning of mop1, an RNA-dependent RNA polymerase gene (RDRP), most similar to the RDRP in plants that is associated with the production of short interfering RNA (siRNA) targeting chromatin5,6. Nuclear run-on assays reveal that the tandem repeats required for b1 paramutation are transcribed from both strands, but siRNAs were not detected. We propose that the mop1 RDRP is required to maintain a threshold level of repeat RNA, which functions in trans to establish and maintain the heritable chromatin states associated with paramutation.

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Figure 1: Genetic mapping of mop1 and identification of candidate genes.
Figure 2: The mop1 gene is rdr101.
Figure 3: Tandem repeats mediating b1 paramutation are transcribed on both strands.
Figure 4: Model for requirement of tandem repeats for RDRP amplification of RNA.

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Acknowledgements

We thank R. Wing and Arizona Genomics Institute scientists H. R. Kim, T. Rambo Mueller and F. Wei for sequencing and finishing the BAC clones; R. Jorgensen, C. Napoli and K. Gendler for performing the alignments and phylogenetic analyses; G. McCarthy and J. Bennetzen for help with the Bac-Breaker retroelement analysis of the BAC sequences; J. Gardiner for providing sequences for a mapping marker; and H. Basinger for technical assistance with the nuclear run-on assays. This work was supported by grants to V.L.C. from the National Science Foundation (NSF) and the National Institutes of Health; M.A. received a sabbatical supplement from the NSF. K.S., a student in the Undergraduate Biology Research Program, was supported in part by the Howard Hughes Medical Institute. Author Contributions J.E.D. performed the initial mapping of mop1. L.S., J.W. and K.S. generated the large mapping population and performed the fine-structure mapping. M.A. compared the mapping data with the rice syntenic sequences, performed the sequencing, characterized the mutant alleles, and generated the figures. V.S. and K.M. performed the RNA and nuclear run-on experiments. V.L.C. directed the experiments and wrote the paper. All authors discussed the results and commented on the manuscript.

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Correspondence to Vicki L. Chandler.

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Competing interests

Sequences described in this paper have been deposited in GenBank under the following accession numbers: DQ417753 (ZMMBBb0178I03), DQ417752 (ZMMBBb0004G18), DQ419917 (mop1-1), DQ417754 (mop1-2), DQ417755 (rdr101 from W22) and DQ414253 (B73). Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Notes

This file contains Supplementary Figures 1 and 2, Supplementary Tables 1 and 3 and Supplementary Methods. Supplementary Figure 1 shows phenotypes of mop1 mutations and b1 paramutation used for mapping. Supplementary Figure shows a phylogenetic analysis of plant RNA dependent RNA polymerases. Supplementary Tables 1 and 2 present the results of mop1 positional mapping. Supplementary Methods describe methods not in the main body of the text and oligonucleotide sequences, with references used in the Supplementary Methods. (PDF 1496 kb)

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Alleman, M., Sidorenko, L., McGinnis, K. et al. An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442, 295–298 (2006). https://doi.org/10.1038/nature04884

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