Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases (2024)

Table of Contents
Subjects Abstract Access options Additional access options: Similar content being viewed by others Distinct roles of Arabidopsis ORC1 proteins in DNA replication and heterochromatic H3K27me1 deposition Histone chaperone ASF1 mediates H3.3-H4 deposition in Arabidopsis DREAM complex suppresses DNA methylation maintenance genes and precludes DNA hypermethylation Accession codes Primary accessions Data deposits Change history References Acknowledgements Author information Authors and Affiliations Contributions Corresponding authors Ethics declarations Competing interests Supplementary information Supplementary Information PowerPoint slides PowerPoint slide for Fig. 1 PowerPoint slide for Fig. 2 PowerPoint slide for Fig. 3 PowerPoint slide for Fig. 4 Rights and permissions About this article Cite this article This article is cited by Distinct roles of Arabidopsis ORC1 proteins in DNA replication and heterochromatic H3K27me1 deposition Regulation of gene editing using T-DNA concatenation H3.1K27me1 loss confers Arabidopsis resistance to Geminivirus by sequestering DNA repair proteins onto host genome NODeJ: an ImageJ plugin for 3D segmentation of nuclear objects The histone variant H2A.W and linker histone H1 co-regulate heterochromatin accessibility and DNA methylation Comments Editorial Summary DNA replication: applying the brakes
  • Letter
  • Published:
  • Yannick Jacob1na1,
  • Hume Stroud2na1,
  • Chantal LeBlanc1,
  • Suhua Feng3,
  • Luting Zhuo1,
  • Elena Caro2,
  • Christiane Hassel1,
  • Crisanto Gutierrez4,
  • Scott D. Michaels1 &
  • …
  • Steven E. Jacobsen2,3

Nature volume466,pages 987–991 (2010)Cite this article

  • 5521 Accesses

  • 137 Citations

  • Metrics details

Subjects

  • DNA replication
  • DNA transposable elements
  • Plant development

This article has been updated

Abstract

Multiple pathways prevent DNA replication from occurring more than once per cell cycle1. These pathways block re-replication by strictly controlling the activity of pre-replication complexes, which assemble at specific sites in the genome called origins. Here we show that mutations in the hom*ologous histone 3 lysine 27 (H3K27) monomethyltransferases, ARABIDOPSIS TRITHORAX-RELATED PROTEIN5 (ATXR5) and ATXR6, lead to re-replication of specific genomic locations. Most of these locations correspond to transposons and other repetitive and silent elements of the Arabidopsis genome. These sites also correspond to high levels of H3K27 monomethylation, and mutation of the catalytic SET domain is sufficient to cause the re-replication defect. Mutation of ATXR5 and ATXR6 also causes upregulation of transposon expression and has pleiotropic effects on plant development. These results uncover a novel pathway that prevents over-replication of heterochromatin in Arabidopsis.

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

Access options

Access through your institution

Change institution

Buy or subscribe

Subscribe to this journal

Receive 51 print issues and online access

$199.00 per year

only $3.90 per issue

Learn more

Buy this article

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

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

Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases (1)
Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases (2)
Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases (3)
Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases (4)

Similar content being viewed by others

Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases (5)

Distinct roles of Arabidopsis ORC1 proteins in DNA replication and heterochromatic H3K27me1 deposition

Article Open access 07 March 2023

Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases (6)

Histone chaperone ASF1 mediates H3.3-H4 deposition in Arabidopsis

Article Open access 15 November 2022

Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases (7)

DREAM complex suppresses DNA methylation maintenance genes and precludes DNA hypermethylation

Article 13 July 2020

Accession codes

Primary accessions

Gene Expression Omnibus

Data deposits

Sequencing files have been deposited at GEO (accession codes GSE22411 and GSE21673).

See Also
Genome-wide maps of chromatin state in pluripotent and lineage-committed cells

Change history

References

  1. Arias, E. E. & Walter, J. C. Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev. 21, 497–518 (2007)

    Article CAS Google Scholar

  2. Jacob, Y. et al. ATXR5 and ATXR6 are H3K27 monomethyltransferases required for chromatin structure and gene silencing. Nature Struct. Mol. Biol. 16, 763–768 (2009)

    Article CAS Google Scholar

  3. Raynaud, C. et al. Two cell-cycle regulated SET-domain proteins interact with proliferating cell nuclear antigen (PCNA) in Arabidopsis. Plant J. 47, 395–407 (2006)

    Article CAS Google Scholar

  4. Jackson, J. P., Lindroth, A. M., Cao, X. & Jacobsen, S. E. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416, 556–560 (2002)

    Article ADS CAS Google Scholar

  5. Malagnac, F., Bartee, L. & Bender, J. An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J. 21, 6842–6852 (2002)

    Article CAS Google Scholar

  6. Bernatavichute, Y. V., Zhang, X., co*kus, S., Pellegrini, M. & Jacobsen, S. E. Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS ONE 3, e3156 (2008)

    Article ADS Google Scholar

  7. Obayashi, T., Hayashi, S., Saeki, M., Ohta, H. & Kinosh*ta, K. ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res. 37, D987–D991 (2009)

    Article CAS Google Scholar

  8. Moldovan, G. L., Pfander, B. & Jentsch, S. PCNA, the maestro of the replication fork. Cell 129, 665–679 (2007)

    Article CAS Google Scholar

  9. Galbraith, D. W., Harkins, K. R. & Knapp, S. Systemic endopolyploidy in Arabidopsis thaliana. Plant Physiol. 96, 985–989 (1991)

    Article CAS Google Scholar

  10. Caro, E., Desvoyes, B., Ramirez-Parra, E., Sanchez, M. P. & Gutierrez, C. Endoreduplication control during plant development. SEB Exp. Biol. Ser. 59, 167–187 (2008)

    CAS PubMed Google Scholar

  11. 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 Google Scholar

  12. Fransz, P., ten Hoopen, R. & Tessadori, F. Composition and formation of heterochromatin in Arabidopsis thaliana. Chromosome Res. 14, 71–82 (2006)

    Article CAS Google Scholar

  13. Soppe, W. J. et al. DNA methylation controls histone H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J. 21, 6549–6559 (2002)

    Article CAS Google Scholar

  14. Pauler, F. M. et al. H3K27me3 forms BLOCs over silent genes and intergenic regions and specifies a histone banding pattern on a mouse autosomal chromosome. Genome Res. 19, 221–233 (2009)

    Article CAS Google Scholar

  15. Gomez, M. Controlled rereplication at DNA replication origins. Cell Cycle 7, 1313–1314 (2008)

    Article CAS Google Scholar

  16. Fuchs, J., Demidov, D., Houben, A. & Schubert, I. Chromosomal histone modification patterns—from conservation to diversity. Trends Plant Sci. 11, 199–208 (2006)

    Article CAS Google Scholar

  17. Lindroth, A. M. et al. Dual histone H3 methylation marks at lysines 9 and 27 required for interaction with CHROMOMETHYLASE3. EMBO J. 23, 4146–4155 (2004)

    Article Google Scholar

  18. Mathieu, O., Probst, A. V. & Paszkowski, J. Distinct regulation of histone H3 methylation at lysines 27 and 9 by CpG methylation in Arabidopsis. EMBO J. 24, 2783–2791 (2005)

    Article CAS Google Scholar

  19. Musselman, C. A. & Kutateladze, T. G. PHD fingers: epigenetic effectors and potential drug targets. Mol. Interv. 9, 314–323 (2009)

    Article CAS Google Scholar

  20. Zhang, X., Bernatavichute, Y. V., co*kus, 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)

    Article Google Scholar

  21. Jiang, H. & Wong, W. H. SeqMap: mapping massive amount of oligonucleotides to the genome. Bioinformatics 24, 2395–2396 (2008)

    Article CAS Google Scholar

  22. Davidson, I. F., Li, A. & Blow, J. J. Deregulated replication licensing causes DNA fragmentation consistent with head-to-tail fork collision. Mol. Cell 24, 433–443 (2006)

    Article CAS Google Scholar

  23. Vongs, A., Kakutani, T., Martienssen, R. A. & Richards, E. J. Arabidopsis thaliana DNA methylation mutants. Science 260, 1926–1928 (1993)

    Article ADS CAS Google Scholar

  24. Lan, F. et al. Recognition of unmethylated histone H3 lysine 4 links BHC80 to LSD1-mediated gene repression. Nature 448, 718–722 (2007)

    Article ADS CAS Google Scholar

  25. Dillon, S. C., Zhang, X., Trievel, R. C. & Cheng, X. The SET-domain protein superfamily: protein lysine methyltransferases. Genome Biol. 6, 227 (2005)

    Article Google Scholar

  26. Joshi, P. et al. Dominant alleles identify SET domain residues required for histone methyltransferase of Polycomb repressive complex 2. J. Biol. Chem. 283, 27757–27766 (2008)

    Article CAS Google Scholar

  27. Earley, K. W. et al. Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616–629 (2006)

    Article CAS Google Scholar

  28. Curtis, M. D. & Grossniklaus, U. A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta[w]. Plant Physiol. 133, 462–469 (2003)

    Article CAS Google Scholar

  29. Shi, X. et al. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442, 96 (2006)

    Article ADS CAS Google Scholar

Download references

Acknowledgements

We thank G. Lambert and D. Galbraith for assistance with flow cytometry; Y. Bernatavichute for assistance with ChIP experiments; and M. Pellegrini and S. co*kus for advice on data analyses. Y.J. was supported by a fellowship from Le Fonds Québécois de la Recherche sur la Nature et les Technologies (FQRNT). S.F. is a Howard Hughes Medical Institute Fellow of the Life Science Research Foundation. Research in the Michaels’ laboratory was supported by grants from the National Institutes of Health (GM075060), the Indiana METACyt Initiative of Indiana University, and the Lilly Endowment, Inc. C.G. was supported by grants from the Spanish Ministry of Science and Innovation (BFU2009-9783 and CSD2007-57B). S.E.J. is an investigator of the Howard Hughes Medical Institute.

Author information

Author notes

  1. Yannick Jacob and Hume Stroud: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Biology, Indiana University, 915 East Third Street, Bloomington, 47405, Indiana, USA

    Yannick Jacob,Chantal LeBlanc,Luting Zhuo,Christiane Hassel&Scott D. Michaels

  2. Department of Molecular, Cell and Developmental Biology, University of California, Los Angeles, Los Angeles, 90095, California, USA

    Hume Stroud,Elena Caro&Steven E. Jacobsen

  3. Howard Hughes Medical Institute, University of California, Los Angeles, Los Angeles, 90095, California, USA

    Suhua Feng&Steven E. Jacobsen

  4. Centro de Biologia Molecular Severo Ochoa, Consejo Superior de Investigaciones Cientificas, Universidad Autonoma de Madrid, Nicolas Cabrera 1, Cantoblanco, Madrid 28049, Spain,

    Crisanto Gutierrez

Authors

  1. Yannick Jacob

    View author publications

    You can also search for this author in PubMedGoogle Scholar

  2. Hume Stroud

    View author publications

    You can also search for this author in PubMedGoogle Scholar

  3. Chantal LeBlanc

    View author publications

    You can also search for this author in PubMedGoogle Scholar

  4. Suhua Feng

    View author publications

    You can also search for this author in PubMedGoogle Scholar

  5. Luting Zhuo

    View author publications

    You can also search for this author in PubMedGoogle Scholar

  6. Elena Caro

    View author publications

    You can also search for this author in PubMedGoogle Scholar

  7. Christiane Hassel

    View author publications

    You can also search for this author in PubMedGoogle Scholar

  8. Crisanto Gutierrez

    View author publications

    You can also search for this author in PubMedGoogle Scholar

  9. Scott D. Michaels

    View author publications

    You can also search for this author in PubMedGoogle Scholar

  10. Steven E. Jacobsen

    View author publications

    You can also search for this author in PubMedGoogle Scholar

Contributions

S.D.M., S.E.J. and C.G. directed the research. Y.J., H.S., C.L., S.F., L.Z., E.C. and C.H. performed experiments. H.S. analysed data. H.S., Y.J., S.E.J. and S.D.M. prepared the manuscript.

Corresponding authors

Correspondence to Scott D. Michaels or Steven E. Jacobsen.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Figures 1-7 with legends and Supplementary Tables 1-2. (PDF 2244 kb)

Rights and permissions

About this article

Cite this article

Jacob, Y., Stroud, H., LeBlanc, C. et al. Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases. Nature 466, 987–991 (2010). https://doi.org/10.1038/nature09290

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature09290

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Access through your institution

Change institution

Buy or subscribe

Editorial Summary

DNA replication: applying the brakes

It is important for the normal function of a cell that DNA replication takes place only once per cell cycle, and various mechanisms exist to prevent its repetition. Another mechanism has been shown to operate in Arabidopsis, this one surprisingly involving two histone (H3K27) monomethyltansferases, ATXR5 and ATXR6. Mutations in the genes encoding these two enzymes lead to re-replication of specific genomic locations, the majority of which correspond to transposons and other repetitive and silenced elements. ATXR5 and ATXR6 are proposed to be components of a pathway required to prevent over-replication of heterochromatin in Arabidopsis.

Advertisem*nt

Regulation of heterochromatic DNA replication by histone H3 lysine 27 methyltransferases (2024)
Top Articles
Spread the Love with 15 Valentine's Day Classroom Activities
Easy Vegan Pecan Pie — The BEST Classic Pecan Pie Recipe!
Ashcroft → Toronto Train: from US$405 | VIA Rail Canada | Busbud
Dutch Railways Guide | Rail Network Netherlands NS Trains Travel
Schiphol Duty Free Catalogue
Busted Newspaper Lawrence County KY Arrests
Bbc Numberblocks
Why Y bye-bye? Is the Y chromosome disappearing and will men really go extinct? — Genetics Unzipped
True West 2017-12 - PDF Free Download
Players Tour Player of the Year Boys Players Tour Player of the Year - Standings
Lifetalent Healthstream Lifepoint
University Of Minnesota Duluth Women's Basketball Schedule
Latest Posts
South African Curry and Rice - aninas recipes
Elderberry Syrup Gummies Recipe
Article information

Author: Twana Towne Ret

Last Updated:

Views: 5572

Rating: 4.3 / 5 (44 voted)

Reviews: 83% of readers found this page helpful

Author information

Name: Twana Towne Ret

Birthday: 1994-03-19

Address: Apt. 990 97439 Corwin Motorway, Port Eliseoburgh, NM 99144-2618

Phone: +5958753152963

Job: National Specialist

Hobby: Kayaking, Photography, Skydiving, Embroidery, Leather crafting, Orienteering, Cooking

Introduction: My name is Twana Towne Ret, I am a famous, talented, joyous, perfect, powerful, inquisitive, lovely person who loves writing and wants to share my knowledge and understanding with you.