An RNA-dependent RNA polymerase is required for paramutation in maize (original) (raw)

• Letter
• Published: 20 July 2006
• Lyudmila Sidorenko1,
• Karen McGinnis1,
• Vishwas Seshadri1 nAff3,
• Jane E. Dorweiler1 nAff4,
• Joshua White1 nAff5,
• Kristin Sikkink1 &
• …
• Vicki L. Chandler1

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

• 3240 Accesses
• 303 Citations
• 18 Altmetric
• Metrics details

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.

This is a preview of subscription content, access via your institution

Access options

Subscribe to this journal

Receive 51 print issues and online access

$199.00 per year

only $3.90 per issue

Buy this article

• Purchase on SpringerLink
• Instant access to full article PDF

Prices may be subject to local taxes which are calculated during checkout

Additional access options:

• Log in
• Learn about institutional subscriptions
• Read our FAQs
• Contact customer support

Similar content being viewed by others

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

Download references

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.

Author information

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

Authors

1. Mary Alleman
   You can also search for this author inPubMed Google Scholar
2. Lyudmila Sidorenko
   You can also search for this author inPubMed Google Scholar
3. Karen McGinnis
   You can also search for this author inPubMed Google Scholar
4. Vishwas Seshadri
   You can also search for this author inPubMed Google Scholar
5. Jane E. Dorweiler
   You can also search for this author inPubMed Google Scholar
6. Joshua White
   You can also search for this author inPubMed Google Scholar
7. Kristin Sikkink
   You can also search for this author inPubMed Google Scholar
8. Vicki L. Chandler
   You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence toVicki L. Chandler.

Ethics declarations

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)

Rights and permissions

About this article

Cite this article

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

Download citation

• Received: 03 March 2006
• Accepted: 11 May 2006
• Issue Date: 20 July 2006
• DOI: https://doi.org/10.1038/nature04884

This article is cited by

Editorial Summary

How maize bends the rules

Paramutation, first discovered in maize in the 1950s and since found in other plants, fungi, and even mice, is an inheritance pattern that breaks the rules. Most of the time Mendel's law holds sway, and gene pairs sort independently. Paramutation is an interaction in which one silent allele of a gene 'mutates' the actively expressed allele, so that it too is silenced. New work in maize now shows that paramutation is RNA-directed. Stability of the chromatin states associated with paramutation and transposon silencing requires the mop1 gene, which encodes an RNA-dependent RNA polymerase.