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

Nature volume 442, pages 295–298 (2006)Cite this article

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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References

  1. Chandler, V. L. & Stam, M. Chromatin conversations: mechanisms and implications of paramutation. Nature Rev. Genet. 5, 532–544 (2004)

    Article  CAS  PubMed  Google Scholar 

  2. Stam, M., Belele, C., Dorweiler, J. E. & Chandler, V. L. Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes Dev. 16, 1906–1918 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Dorweiler, J. E. et al. Mediator of paramutation1 is required for establishment and maintenance of paramutation at multiple maize loci. Plant Cell 12, 2101–2118 (2000)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Lisch, D., Carey, C. C., Dorweiler, J. E. & Chandler, V. L. A mutation that prevents paramutation in maize also reverses Mutator transposon methylation and silencing. Proc. Natl Acad. Sci. USA 99, 6130–6135 (2002)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  5. Xie, Z. et al. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2, E104 (2004)

    Article  PubMed  PubMed Central  Google Scholar 

  6. Chan, S. W. et al. RNA silencing genes control de novo DNA methylation. Science 303, 1336 (2004)

    Article  CAS  PubMed  Google Scholar 

  7. Hollick, J. B. & Chandler, V. L. Genetic factors required to maintain repression of a paramutagenic maize pl1 allele. Genetics 157, 369–378 (2001)

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Bennetzen, J. & Ma, J. The genetic colinearity of rice and other cereals on the basis of genomic sequence analysis. Curr. Opin. Plant Biol. 6, 128–133 (2003)

    Article  CAS  PubMed  Google Scholar 

  9. Feng, Q. et al. Sequence and analysis of rice chromosome 4. Nature 420, 316–320 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  10. Herr, A. J. Pathways through the small RNA world of plants. FEBS Lett. 579, 5879–5888 (2005)

    Article  CAS  PubMed  Google Scholar 

  11. Bernstein, E. & Allis, C. D. RNA meets chromatin. Genes Dev. 19, 1635–1655 (2005)

    Article  CAS  PubMed  Google Scholar 

  12. Kohalmi, S. E. & Kunz, B. A. Role of neighbouring bases and assessment of strand specificity in ethylmethanesulphonate and N-methyl-N′-nitro-N-nitrosoguanidine mutagenesis in the SUP4-o gene of Saccharomyces cerevisiae. J. Mol. Biol. 204, 561–568 (1988)

    Article  CAS  PubMed  Google Scholar 

  13. Dalmay, T., Hamilton, A., Rudd, S., Angell, S. & Baulcombe, D. C. An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101, 543–553 (2000)

    Article  CAS  PubMed  Google Scholar 

  14. Kakutani, T., Jeddeloh, J. A., Flowers, S. K., Munakata, K. & Richards, E. J. Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc. Natl Acad. Sci. USA 93, 12406–12411 (1996)

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  15. Jeddeloh, J. A., Stokes, T. L. & Richards, E. J. Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nature Genet. 22, 94–97 (1999)

    Article  CAS  PubMed  Google Scholar 

  16. Brzeski, J. & Jerzmanowski, A. Deficient in DNA Methylation 1 (DDM1) defines a novel family of chromatin-remodeling factors. J. Biol. Chem. 278, 823–828 (2003)

    Article  CAS  PubMed  Google Scholar 

  17. Volpe, T. A. et al. Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297, 1833–1837 (2002)

    Article  ADS  CAS  PubMed  Google Scholar 

  18. Sugiyama, T., Cam, H., Verdel, A., Moazed, D. & Grewal, S. I. RNA-dependent RNA polymerase is an essential component of a self-enforcing loop coupling heterochromatin assembly to siRNA production. Proc. Natl Acad. Sci. USA 102, 152–157 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  19. Motamedi, M. R. et al. Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119, 789–802 (2004)

    Article  CAS  PubMed  Google Scholar 

  20. Slotkin, R. K., Freeling, M. & Lisch, D. Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nature Genet. 37, 641–644 (2005)

    Article  CAS  PubMed  Google Scholar 

  21. Patterson, G. I., Thorpe, C. J. & Chandler, V. L. Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize b regulatory gene. Genetics 135, 881–894 (1993)

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Lippman, Z. et al. Role of transposable elements in heterochromatin and epigenetic control. Nature 430, 471–476 (2004)

    Article  ADS  CAS  PubMed  Google Scholar 

  23. Melquist, S. & Bender, J. Transcription from an upstream promoter controls methylation signaling from an inverted repeat of endogenous genes in Arabidopsis. Genes Dev. 17, 2036–2047 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Herr, A. J., Jensen, M. B., Dalmay, T. & Baulcombe, D. C. RNA polymerase IV directs silencing of endogenous DNA. Science 308, 118–120 (2005)

    Article  ADS  CAS  PubMed  Google Scholar 

  25. Maine, E. M. et al. EGO-1, a putative RNA-dependent RNA polymerase, is required for heterochromatin assembly on unpaired DNA during C. elegans meiosis. Curr. Biol. 15, 1972–1978 (2005)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Martienssen, R. A. Maintenance of heterochromatin by RNA interference of tandem repeats. Nature Genet. 35, 213–214 (2003)

    Article  CAS  PubMed  Google Scholar 

  27. May, B. P., Lippman, Z. B., Fang, Y., Spector, D. L. & Martienssen, R. A. Differential regulation of strand-specific transcripts from Arabidopsis centromeric satellite repeats. PLoS Genet. 1, e79 (2005)

    Article  PubMed  PubMed Central  Google Scholar 

  28. Martienssen, R. A., Doerge, R. W. & Colot, V. Epigenomic mapping in Arabidopsis using tiling microarrays. Chromosome Res. 13, 299–308 (2005)

    Article  CAS  PubMed  Google Scholar 

  29. Lee, D. W., Seong, K. Y., Pratt, R. J., Baker, K. & Aramayo, R. Properties of unpaired DNA required for efficient silencing in Neurospora crassa. Genetics 167, 131–150 (2004)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Rassoulzadegan, M. et al. RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 441, 469–474 (2006)

    Article  ADS  CAS  PubMed  Google Scholar 

  31. Makeyev, E. V. & Bamford, D. H. Cellular RNA-dependent RNA polymerase involved in posttranscriptional gene silencing has two distinct activity modes. Mol. Cell 10, 1417–1427 (2002)

    Article  CAS  PubMed  Google Scholar 

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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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Author notes

  1. Mary Alleman

    Present address: Department of Biological Sciences, Duquesne University, Pittsburgh, Pennsylvania, 15282, USA

  2. Vishwas Seshadri

    Present address: Biologics Development Center Developing Businesses, Dr Reddy's Laboratories Ltd, Survey no. 47, R. R. District, Andhra Pradesh, 500072, India

  3. Jane E. Dorweiler

    Present address: Department of Biological Sciences, Marquette University, Milwaukee, Wisconsin, 53201, USA

  4. Joshua White

    Present address: Institute for Cellular and Molecular Biology, University of Texas at Austin, College of Natural Sciences, 1 University Station A4800, Austin, Texas, 78712, USA

Authors and Affiliations

  1. Department of Plant Sciences, University of Arizona, 303 Forbes Hall, Arizona, 85721, Tucson, USA

    Mary Alleman, Lyudmila Sidorenko, Karen McGinnis, Vishwas Seshadri, Jane E. Dorweiler, Joshua White, Kristin Sikkink & Vicki L. Chandler

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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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