Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Polycomb-mediated gene silencing by the BAH–EMF1 complex in plants

Nature Genetics volume 50, pages 1254–1261 (2018)Cite this article

Subjects

Abstract

Polycomb proteins implement genome-wide transcriptional repression in multicellular organisms. The evolutionarily conserved Polycomb repressive complex 2 (PRC2) catalyzes histone H3 Lys27 trimethylation (H3K27me3) that is read and effected by Polycomb repressive complex 1 (PRC1) in animals, but the interpretation of this mark remains unclear in plants. Here we report that in the eudicot Arabidopsis thaliana two homologous BAH (Bromo adjacent homology) domain–containing proteins form a plant-specific complex with EMBRYONIC FLOWER 1 (EMF1), and that the BAH–EMF1 complex (BAH–EMF1c) reads and effects the H3K27me3 mark and mediates genome-wide transcriptional repression. Furthermore, in the monocot rice a homolog of the Arabidopsis BAH-domain proteins also binds methylated H3K27 and forms a complex with the rice homolog of EMF1, suggesting that BAH–EMF1c is conserved in flowering plants. Therefore, our results show that the plant-specific BAH–EMF1c fulfills PRC1-like functions in higher plants, suggesting a convergent evolution of PRC1 activity in plants and animals.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Fig. 1: SHL and EBS directly associate with EMF1 and At BMI1a.
Fig. 2: Functional analysis of the BAH domains from the SHL- and EBS-family proteins.
Fig. 3: SHL and EBS function in partial redundancy to regulate genome-wide gene expression.
Fig. 4: EBS, SHL, and EMF1 co-occupy a large number of genomic regions marked by H3K27me3.
Fig. 5: Analysis of a set of selected EBS and/or SHL loci and characterization of histone modifications upon loss of EBS, SHL and/or LHP1 function.

Similar content being viewed by others

References

  1. Simon, J. A. & Kingston, R. E. Mechanisms of Polycomb gene silencing: knowns and unknowns. Nat. Rev. Mol. Cell Biol. 10, 697–708 (2009).

    CAS  PubMed  Google Scholar 

  2. Mozgova, I. & Hennig, L. The Polycomb group protein regulatory network. Annu. Rev. Plant Biol. 66, 269–296 (2015).

    CAS  PubMed  Google Scholar 

  3. Blackledge, N. P., Rose, N. R. & Klose, R. J. Targeting Polycomb systems to regulate gene expression: modifications to a complex story. Nat. Rev. Mol. Cell Biol. 16, 643–649 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Yang, C. et al. VAL- and AtBMI1-mediated H2Aub initiate the switch from embryonic to postgerminative growth in Arabidopsis. Curr. Biol. 23, 1324–1329 (2013).

    CAS  PubMed  Google Scholar 

  5. Beh, L. Y., Colwell, L. J. & Francis, N. J. A core subunit of Polycomb repressive complex 1 is broadly conserved in function but not primary sequence. Proc. Natl Acad. Sci. USA 109, E1063–E1071 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Kim, S. Y., Lee, J., Eshed-Williams, L., Zilberman, D. & Sung, Z. R. EMF1 and PRC2 cooperate to repress key regulators of Arabidopsis development. PLoS Genet. 8, e1002512 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Turck, F. et al. Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet. 3, e86 (2007).

    PubMed  PubMed Central  Google Scholar 

  8. Zhang, X. et al. The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat. Struct. Mol. Biol. 14, 869–871 (2007).

    CAS  PubMed  Google Scholar 

  9. Zhou, Y., Hartwig, B., James, G. V., Schneeberger, K. & Turck, F. Complementary activities of TELOMERE REPEAT BINDING proteins and Polycomb group complexes in transcriptional regulation of target genes. Plant Cell 28, 87–101 (2016).

    CAS  PubMed  Google Scholar 

  10. Zhou, Y., Romero-Campero, F. J., Gómez-Zambrano, Á. & Turck, F. H2A monoubiquitination in Arabidopsis thaliana is generally independent of LHP1 and PRC2 activity. Genome Biol. 18, 69 (2017).

    PubMed  PubMed Central  Google Scholar 

  11. Kim, S. Y., Zhu, T. & Sung, Z. R. Epigenetic regulation of gene programs by EMF1 and EMF2 in Arabidopsis. Plant Physiol. 152, 516–528 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. López-González, L. et al. Chromatin-dependent repression of the Arabidopsis floral integrator genes involves plant specific PHD-containing proteins. Plant Cell 26, 3922–3938 (2014).

    PubMed  PubMed Central  Google Scholar 

  13. Yang, N. & Xu, R. M. Structure and function of the BAH domain in chromatin biology. Crit. Rev. Biochem. Mol. Biol. 48, 211–221 (2013).

    CAS  PubMed  Google Scholar 

  14. Wang, Y., Gu, X., Yuan, W., Schmitz, R. J. & He, Y. Photoperiodic control of the floral transition through a distinct Polycomb repressive complex. Dev. Cell 28, 727–736 (2014).

    CAS  PubMed  Google Scholar 

  15. Bratzel, F., López-Torrejón, G., Koch, M., Del Pozo, J. C. & Calonje, M. Keeping cell identity in Arabidopsis requires PRC1 RING-finger homologs that catalyze H2A monoubiquitination. Curr. Biol. 20, 1853–1859 (2010).

    CAS  PubMed  Google Scholar 

  16. Gray, F. et al. BMI1 regulates PRC1 architecture and activity through homo- and hetero-oligomerization. Nat. Commun. 7, 13343 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Piñeiro, M., Gómez-Mena, C., Schaffer, R., Martínez-Zapater, J. M. & Coupland, G. EARLY BOLTING IN SHORT DAYS is related to chromatin remodeling factors and regulates flowering in Arabidopsis by repressing FT. Plant Cell 15, 1552–1562 (2003).

    PubMed  PubMed Central  Google Scholar 

  18. Berke, L. & Snel, B. The plant Polycomb repressive complex 1 (PRC1) existed in the ancestor of seed plants and has a complex duplication history. BMC Evol. Biol. 15, 44 (2015).

    PubMed  PubMed Central  Google Scholar 

  19. Yan, D. et al. Curved chimeric palea 1 encoding an EMF1-like protein maintains epigenetic repression of OsMADS58 in rice palea development. Plant J. 82, 12–24 (2015).

    CAS  PubMed  Google Scholar 

  20. Turck, F., Fornara, F. & Coupland, G. Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu. Rev. Plant Biol. 59, 573–594 (2008).

    CAS  PubMed  Google Scholar 

  21. Chen, D., Molitor, A., Liu, C. & Shen, W. H. The Arabidopsis PRC1-like ring-finger proteins are necessary for repression of embryonic traits during vegetative growth. Cell Res. 20, 1332–1344 (2010).

    CAS  PubMed  Google Scholar 

  22. Wang, H. et al. Arabidopsis flower and embryo developmental genes are repressed in seedlings by different combinations of Polycomb group proteins in association with distinct sets of cis-regulatory elements. PLoS Genet. 12, e1005771 (2016).

    PubMed  PubMed Central  Google Scholar 

  23. Li, C. et al. Concerted genomic targeting of H3K27 demethylase REF6 and chromatin-remodeling ATPase BRM in Arabidopsis. Nat. Genet. 48, 687–693 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Heo, J. B. & Sung, S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76–79 (2011).

    CAS  PubMed  Google Scholar 

  25. Cui, X. et al. REF6 recognizes a specific DNA sequence to demethylate H3K27me3 and regulate organ boundary formation in Arabidopsis. Nat. Genet. 48, 694–699 (2016).

    CAS  PubMed  Google Scholar 

  26. Molitor, A. et al. The Arabidopsis hnRNP-Q Protein LIF2 and the PRC1 subunit LHP1 function in concert to regulate the transcription of stress-responsive genes. Plant Cell 28, 2197–2211 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Derkacheva, M. et al. Arabidopsis MSI1 connects LHP1 to PRC2 complexes. EMBO J. 32, 2073–2085 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Molitor, A. M., Bu, Z., Yu, Y. & Shen, W. H. Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes. PLoS Genet. 10, e1004091 (2014).

    PubMed  PubMed Central  Google Scholar 

  29. Liang, S. C. et al. Kicking against the PRCs – a domesticated transposase antagonises silencing mediated by Polycomb group proteins and is an accessory component of Polycomb repressive complex 2. PLoS Genet. 11, e1005660 (2015).

    PubMed  PubMed Central  Google Scholar 

  30. Schmitges, F. W. et al. Histone methylation by PRC2 is inhibited by active chromatin marks. Mol. Cell 42, 330–341 (2011).

    CAS  PubMed  Google Scholar 

  31. Qüesta, J. I., Song, J., Geraldo, N., An, H. & Dean, C. Arabidopsis transcriptional repressor VAL1 triggers Polycomb silencing at FLC during vernalization. Science 353, 485–488 (2016).

    PubMed  Google Scholar 

  32. Zhang, X., Bernatavichute, Y. V., Cokus, S., Pellegrini, M. & Jacobsen, S. E. Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol. 10, R62 (2009).

    PubMed  PubMed Central  Google Scholar 

  33. Alvarez-Venegas, R. et al. ATX-1, an Arabidopsis homolog of trithorax, activates flower homeotic genes. Curr. Biol. 13, 627–637 (2003).

    CAS  PubMed  Google Scholar 

  34. Kotake, T., Takada, S., Nakahigashi, K., Ohto, M. & Goto, K. Arabidopsis TERMINAL FLOWER 2 gene encodes a heterochromatin protein 1 homolog and represses both FLOWERING LOCUS T to regulate flowering time and several floral homeotic genes. Plant Cell Physiol. 44, 555–564 (2003).

    CAS  PubMed  Google Scholar 

  35. Sung, S. et al. Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat. Genet. 38, 706–710 (2006).

    CAS  PubMed  Google Scholar 

  36. Gu, X. et al. Arabidopsis FLC clade members form flowering-repressor complexes coordinating responses to endogenous and environmental cues. Nat. Commun. 4, 1947 (2013).

    PubMed  Google Scholar 

  37. Schönrock, N. et al. Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway. Genes Dev. 20, 1667–1678 (2006).

    PubMed  PubMed Central  Google Scholar 

  38. Pien, S. et al. ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell 20, 580–588 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Lee, L. Y., Fang, M. J., Kuang, L. Y. & Gelvin, S. B. Vectors for multi-color bimolecular fluorescence complementation to investigate protein-protein interactions in living plant cells. Plant Methods 4, 24 (2008).

    PubMed  PubMed Central  Google Scholar 

  40. Jiang, D., Kong, N. C., Gu, X., Li, Z. & He, Y. Arabidopsis COMPASS-like complexes mediate histone H3 lysine-4 trimethylation to control floral transition and plant development. PLoS Genet. 7, e1001330 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Wysocka, J. et al. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121, 859–872 (2005).

    CAS  PubMed  Google Scholar 

  42. Curtis, M. D. & Grossniklaus, U. A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133, 462–469 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Hajdukiewicz, P., Svab, Z. & Maliga, P. The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol. Biol. 25, 989–994 (1994).

    CAS  PubMed  Google Scholar 

  44. Karimi, M., De Meyer, B. & Hilson, P. Modular cloning in plant cells. Trends Plant Sci. 10, 103–105 (2005).

    CAS  PubMed  Google Scholar 

  45. Jiang, D., Wang, Y., Wang, Y. & He, Y. Repression of FLOWERING LOCUS C and FLOWERING LOCUS T by the Arabidopsis Polycomb repressive complex 2 components. PLoS One 3, e3404 (2008).

    PubMed  PubMed Central  Google Scholar 

  46. Johnson, L., Cao, X. & Jacobsen, S. Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr. Biol. 12, 1360–1367 (2002).

    CAS  PubMed  Google Scholar 

  47. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

    PubMed  PubMed Central  Google Scholar 

  50. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).

    PubMed  PubMed Central  Google Scholar 

  51. Yu, G., Wang, L. G. & He, Q. Y. ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics 31, 2382–2383 (2015).

    CAS  PubMed  Google Scholar 

  52. Ramírez, F. et al. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res. 44, W160–W165 (2016). W1.

    PubMed  PubMed Central  Google Scholar 

  53. Quinlan, A. R. & Hall, I. M. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26, 841–842 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Hahne, F. & Ivanek, R. Visualizing genomic data using Gviz and Bioconductor. in Statistical Genomics. Methods in Molecular Biology Vol. 1418 (eds. Mathé, E. & Davis, S.) (Humana, New York, 2016).

  55. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36 (2013).

    PubMed  PubMed Central  Google Scholar 

  56. Anders, S., Pyl, P. T. & Huber, W. HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169 (2015).

    CAS  PubMed  Google Scholar 

  57. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).

    CAS  PubMed  Google Scholar 

  58. Kumar, S., Stecher, G. & Tamura, K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank J. Du and X. Zhong for exchange of unpublished information; G. Xu, X. Gu, H. Zhang and the in-house genomics facility for assistance; and R. J. Schmitz for critically reading this manuscript. This work was supported in part by funding from the National Natural Science Foundation of China (grant no. 31721001) and the Chinese Academy of Sciences.

Author information

Author notes

  1. Yizhong Wang

    Present address: School of Life Sciences, Huazhong Normal University, Wuhan, China

  2. Renyi Liu

    Present address: Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fuzhou, China

  3. These authors contributed equally to this work: Xing Fu, Yizhong Wang.

Authors and Affiliations

  1. National Key Laboratory of Plant Molecular Genetics, Shanghai Center for Plant Stress Biology, CAS Center for Excellence in Molecular Plant Sciences, Chinese Academy of Sciences (CAS), Shanghai, China

    Zicong Li & Yuehui He

  2. Shanghai Center for Plant Stress Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China

    Xing Fu, Yizhong Wang & Renyi Liu

  3. Department of Biological Sciences, National University of Singapore, Singapore, Singapore

    Yizhong Wang & Yuehui He

Authors
  1. Zicong Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xing Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yizhong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Renyi Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuehui He
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Y.H. conceived and supervised the project. Z.L. and Y.W. performed the experimental work. X.F. and R.L. carried out all bioinformatic analyses. Z.L., X.F., Y.W., R.L. and Y.H. analyzed the data. Y.H. and Z.L. wrote the manuscript.

Corresponding author

Correspondence to Yuehui He.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Figures

Supplementary Figures 1–14 and Supplementary Table 3

Reporting Summary

Supplementary Table 1

List of genes differentially expressed in lhp1, ebs shl, ebs shl lhp1 and emf1, compared to WT seedlings

Supplementary Table 2

List of genes occupied by SHL and EBS at a seedling stage

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, Z., Fu, X., Wang, Y. et al. Polycomb-mediated gene silencing by the BAH–EMF1 complex in plants. Nat Genet 50, 1254–1261 (2018). https://doi.org/10.1038/s41588-018-0190-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41588-018-0190-0

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing