Skip to main content
SpringerLink
Log in

The dynamics of histone H3 modifications is species-specific in plant meiosis

  • Original Paper
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Different histone modifications often modify DNA-histone interactions affecting both local and global structure of chromatin, thereby providing a vast potential for functional responses. Most studies have focused on the role of several modifications in gene transcription regulation, being scarce on other aspects of eukaryotic chromosome structure during cell division, mainly in meiosis. To solve this issue we have performed a cytological analysis to determine the chromosomal distribution of several histone H3 modifications throughout all phases of both mitosis and meiosis in different plant species. We have chosen Aegilops sp. and Secale cereale (monocots) and Arabidopsis thaliana (dicots) because they differ in their phylogenetic affiliation as well as in content and distribution of constitutive heterochromatin. In the species analyzed, the patterns of H3 acetylation and methylation were held constant through mitosis, including modifications associated with “open chromatin”. Likewise, the immunolabeling patterns of H3 methylation remained invariable throughout meiosis in all cases. On the contrary, there was a total loss of acetylated H3 immunosignals on condensed chromosomes in both meiotic divisions, but only in monocot species. Regarding the phosphorylation of histone H3 at Ser10, present on condensed chromosomes, although we did not observe any difference in the dynamics, we found slight differences between the chromosomal distribution of this modification between Arabidopsis and cereals (Aegilops sp. and rye). Thus far, in plants chromosome condensation throughout cell division appears to be associated with a particular combination of H3 modifications. Moreover, the distribution and dynamics of these modifications seem to be species-specific and even differ between mitosis and meiosis in the same species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

BSA:

Bovine serum albumin

DAPI:

4′,6-Diamidino-2-phenylindole

H3K9K14ac:

Histone H3 acetylation at lysine 9 and/or lysine 14

H3K4me2:

Histone H3 di-methylation at lysine 4

H3K4me3:

Histone H3 tri-methylation at lysine 4

H3K9me2:

Histone H3 di-methylation at lysine 9

H3K27me3:

Histone H3 tri-methylation at lysine 27

H3S10ph:

Histone H3 phosphorylation at serine 10

PBS :

Phosphate-Buffered Saline

L:

Leptotene

Z:

Zygotene

P:

Pachytene

Dp:

Diplotene

Dk:

Diakinesis

MI:

Metaphase I

AI:

Anaphase I

TI:

Telophase I

Dd:

Dyad

PII:

Prophase II

MII:

Metaphase II

AII:

Anaphase II

TIIt:

Telophase II

Td:

Tetrad

I:

Interphase

I*:

Interphase of tapetum binucleated cells

P:

Prophase

M:

Metaphase

A:

Anaphase

T:

Telophase

References

  • Ambros P, Schweizer D (1976) The Giemsa C-banded karyotype of Arabidopsis thaliana (L.) Heynh. Arabidopsis Inf Serv 13:167–171

    Google Scholar 

  • Bauwens S, Vanoostveldt P, Engler G, Vanmontagu M (1991) Distribution of the rDNA and three classes of highly repetitive DNA in the chromatin of interphase nuclei of Arabidopsis thaliana. Chromosoma 101:41–48

    Article  PubMed  CAS  Google Scholar 

  • Bennett MD, Leitch IJ (2005) Nuclear DNA amounts in angiosperms—progress, problems and prospects. Ann Bot 95:45–90

    Article  PubMed  CAS  Google Scholar 

  • Belyaev ND, Houben A, Baranczewski P, Schubert I (1998) The acetylation patterns of histones H3 and H4 along Vicia faba chromosomes are different. Chromosome Res 6:59-63

    Google Scholar 

  • Berke L, Sanchez-Perez GF, Snel B (2012) Contribution of the epigenetic mark H3K27me3 to functional divergence after whole genome duplication in Arabidopsis. Genome Biol 13:R94

    Article  PubMed  CAS  Google Scholar 

  • Borde V, Robine N, Lin W, Bonfils S, Géli V, Nicolas A (2009) Histone H3 lysine 4 trimethylation marks meiotic recombination initiation sites. EMBO J 28:99–111

    Article  PubMed  CAS  Google Scholar 

  • Buard J, Barthès P, Grey C, de Massy B (2009) Distinct histone modifications define initiation and repair of meiotic recombination in the mouse. EMBO J 28:2616–2624

    Article  PubMed  CAS  Google Scholar 

  • Cermeño MC, Cuñado N, Orellana J (1985) Meiotic behavior of Un, D and R genomes in the amphidiploid Aegilops ventricosa–Secale cereale and the parental species. Theor Appl Genet 70:679–683

    Article  Google Scholar 

  • Cerutti H, Casas-Mollano JA (2009) Histone H3 phosphorylation. Universal code or lineage specific dialects? Epigenetics 4:71–75

    Article  PubMed  CAS  Google Scholar 

  • Cuñado N (1992) Analysis of metaphase I chromosome association in species of the genus Aegilops. Theor Appl Genet 85:283–292

    Google Scholar 

  • Dong X, Reimer J, Gobel U, Engelhorn J, He F, Schoof H, Turck F (2012) Natural variation of H3K27me3 distribution between two Arabidopsis accessions and its association with flanking transposable elements. Genome Biol 13:R117

    Article  PubMed  Google Scholar 

  • Fischle W, Wang Y, Allis CD (2003) Histone and chromatin cross-talk. Curr Op Cell Biol 15:172-183

    Google Scholar 

  • Flavell RB, Bennett MD, Smith JB, Smith DB (1974) Genome size and the proportion of repeated nucleotide sequence DNA in plants. Biochem Genet 12:257–279

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Granot G, Sikron-Persi N, Li Y, Grafi G (2009) Phosphorylated H3S10 occurs in distinct regions of the nucleolus in differentiated leaf cells. Biochim Biophys Acta 1789:220–224

    Article  PubMed  CAS  Google Scholar 

  • Hernández-Hernández A, Ortiz R, Ubaldo E, Echeverría-Martínez OM, Vázquez-Nin GH, Recillas-Targa F (2010) Synaptonemal complex stability depends on repressive histone marks of the lateral element-associated repeat sequences. Chromosoma 119:41–58

    Article  PubMed  Google Scholar 

  • Heslop-Harrison JS, Schwarzacher T (2011) Organisation of the plant genome in chromosomes. Plant J 66:18–33

    Article  PubMed  CAS  Google Scholar 

  • Houben A, Wako T, Furushima-Shimogawara R et al (1999) The cell cycle dependent phosphorylation of histone H3 is correlated with the condensation of plant mitotic chromosomes. Plant J 19:1–5

    Article  Google Scholar 

  • Houben A, Demidov D, Gernand D, Meister A, Leach CR, Schubert I (2003) Methylation of histone H3 in euchromatin of plant chromosomes depends on basis nuclear DNA Content. Plant J 33:967–973

    Article  PubMed  CAS  Google Scholar 

  • Jasencakova Z, Meister A, Schubert I (2001) Chromatin organization and its relation to replication and histone acetylation during the cell cycle in barley. Chromosoma 110:83–92

    Article  PubMed  CAS  Google Scholar 

  • Jasencakova Z, Soppe WJJ, Meister A, Gernand D, Turner BM, Schubert I (2003) Histone modifications in Arabidopsis—high methylation of H3 lysine 9 is dispensable for constitutive heterochromatin. Plant J 33:471–480

    Article  PubMed  CAS  Google Scholar 

  • Kaszás E, Cande WZ (2000) Phosphorylation of histone H3 is correlated with changes in the maintenance of sister chromatid cohesion during meiosis in maize, rather than the condensation of the chromatin. J Cell Sci 113:3217–3226

    PubMed  Google Scholar 

  • Kheir TB, Lund AH (2010) Epigenetic dynamics across the cell cycle. Essays Biochem 48:107–120

    Article  CAS  Google Scholar 

  • Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705

    Article  PubMed  CAS  Google Scholar 

  • Lachner M, Sengupta R, Schotta G, Jenuwein T (2004) Trilogies of histone lysine methylation as epigenetic landmarks of the eukaryotic genome. Cold Spring Harb Symp Quant Biol 69:209–218

    Article  PubMed  CAS  Google Scholar 

  • Lauria M, Rossi V (2011) Epigenetic control of gene regulation in plants. Biochim Biophys Acta 1809:369–378

    Article  PubMed  CAS  Google Scholar 

  • Leutwiler LS, Hough-Evans BR, Meyerowitz EM (1984) The DNA of Arabidopsis thaliana. Mol Genet Genom 194:15–23

    Article  CAS  Google Scholar 

  • Li Y, Butenko Y, Grafi G (2005) Histone deacetylation is required for progression through mitosis in tobacco cells. Plant J 41:346–352

    Article  PubMed  CAS  Google Scholar 

  • Loidl P (2004) A plant dialect of the histone language. Trends Plant Sci 9:84–90

    Article  PubMed  CAS  Google Scholar 

  • López E, Pradillo M, Romero C, Santos JL, Cuñado N (2008) Pairing and synapsis in wild type Arabidopsis thaliana. Chromosome Res 16:701–708

    Article  PubMed  Google Scholar 

  • Maluszynska J, Heslop-Harrison JS (1991) Location of tandemly repeated DNA sequences in Arabidopsis thaliana. Plant J 1:159–166

    Article  Google Scholar 

  • Manzanero S, Arana P, Puertas MJ, Houben A (2000) The chromosomal distribution of phosphorylated histone H3 differs between plants and animals at meiosis. Chromosoma 109:308–317

    Article  PubMed  CAS  Google Scholar 

  • Pérez-Cadahía B, Drobic B, Davie JR (2009) H3 phosphorylation: dual role in mitosis and interphase. Biochem Cell Biol 87:695–709

    Article  PubMed  Google Scholar 

  • Perrella G, Consiglio MF, Aiese-Cigliano R et al (2010) Histone hyperacetylation affects meiotic recombination and chromosome segregation in Arabidopsis. Plant J 62:796–806

    Article  PubMed  CAS  Google Scholar 

  • Pfluger J, Wagner D (2007) Histone modifications and dynamic regulation of genome accessibility in plants. Curr Op Plant Biol 6:645–652

    Article  Google Scholar 

  • Prigent C, Dimitrov S (2003) Phosphorylation of serine 10 in histone H3, what for? J Cell Sci 116:3677–3685

    Article  PubMed  CAS  Google Scholar 

  • Probst AV, Fagard M, Proux F et al (2004) Arabidopsis histone deacetylase HDA6 is required for maintenance of transcriptional gene silencing and determines nuclear organization of rDNA repeats. Plant Cell 16:1021–1034

    Article  PubMed  CAS  Google Scholar 

  • Roudier F, Teixeira FK, Colot V (2009) Chromatin indexing in Arabidopsis: an epigenomic tale of tails and more. Trends Genet 25:511–517

    Article  PubMed  CAS  Google Scholar 

  • Roudier F, Ikhlak A, Caroline B et al (2011) Integrative epigenomic mapping define four main chromatin states in Arabidopsis. EMBO J 30:1928–1938

    Article  PubMed  CAS  Google Scholar 

  • Soppe WJ, Jasencakova Z, Houben A et al (2002) DNA methylation controls H3 lysine 9 methylation and heterochromatin assembly in Arabidopsis. EMBO J 21:6549–6559

    Article  PubMed  CAS  Google Scholar 

  • Teoh SB, Hutchinson J (1983) Interspecific variation in C-banded chromosomes of diploid Aegilops species. Theor Appl Genet 65:31–40

    Google Scholar 

  • Van Hooser A, Goodrich DW, Allis CD, Brinkley BR, Mancini MA (1998) Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation. J Cell Sci 111:3497–3506

    PubMed  Google Scholar 

  • Wako T, Fukuda M, Furushima-Shimogawara R, Belyaev ND, Fukui K (2002) Cell cycle-dependent and lysine residue-specific dynamic changes of histone H4 acetylation in barley. Plant Mol Biol 49:645–653

    Article  PubMed  CAS  Google Scholar 

  • Wei Y, Mizzen CA, Cook RG, Gorovsky MA, Allis CD (1998) Phosphorylation of histone H3 Serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc Natl Acad Sci USA 95:7480–7484

    Article  PubMed  CAS  Google Scholar 

  • Wei Y, Yu L, Bowen J, Gorovsky MA, Allis CD (1999) Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 97:99–109

    Article  PubMed  CAS  Google Scholar 

  • Xu D, Bai J, Duan Q, Costa M, Dai W (2009) Covalent modifications of histones during mitosis and meiosis. Cell Cycle 8:3688–3694

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Bernatavichute YV, Cokus S, Pellegrini M, Jacobsen SE (2009) Genome-wide analysis of mono-, di- and trimethylation of histone H3 lysine 4 in Arabidopsis thaliana. Genome Biol 10:R62

    Article  PubMed  Google Scholar 

  • Zickler D, Kleckner N (1999) Meiotic chromosomes: integrating structure and function. Annu Rev Genet 33:603–754

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Ministerio de Ciencia e Innovación of Spain [Grant number BFU2008-00459/BMC], the Universidad Complutense-Banco Santander of Spain [Grant number 910452] and the European Union Framework Program 7 [Meiosys-KBBE-2009-222883].

Author information

Authors and Affiliations

  1. Departamento de Genética, Facultad de Biología, Universidad Complutense, C/José Antonio Nováis 12, 28040, Madrid, Spain

    Cecilia Oliver, Mónica Pradillo, Eduardo Corredor & Nieves Cuñado

Authors
  1. Cecilia Oliver
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mónica Pradillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eduardo Corredor
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nieves Cuñado
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nieves Cuñado.

Electronic supplementary material

Below is the link to the electronic supplementary material.

425_2013_1885_MOESM1_ESM.tif

Fig. S1 Dynamics of histone H3K9K14ac immunosignals during most of the stages of mitosis and meiosis in Arabidopsis thaliana (a-k), Aegilops uniaristata (l-n, p-q, s-t, v), and Ae. ventricosa- Secale cereale amphiploid (o, r, u). Left: Immunostaining with antibodies against H3K9K14ac (green). Middle: Nuclei counterstained with DAPI (gray). Right: Merge, DAPI shown in red. Bars represent 10 µm. A. thaliana. Mitosis: interphase and metaphase cells (a), anaphase (b); Meiosis: zygotene (c), pachytene (d), diplotene (e), diakinesis (f), anaphase I (g), dyad (h), metaphase II (i), anaphase II (j), tetrad (k).Ae. uniaristata (l-n, p-q, s-t, v) and Ae. ventricosa- S. cereale amphiploid (o, r, u). Mitosis: interphase and anaphase cells (l), metaphase (m); Meiosis: zygotene (n), zygotene-pachytene (o), diplotene and an arrowhead indicates one pro-metaphase I (p), metaphase I (q), metaphase I (r, arrowheads indicate some univalents), anaphase I (s), dyad (t), late prophase II (u), anaphase-telophase II (v) (TIFF 38172 kb)

425_2013_1885_MOESM2_ESM.tif

Fig. S2 Chromosomal distribution of histone H3K9me2 inmunosignals through mitosis and meiosis in Arabidopsis thaliana (a-i), Aegilops ventricosa (j-l), and Ae. uniaristata (m-r). Left: Immunostaining with antibodies against H3K9me2 (green). Middle: Nuclei counterstained with DAPI (gray). Right: Merge, DAPI shown in red. Bars represent 10 µm. A. thaliana. Mitosis: metaphase (a); Meiosis: leptotene (b), zygotene (c), pachytene (d), diplotene-diakinesis (e), metaphase I (f), several dyads (g), metaphase II (h), tetrads (i). Ae. ventricosa (j-l) and Ae. uniaristata (m-r). Mitosis: interphase of tapetum binucleated cell (j), metaphase (k), anaphase (l); Meiosis: zygotene (m), diplotene-diakinesis (n), metaphase I (o), anaphase I (p), late prophase II (q), metaphase II (r) (TIFF 32163 kb)

425_2013_1885_MOESM3_ESM.tif

Fig. S3 Distribution of histone H3K27me3 during most of the phases of mitosis and meiosis in Arabidopsis thaliana (a-j), Aegilops cylindrica x Ae. caudata hybrid (k-p), and Ae. uniaristata (q-t). Left: Immunostaining with antibodies against H3K27me3 (green). Middle: Nuclei counterstained with DAPI (gray). Right: Merge, DAPI shown in red. Bars represent 10 µm. A. thaliana. Mitosis: late prophase (a), metaphase (b), anaphase and interphase nuclei (c); Meiosis: leptotene (d), zygotene-pachytene (e), diplotene-diakinesis (f), metaphase I (g), dyad (h), metaphase II (i), tetrad (j). Ae. cylindrica x Ae. caudata hybrid (k-p) and Ae. uniaristata (q-t). Mitosis: interphase of tapetum binucleated cells (k), metaphase and anaphase (l); Meiosis: leptotene (m), zygotene (n), diplotene (o), diakinesis and metaphase I (p, arrowheads indicate some univalents), telophase I (q), late prophase II (r), anaphase II (s), tetrad (t) (TIFF 34920 kb)

425_2013_1885_MOESM4_ESM.tif

Fig. S4 Immunolocalization of histone H3K27me3 at representative meiotic stages of the amphiploid Aegilops ventricosa-Secale cereale: metaphase I (a, arrowheads indicate some univalents), anaphase I (b), dyad (c), metaphase II (d), anaphase II (e). Left: Immunostaining with antibodies against H3K27me3 (green). Middle: Nuclei counterstained with DAPI (gray). Right: Merge, DAPI shown in red. Bars represent 10 µm (TIFF 15440 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oliver, C., Pradillo, M., Corredor, E. et al. The dynamics of histone H3 modifications is species-specific in plant meiosis. Planta 238, 23–33 (2013). https://doi.org/10.1007/s00425-013-1885-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-013-1885-1

Keywords

Search

Navigation