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Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis

Nature volume 460, pages 283–286 (2009)Cite this article

Abstract

Most eukaryotes produce small RNA (sRNA) mediators of gene silencing that bind to Argonaute proteins and guide them, by base pairing, to an RNA target. MicroRNAs (miRNAs) that normally target messenger RNAs for degradation or translational arrest are the best-understood class of sRNAs. However, in Arabidopsis thaliana flowers, miRNAs account for only 5% of the sRNA mass and less than 0.1% of the sequence complexity. The remaining sRNAs form a complex population of more than 100,000 different small interfering RNAs (siRNAs) transcribed from thousands of loci1,2,3,4,5. The biogenesis of most of the siRNAs in Arabidopsis are dependent on RNA polymerase IV (PolIV), a homologue of DNA-dependent RNA polymerase II2,3,6. A subset of these PolIV-dependent (p4)-siRNAs are involved in stress responses, and others are associated with epigenetic modifications to DNA or chromatin; however, the biological role is not known for most of them. Here we show that the predominant phase of p4-siRNA accumulation is initiated in the maternal gametophyte and continues during seed development. Expression of p4-siRNAs in developing endosperm is specifically from maternal chromosomes. Our results provide the first evidence for a link between genomic imprinting and RNA silencing in plants.

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Figure 1: p4-siRNAs accumulate to high concentrations in seeds during early embryogenesis.
Figure 2: p4-siRNA expression in the zygote requires maternal NRPD1A.
Figure 3: p4-siRNA expression in developing seeds is uniparental genome-wide.
Figure 4: Uniparental expression of p4-siRNAs is specific to the seed.

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References

  1. Aravin, A. A. et al. The small RNA profile during Drosophila melanogaster development. Dev. Cell 5, 337–350 (2003)

    Article  CAS  Google Scholar 

  2. Kasschau, K. D. et al. Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol. 5, 0479–0493 (2007)

    Article  CAS  Google Scholar 

  3. Mosher, R. A., Schwach, F., Studholme, D. J. & Baulcombe, D. C. PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc. Natl Acad. Sci. USA 105, 3145–3150 (2008)

    Article  ADS  CAS  Google Scholar 

  4. Reinhart, B. J., Weinstein, E. G., Rhoades, M., Bartel, B. & Bartel, D. P. MicroRNAs in plants. Genes Dev. 16, 1616–1626 (2002)

    Article  CAS  Google Scholar 

  5. Ruby, J. G. et al. Large-scale sequencing reveals 21U-RNAs and additional Micro-RNAs and endogenous siRNAs in C. elegans. Cell 127, 1193–1207 (2006)

    Article  CAS  Google Scholar 

  6. Zhang, X., Henderson, I. R., Lu, C., Green, P. J. & Jacobsen, S. E. Role of RNA polymerase IV in plant small RNA metabolism. Proc. Natl Acad. Sci. USA 104, 4536–4541 (2007)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  8. Kanno, T. et al. Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nature Genet. 37, 761–765 (2005)

    Article  CAS  Google Scholar 

  9. Onodera, Y. et al. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120, 613–622 (2005)

    Article  CAS  Google Scholar 

  10. Pontier, D. et al. Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes Dev. 19, 2030–2040 (2005)

    Article  CAS  Google Scholar 

  11. 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  Google Scholar 

  12. Singer, T., Yordan, C. & Martienssen, R. A. Robertson’s Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev. 15, 591–602 (2001)

    Article  CAS  Google Scholar 

  13. Lu, C. et al. Elucidation of the small RNA component of the transcriptome. Science 309, 1567–1569 (2005)

    Article  ADS  CAS  Google Scholar 

  14. Swiezewski, S. et al. Small RNA-mediated chromatin silencing directed to the 3′ region of the Arabidopsis gene encoding the developmental regulator, FLC. Proc. Natl Acad. Sci. USA 104, 3633–3638 (2007)

    Article  ADS  CAS  Google Scholar 

  15. Vielle-Calzada, J. P., Baskar, R. & Grossniklaus, U. Delayed activation of the paternal genome during seed development. Nature 404, 91–94 (2000)

    Article  ADS  CAS  Google Scholar 

  16. Jullien, P. E., Katz, A., Oliva, M., Ohad, N. & Berger, F. Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA in Arabidopsis. Curr. Biol. 16, 486–492 (2006)

    Article  CAS  Google Scholar 

  17. Kinoshita, T. et al. One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303, 521–523 (2004)

    Article  ADS  CAS  Google Scholar 

  18. Jullien, P. E., Kinoshita, T., Ohad, N. & Berger, F. Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. Plant Cell 18, 1360–1372 (2006)

    Article  CAS  Google Scholar 

  19. Kinoshita, T., Yadegari, R., Harada, J. J., Goldberg, R. B. & Fischer, R. L. Imprinting of the MEDEA Polycomb gene in the Arabidopsis endosperm. Plant Cell 11, 1945–1952 (1999)

    Article  CAS  Google Scholar 

  20. Kohler, C. et al. The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev. 17, 1540–1553 (2003)

    Article  Google Scholar 

  21. Slotkin, R. K. et al. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136, 461–472 (2009)

    Article  CAS  Google Scholar 

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Acknowledgements

We thank I. Furner for met1-1 seed and A. Davis for photography. This work was supported by the Gatsby Charitable Foundation, the European Union Sixth Framework Programme Integrated Project SIROCCO (grant LSHG-CT-2006-037900), a postdoctoral fellowship from the National Science Foundation (to R.A.M.), and Commonwealth and NSERC Scholarships (to C.W.M.). D.C.B. is funded as a Royal Society Research Professor.

Author Contributions Experiments were designed by R.A.M. and D.C.B. and executed by R.A.M. with assistance from C.W.M. Bioinformatic and statistical analyses were performed by K.A.K., R.M.D. and D.J.S. The manuscript was prepared by R.A.M. and D.C.B.

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Authors and Affiliations

  1. Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, UK,

    Rebecca A. Mosher, Charles W. Melnyk, Krystyna A. Kelly, Ruth M. Dunn & David C. Baulcombe

  2. The Sainsbury Laboratory, Colney Lane, Norwich NR4 7UH, UK,

    David J. Studholme

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  1. Rebecca A. Mosher
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  2. Charles W. Melnyk
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  3. Krystyna A. Kelly
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  4. Ruth M. Dunn
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  5. David J. Studholme
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  6. David C. Baulcombe
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Corresponding author

Correspondence to David C. Baulcombe.

Additional information

Deep sequencing libraries are deposited in NCBI GEO (GSE15348).

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Supplementary Information

This file contains Supplementary Notes, Supplementary Tables S1-S3, Supplementary Figures S1-S4 with Legends and Supplementary References. (PDF 960 kb)

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Mosher, R., Melnyk, C., Kelly, K. et al. Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 460, 283–286 (2009). https://doi.org/10.1038/nature08084

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