A novel mitosis-specific phosphorylation site in histone H3 at threonine 11 has been described for mammalian cells. This modification is restricted to the centromeric region while phosphorylation at the classical H3 sites, Ser10 and Ser28 occurs along the entire chromosomal arms. Using phosphorylation state-specific antibodies we found that phosphorylation at threonine 11 occurs also in plant cells, during mitosis as well as meiosis. However, in contrast to animal cells, ph(Thr11)H3 was distributed along the entire length of condensed chromosomes, whereas H3 phosphorylated at Ser10 and Ser28 appeared to be restricted to centromeric/pericentromeric chromatin. Phosphorylation at Thr11 started in prophase and ended in telophase, it correlated with the condensation of mitotic and meiotic chromosomes and was independent of the distribution of late replicating heterochromatin and Giemsa-banding positive regions. Interestingly, treatment of cells with the phosphatase inhibitor cantharidin revealed a high level of Thr11 phosphorylation in interphase cells, in this case particularly in pericentromeric regions. These data show that histone modifications are highly dynamic. Moreover, animal and plant organisms may have evolved individual histone codes.    

1.
Crosio C, Fimia GM, Loury R, Kimura M, Okano Y, Zhou H, Sen S, Allis CD, Sassone-Corsi P: Mitotic phosphorylation of histone H3: spatio-temporal regulation by mammalian Aurora kinases. Mol Cell Biol 22:874–885 (2002).
2.
Döbel P, Schubert I, Rieger R: Distribution of heterochromatin in a reconstructed karyotype of Vicia faba as identified by banding and DNA-late replication patterns. Chromosoma 69:193–209 (1978).
3.
Fischle W, Wang Y, Allis CD: Histone and chromatin cross-talk. Curr Opin Cell Biol 15:172–183 (2003).
4.
Gernand D, Demidov D, Houben A: The temporal and spatial pattern of histone H3 phosphorylation at serine 28 and serine 10 is similar in plants but differs between mono- and polycentric chromosomes. Cytogenet Genome Res 101:172–176 (2003).
5.
Goto H, Tomono Y, Ajiro K, Kosako H, Fujita M, Sakurai M, Okawa K, Iwamatsu A, Okigaki T, Takahashi T, Inagaki M: Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J Biol Chem 274:25543–25549 (1999).
6.
Gurtley LR, Walters RA, Tobey RA: Sequential phosphorylation of histone subfractions in the Chinese hamster cell cycle. J Biol Chem 250:3936–3944 (1975).
7.
Hans F, Dimitrov S: Histone H3 phosphorylation and cell division. Oncogene 20:3021–3027 (2001).
8.
Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD: Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348–360 (1997).
9.
Houben A, Guttenbach M, Kress W, Pich U, Schubert I, Schmid M: Immunostaining and interphase arrangement of field bean kinetochores. Chromosome Res 3:27–31 (1995).
10.
Houben A, Wako T, Furushima-Shimogawara R, Presting G, Künzel G, Schubert I, Fukui K: The cell cycle dependent phosphorylation of histone H3 is correlated with the condensation of plant mitotic chromosomes. Plant J 18:675–679 (1999).
11.
Jasencakova Z, Soppe WJ, Meister A, Gernand D, Turner BM, Schubert I: Histone modifications in Arabidopsis – high methylation of H3 lysine 9 is dispensable for constitutive heterochromatin. Plant J 33:471–480 (2003).
12.
Kaszas E, Cande WZ: 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 (2000).
13.
Kogel D, Prehn JH, Scheidtmann KH: The DAP kinase family of pro-apoptotic proteins: novel players in the apoptotic game. Bioessays 23:352–358 (2001).
14.
MacKintosh C, MacKintosh RM: Inhibitors of protein kinases and phosphatases. Trends Biochem Sci 19:444–448 (1994).
15.
Manzanero S, Arana P, Puertas MJ, Houben A: The chromosomal distribution of phosphorylated histone H3 differs between plants and animals at meiosis. Chromosoma 109:308–317 (2000).
16.
Manzanero S, Rutten T, Kotseruba V, Houben A: Alterations in the distribution of histone H3 phosphorylation in mitotic plant chromosomes in response to cold treatment and the protein phosphatase inhibitor cantharidin. Chromosome Res 10:467–476 (2002).
17.
Pedrosa A, Jantsch MF, Moscone EA, Ambros PF, Schweizer D: Characterisation of pericentrometric and sticky intercalary heterochromatin in Ornithogalum longibracteatum (Hyacinthaceae). Chromosoma 110:203–213 (2001).
18.
Preuss U, Landsberg G, Scheidtmann KH: Novel mitosis-specific phosphorylation of histone H3 at Thr11 mediated by Dlk/ZIP kinase. Nucleic Acids Res 31:878–885 (2003).
19.
Prigent C, Dimitrov S: Phosphorylation of serine 10 in histone H3, what for? J Cell Sci 116:3677–3685 (2003).
20.
Rabl C: Zellteilung. Morphol Jahrb 10:214–330 (1885).
21.
Schlegel R, Gill BS: N-banding analysis of rye chromosomes and the relationship between N-banded and C-banded heterochromatin. Can J Genet Cytol 26:765–769 (1984).
22.
Schroeder-Reiter E, Houben A, Wanner G: Immunogold labeling of chromosomes for scanning electron microscopy: A closer look at phosphorylated histone H3 in mitotic metaphase chromosomes of Hordeum vulgare. Chromosome Res 11:585–596 (2003).
23.
Schubert I, Dolezel J, Houben A, Scherthan H, Wanner G: Refined examination of plant metaphase chromosome structure at different levels made feasible by new isolation methods. Chromosoma 102:96–101 (1993).
24.
Thomson S, Clayton AL, Hazzalin CA, Rose S, Barratt MJ, Mahadevan LC: The nucleosomal response associated with immediate-early gene induction is mediated via alternative MAP kinase cascades: MSK1 as a potential histone H3/HMG-14 kinase. EMBO J 18:4779–4793 (1999).
25.
Waterborg JH, Robertson AJ: Common features of analogous replacement histone H3 genes in animals and plants. J Mol Evol 43:194–206 (1996).
26.
Wei Y, Allis CD: A new marker for mitosis. Trends Cell Biol 8:266 (1998).
27.
Zeitlin SG, Barber CM, Allis CD, Sullivan KF, Sullivan K: Differential regulation of CENP-A and histone H3 phosphorylation in G2/M. J Cell Sci 114:653–661 (2001).
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