chromosomal histone modification patterns – from conservation to diversity

Chromosomal histone modificationpatterns – from conservationto diversityJorg Fuchs, Dmitri Demidov, Andreas Houben and Ingo Schubert

Leibniz-Institute of Plant Genetics and Crop Plant Research, Corrensstrasse 3, D-06466 Gatersleben, Germany

The organization of DNA into chromatin regulates

expression and maintenance (replication, repair, recom-

bination, segregation) of genetic information in a

dynamic manner. The N-terminal tails of the nucleoso-

mal core histones are subjected to post-translational

modifications such as acetylation, methylation, phos-

phorylation, ubiquitination, glycosylation, ADP-ribosy-

lation, carbonylation and sumoylation. These

modifications, together with DNA methylation, control

the folding of the nucleosomal array into higher order

structures and mediate signalling for cellular processes.

Although histones and their modifications are highly

conserved, recent data show that chromosomal distri-

bution of individual modifications (acetylation, methyl-

ation, phosphorylation) can differ along the cell cycle as

well as among and between groups of eukaryotes. This

implies the possibility of evolutionary divergence in

reading the ‘histone code’.

Introduction

Specific antibodies are invaluable tools for localizingdifferent types of histone modifications in situ. Theyrecognize a post-translationally modified amino acid inthe context of the surrounding amino acid sequence,although which variant of histone H3 is modified orwhether distinct modifications occur together on thesame histone molecule or separately on different histonemolecules cannot be distinguished. Here, we compare thedistribution of selected histone modifications alongchromosomes during the cell cycle in plant species thatdiffer in genome size and phylogenetic affiliation withcorresponding data reported for non-plant eukaryotes.Patterns that can diverge during cell-cycle stages (e.g.some acetylation or phosphorylation), in mutants (inparticular methylation) or between (groups of) organisms(acetylation, methylation, phosphorylation) are discussedin terms of potential functionalmeaning or are highlightedas open questions that should be addressed in future work.

Methylated histones – stable marks for ‘open’ versus

repressive chromatin state

Although mono-, di- or trimethylation of specific lysines(K4, 9, 27, 36 of H3 and K20 of H4) has long been known

Corresponding author: Schubert, I. ([email protected]).Available online 20 March 2006

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(reviewed in [1]), the importance of the ‘trilogies’ ofmethylation sites for epigenetic regulation processes waselucidated only recently (reviewed in [2]), and demethylat-ing activity was discovered even more recently [3,4].Methylated H3K4 and H3K36 are considered to be marksfor ‘open’ chromatin structures (transcriptional potent)and methylated H3K9, H3K27 and H4K20 marks forrepressive chromatin structures. In spite of the ubiquitousoccurrence of most methylated histone isoforms, theirsubnuclear distribution can vary between yeasts, Neuro-spora,Drosophila, mammals and plants, as well as amongplant species.

Chromosomal distribution of ‘heterochromatin-specific’

histone methylation marks in different organisms

Whereas the euchromatin-specific methylation of H3K4and H3K36 is highly conserved among eukaryotes,heterochromatin indexing by methylation marks atH3K9, H3K27 and H4K20 is more variable (Table 1). InSaccharomyces pombe, H3K9me2 was found to beassociated with the limited amount of repressed chroma-tin, located at centromeres, telomeres and mating-typeloci [5,6], whereas H3K27 methylation was not detectable[2], as is also the case in other unicellular organisms.Although H4K20me1,2,3 is prominent within theS. pombe genome [2,7], no role in gene regulation orheterochromatin formation has been found. Instead, itmight be involved in the DNA damage response [7].

In Neurospora, besides H3K9me3, no other repressivemethylation marks have been reported; H3K9me3 isrequired for all types of DNA methylation [8].

H3K9me1,2, H3K27me1,2 and H4K20me3 are promi-nent marks in the pericentric heterochromatin of Droso-phila. In addition, H3K9me3 and H3K27me3 display afocal enrichment at the chromocentre core [9,10].

In mouse nuclei, H3K9me3, H3K27me1 andH4K20me3 preferentially mark constitutive heterochro-matin [10–12]; the facultative heterochromatin, rep-resented by the inactive X chromosome, is marked byH3K9me2, H3K27me3 and H4K20me1 [2,13–15].

Most data on global distribution of methylation marksin plants are available for Arabidopsis thaliana(160 Mbp/1C [16]). Immunostaining with antibodies thatdiscriminate between mono-, di- and trimethylation ofspecific lysines (K4, K9, K27and K36 of H3 and K20 of H4)identified H3K4me1,2,3 and H3K36me1,2,3, together

Review TRENDS in Plant Science Vol.11 No.4 April 2006

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Table 1. Heterochromatin-specificity of chromatin modifications in different organisms

Methylation

mark

Saccharomyces

pombea

Neurosporaa Drosophila Mouse Plants

Arabidopsis Vicia Hordeum

Histone

methylation

H3K4me1 K ? ? K K K K

H3K4me2 K K K K K K K

H3K4me3 K ? K K K K K

H3K9me1 ? ? C K C C C

H3K9me2 C K C (C)b/Cc C C C

H3K9me3 C C (C)d C K (K) K

H3K27me1 ND ? C C C C C

H3K27me2 ND ? C K C C K

H3K27me3 ND ? (C)d K/Cc K (C) K

H3K36me1 ? (K)e Kh ? K ? ?

H3K36me2 K (K)e Kh ? K ? ?

H3K36me3 K K Kh ? K ? ?

H4K20me1 (C)f ? (C)b K/Cc C C C

H4K20me2 (C)f ? (C)b K K ? ?

H4K20me3 (C)f ? C C K ? ?

DNA

methylation

K (C) (C)g C C (C) (C)

Refs [2,5,7,102] [8,103,104] [9,10,105–107]h [10,11,15,25] [17–20,30] [24]i [24]i

Abbreviations: C, increased levels; K, decreased levels; (C), partially increased or equal levels to euchromatin; ?, nuclear distribution not yet investigated; ND, not

detectable. Grey highlighted boxes indicate the presence of the corresponding modification as a hallmark of heterochromatin within the respective organisms.aData about nuclear distribution of the methylation marks in these species are mainly based on ChIP analysis of active genes versus inactive chromosomal regions.bSimilar levels as euchromatin.cProminent marks of facultative heterochromatin.dOnly chromocentre core labelled.ePresent in the genome, but a preferential enrichment in coding regions of actively transcribed genes is not shown.fA role in heterochromatin formation is not demonstrated.gMainly in DNA of embryos.hG. Reuter, personal communication.iJ. Fuchs et al., unpublished.


with H3K9me3, H3K27me3 and H4K20me2,3 as typicalmarks for euchromatin [17–20] (Figure 1a). By contrast,the heterochromatic chromocentres of Arabidopsis werefound to be enriched in H3K9me1,2, H3K27me1,2 andH4K20me1 [17,19–22] (Figure 1a). Clustering ofH3K9me2 is typical but not essential for heterochromatinformation in Arabidopsis [21].

These distribution patterns are not conserved amongplants. Andreas Houben et al. [21] studied 24 plant specieswith different genome sizes and found that immunostain-ing with antibodies against H3K4me2 exclusively labelledeuchromatic regions in all species tested (also in mostlytranscriptionally inactive B-chromosomes), whereasH3K9me2 displayed two different distribution patterns.In species with a genome size of ?500 Mbp/1C, thelabelling was confined to heterochromatic chromocentres,whereas, in species with larger genome size, signals weredispersed all over the nuclei.

In Hordeum vulgare (5100 Mbp/1C) [16], the euchro-matin-specific methylation marks H3K4me1,2,3,H3K9me3 and H3K27me3 strongly labelled the euchro-matic pole of interphase nuclei and the gene-rich terminiof metaphase chromosomes (Figure 1b). Surprisingly,H3K27me2, which labelled Arabidopsis heterochromatic

euchromatin-specific methylation marks show a gradual reduction of labelling from th

show strong signals at the chromosome termini and less-intense signals towards th

interphase nuclei and metaphase chromosomes uniformly. Reduced signal intensities

applied to V. faba nuclei revealed larger and smaller heterochromatin clusters (scale barZaccording to their intensity and reproducibility into marker and additional bands [23]; se

euchromatin-specific marks are excluded from the clusters of heterochromatin. Right: he

on the isoform studied, signal clusters appear at marker bands (H3K9me1), at minor band

(scale barZ5 mm). The distribution of H3K36 and H4K20me2,3 has not yet been investig

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chromocentres more intensely than euchromatin, hasbeen found exclusively in euchromatic nuclear domainsin barley and is strongest at the distal metaphasechromosome regions. The remaining heterochromaticmarks of Arabidopsis (H3K9me1,2, H3K27me1 andH4K20me1) were more-or-less uniformly distributedover the interphase chromatin and metaphase chromo-somes (Figure 1b), similar to H3K9me2. In Vicia faba (12740 Mb/1C [16]), the euchromatin-specific marksH3K4me1,2,3 occurred exclusively within the cytologi-cally defined euchromatin (Figure 1c). H3K9me1,2,H3K27me1,2,3 and H4K20me1 were uniformly distribu-ted over the entire chromatin, as is typical for ‘hetero-chromatin-specific’ marks in plants with a large genome.Beyond this, H3K9me1 and H3K27me2 were locallyenriched at different individual heterochromatic regions(mainly at weaker Giemsa bands [23]) and H3K27me3was locally enriched even in regions not defined asGiemsa-banded heterochromatin (Figure 1c).

Consistent with data from other organisms, all meth-ylation states of H3K4 are restricted to euchromatin inplants (for H3K36 this is so far only known forArabidopsis). By contrast, H3K9me1,2, H3K27me1 andH4K20me1 are conserved heterochromatin marks in

e telomeric towards the centromeric pole. Consistently, metaphase chromosomes

e centromeres. Right: antibodies of heterochromatic methylation marks decorate

are detectable in euchromatic regions only occasionally. (c) Left: Giemsa-banding

5 mm), which on metaphase chromosomes are resolved as distinct bands, classified

e also the scheme of chromosome III of karyotype ACB in the lower panel. Middle:

terochromatin-specific marks show a disperse distribution. Lower panel: depending

s (H3K27me2) or at positions not characterized by Giemsa-banded heterochromatin

ated in plants other than Arabidopsis


(a)

(b)

(c)

Arabidopsis thalianaMethylation marks for:

Chromatin organizationEuchromatin Heterochromatin

H3K4me1 H3K9me1Euchromatin

Heterochromatin

H3K4me1,2,3H3K9me3H3K27me3

H3K36me1,2,3H4K20me2H4K20me3

H3K9me1H3K9me2H3K27me1

H3K27me2H4K20me1

Hordeum vulgare

Heterochromaticcentromeric pole

BAC7

HvT01

Euchromatictelomeric pole

H3K4me1,2,3H3K9me3

H3K27me2H3K27me3

H3K9me1H3K9me2

H3K27me1H4K20me1

H3K4me3 H3K9me1

Vicia faba

Heterochromatin

H3K4me2 H3K27me2

Euchromatin

H3K4me1,2,3 H3K9me1H3K9me2H3K27me1

H3K27me2(H3K27me3)H4K20me1

Marker bands

Additional bands

Giemsabands

H3K4me2

H3K9me1 me2

H3K27me1 me2 me3

H4K20me1

Figure 1. Conservation and variability of histone methylation marks in Arabidopsis thaliana, Hordeum vulgare and Vicia faba. (a) Heterochromatin in Arabidopsis is organized

as condensed chromocentres. Left: intensely DAPI stained chromocentres (scale barZ5 mm). Middle: immunostaining with antibodies against euchromatin-specific

methylation marks shows intense labelling of the euchromatin, whereas the nucleolus and the chromocentres remain unlabelled. Right: by contrast, antibodies against

heterochromatin-specific methylation marks yield signals preferentially at the chromocentres. (b) Chromatin organization in H. vulgare resembles the so-called Rabl-

orientation, with the gene-rich chromosome termini clustered in one hemisphere of the nucleus, and pericentromeric heterochromatin, including the centromeres, in the

opposite hemisphere. Left: FISH with probes to highlight the centromeres (BAC7 – cyan) and the telomeres (HvT01 – green) (modified from [91]) (scale barZ5 mm). Middle:

Review TRENDS in Plant Science Vol.11 No.4 April 2006 201




plants, although their nuclear distribution can differdepending on the genome size and organization. Appar-ently, increasing quantities of mobile elements interspersethe euchromatin of larger genomes and have to be silencedby ‘heterochromatinization’ [24] involving these marks.H3K27me2,3 show a species-specific chromosomal distri-bution; H3K27me2 is typical for heterochromatin inArabidopsis and characteristic of euchromatin in barley,whereas H3K27me3 is euchromatin-specific in Arabidop-sis and barley but clusters at certain heterochromaticpositions in V. faba. To date, there are no data on thechromosomal distribution of methylated H3K14, H3K18and H3K23 or the methylated terminal arginines of H3and H4 in plants.

In general, H3K9 methylation is a hallmark ofconstitutive heterochromatin conserved from fissionyeast to mammals and plants. In Neurospora andmammals, H3K9me3 is enriched at silent loci, whereas,in Drosophila and plants, H3K9me1,2 is enriched atheterochromatin. H3K27 methylation has only beenreported in metazoa and plants. In mammals,H3K27me1 occurs at centromeric heterochromatin. InDrosophila and Arabidopsis, heterochromatin also con-tains H3K27me2. The ubiquitous H4K20 methylation iscorrelated with heterochromatin in Drosophila, mammalsand plants. H4K20me3 is heterochromatin specific in fliesand mammals and H4K20me1 is heterochromatin specificin Arabidopsis. Contrary to the situation in metazoa, theconstitutive heterochromatin in Arabidopsis is character-ized by mono- and dimethylation marks only. This issurprising because N-terminal trimethylated lysines areconsidered to be more robust than mono- and dimethy-lated ones [11].

H3K9-dimethylation: a consequence of CG methylation

and a prerequisite for CNG methylation in plants

It has been assumed that the combination of DNAmethylation and histone modifications determines chro-matin structure and transcriptional competence, eventhough the causal relation between histone and DNAmethylation has been hotly debated.

In mammals, DNA methylation is mainly restricted tosymmetrical CG sequences [25], whereas, in plants,methylation occurs at CG, CNG (NZany nucleotide) andCHH (HZA, C or T) sequences [26]. The Arabidopsisgenome contains three classes of DNA methyltransfer-ases.METHYLTRANSFERASE 1 (MET1) is considered tobe the maintenance DNA methyltransferase. Null allelemutants of MET1 resulted in a complete loss of CGmethylation [27]. Plant-specific CNG methylation iscatalysed by CHROMOMETHYLASE 3 (CMT3) [28,29].CMT3 also controls the asymmetric CHHmethylation in alocus-specific manner, probably redundant withDOMAINS REARRANGED METHYLTRANSFERASES(DRM) 1 and DRM2 [30]. DRM1 and DRM2 areresponsible for maintaining CHH methylation and for denovo methylation (reviewed in [31]).

Immunostaining with antibodies against H3K9me2labelled the heterochromatic chromocentres of the DNAhypomethylation (partial loss-of-function) mutant met1less strongly than those of wild type, even in nuclei of F1 of


a backcross [17]. Comparable data were found for amutant of the chromatin remodelling factor DDM1(DECREASE IN DNA METYLATION 1 [32]). However,the distribution of H3K27me1,2 is not influenced by DNAmethylation at CG sites [33]. Together with the loss ofH3K9me2 in an Arabidopsis null mutant of MET1 [22],these observations suggest that DNA methylation at CGsequences directs H3K9-dimethylation at the chromocen-tres. The alteration in DNA methylation is accompaniedby a relaxation of the heterochromatic chromocentres [17](J. Paszkowski, personal communication).

In contrast with the methylation at CG sites, methyl-ation outside CG has no effect on histone methylation [34],but histone methylation in turn directs DNA methylationat CNG sites [35]. Mutants of the H3K9me2-specifichistone methyltransferase KRYPTONITE (KYPZSUVH4) and of the DNA methyltransferase CMT3 resultin a loss of cytosine methylation at CNG sites [35].

Given that the CMT3 chromodomain binds to H3peptides only when K9 and K27 are methylated, AndersLindroth et al. [19] proposed that methylated H3K9 andH3K27 are both required to recruit CMT3 to target loci.Studying the functional interaction of the histone methyl-transferase SUVH2, which is involved in the methylationof all heterochromatin-specific marks (in particular ofH4K20me1), revealed a dependence on MET1 and DDM1but not on CMT3 [20].

The heterochromatin protein 1 (HP1) and its homol-ogues are key components of heterochromatin in fissionyeast, Neurospora, Drosophila and mammals [36–39],probably to bind H3K9me1,2 and to recruit DNAmethyltransferases to these sites [40]. Surprisingly, theonly homologue of HP1 in the Arabidopsis genome doesnot contribute to heterochromatin formation. It localizespreferentially to euchromatic regions for development-specific gene suppression, but not to heterochromaticchromocentres [19,41,42].

Histone phosphorylation is conserved, dynamic

and serves variable functions

Phosphorylation of histone H3 seems to be crucial foractivating transcription, apoptosis and DNA repair as wellas for cell cycle-dependent chromosome condensation andsegregation [43,44]. H3 phosphorylation probably also hasa role in the transcriptional activation of genes inplants [45].

The primary function of histone H3 phosphorylation isstill controversial. Itmightbe to label different chromosomaldomains and to mark their progress through the cell cycle[44]. Older models proposed that histone modificationsmight directly influence either the structure or the foldingdynamics of nucleosomal arrays, but evidence for suchmodels is lacking [46]. More likely, histone modificationscontrol the binding of non-histone proteins to the chromatinfibre. Although some chromodomains bind to methylatedlysines, and bromodomains bind to acetylated lysines, noproteins that specifically interact with phosphorylatedhistones have been describeduntil now.Nophosphorylationis known for H3 threonines 3, 6, 22, 32 in plants.

The histone variant H2AX in yeast and metazoabecomes phosphorylated at its C-terminal serine139 on



either site of a DNA double-strand break at a distance of 1to 50 kb by specific kinases (ATM, ATR). PhosphorylatedH2AX reversibly triggers the loss of nucleosomes [47] andaccumulation of components involved in DNA recombina-tion repair and cell-cycle-checkpoint activation, includinghistone acetyltransferase and cohesin (reviewed in [48]).In plants, phosphorylation of H2AX is induced byY-irradiation at only a third of the rate observed in yeastand mammals [49].

Phosphorylated H3 histones are linked with nuclear

division

In several eukaryotes, the level of H3 phosphorylation islow in interphase and increases during nuclear divisions[50]. In mammals, the cell cycle-dependent phosphoryl-ation of H3S10 and H3S28 originates in the pericentro-mere [51] and spreads throughout the chromosomesduring the G2–M phase transition, and is probablyinterlinked with the initiation of chromosome conden-sation [52]. Although the chromosomal distribution of

Metaphase

(a) (b)

(e)

Mit

osi

sM

eio

sis

(f) (g)

H3S28phH3T11ph

H3S28phH3S10ph

Thr

11ph

Interphase

H3Chromosome condensation

H3S28phH3T11ph

HH

T. aestivumMet

apha

se I

S. cereale

V. faba H. vulgare

Figure 2. Cell-cycle-regulated histone H3 phosphorylation in plants. (a–e) Mitosis. (a) H3

10 mm). (b) On monocentric chromosomes, the pericentromeric regions show H3S10

pericentromeric region (inset). DAPI-stained interphase nuclei (blue) display no detecta

entirely labelled with H3 phosphorylated at both serine positions (scale barZ5 mm). (d) A

cohere and where H3 is phosphorylated at S10 and S28 (scale barZ5 mm). (e) Model: in

other proteins involved in chromosome condensation, whereas H3S10ph and H3S28ph i

chromosomes during mitosis and meiosis II. (f–h) Meiosis. (f) H3S28ph and H3T11ph du

metaphase II (the pericentromeric regions show H3S28ph, whereas H3T11ph decorates t

from equational division of univalents at anaphase I, show no pericentromeric H3S10ph


H3S10ph in mammals and Drosophila is comparable, alack of correlation between H3S10ph and chromosomecondensation has been reported for borr and greatwall flymutants [53,54]. If phosphorylation of H3S10 is inhibited,HP1 is not released from mammalian mitotic chromo-somes [55,56]. In yeast, H3S10ph is not required for cell-cycle progression, instead phosphorylated histone H2Bmight take over this function [57]. Phosphorylation ofthreonine 11 of H3 in mammals is restricted to centro-meres during mitosis and meiosis [58].

In plants, the distribution of H3S10ph [59,60] andH3S28ph [61,62] is restricted to pericentromeric regionsduring mitosis and meiosis II (Figure 2a,b,g,h), whereas,during the first meiotic division (Figure 2f), both residuesare phosphorylated along the entire length of thechromosomes [61,63]. Single chromatids, resulting fromequational division of univalents at anaphase I, show noH3 phosphorylation during meiosis II. In spite of this,such prematurely separated chromatids are normallycondensed and their kinetochores interact with spindle

Metaphase

(c) (d) AtAurora

(h)

L. luzuloides V. faba

H3S28phH3S10ph

Phosphorylationby AtAurora

Ser

28ph

Ser

10ph

Interphase

Sister chromatid cohesion

3S28ph3T11ph

TubulinH3S10ph

Ana

phas

e II

Met

apha

se II

T. aestivum

T11ph correlates with condensation of plant metaphase chromosomes (scale barZph (scale barZ10 mm), whereas H3S28ph is confined to the central part of the

ble H3 phosphorylation. (c) The polycentric chromosomes of Luzula luzuloides are

nti-AtAurora antibodies label the pericentromeric regions where sister chromatids

plants, the cell-cycle-dependent phosphorylation at H3T11 can serve as a signal for

s apparently needed for sister chromatid cohesion at pericentromeres of metaphase

ring metaphase I (entire chromosomes labelled) (scale barZ10 mm) and (g) during

he entire chromosome) (scale barZ10 mm). (h) Single chromatids (arrow), resulting

during the second meiotic division (scale barZ10 mm).



microtubules (Figure 2h). Furthermore, in a maizemutant (afdI) defective in sister chromatid cohesion,univalents only showed strong phosphorylation duringmetaphase I at the pericentromeric regions [60] and a‘semi-dicentric’ barley chromosome revealed thatH3S10ph was only present at the functional centromere[59], whereas the polycentric chromosomes of Luzulaluzuloides (Figure 2c) were labelled along the entirelength of the chromosomes during mitosis [61,64]. Theseobservations led to the hypothesis that, in plants,pericentromeric H3 phosphorylation at both serine pos-itions is required for cohesion of sister chromatids duringmetaphase I, and for cohesion of sister pericentromeresduring mitosis and metaphase II [61,63]. The Arabidopsiskinases AtAurora1 [65] and AtAurora3 [66] phosphorylateH3Ser10. H3S10 and H3S28 become dephosphorylated atinterkinesis and re-phosphorylated during prophase II;phosphorylation is extended after cold treatment (toadditional chromosome regions) and exposure to thephosphatase inhibitor cantharidin (to entire chromo-somes) [67], which indicates that H3S10 and H3S28phosphorylation is reversible and independent ofDNA replication.

Contrary to the situation in mammals, H3T11ph(Figure 2a,f,g) occurs along entire chromosome arms inplants and correlates with chromosome condensationduring mitosis and meiosis [68]. Although cell-cycle-dependent phosphorylation of H3S10, H3S28 and H3T11is conserved between plants and animals, the functionalsignificance of the two modified amino acids apparentlyhas been reversed during evolution (Figure 2e). In plants,H3T11ph along the chromosomal arms is linked tochromosome condensation. Phosphorylation of H3S10and H3S28, restricted to pericentromeric regions duringmitotic and second meiotic division, is connected withcentromere cohesion. The opposite situation is seen inmammals. Here, H3S10ph and H3S28ph along thechromosomal arms is linked to chromosome condensation,and H3T11ph at centromeres might serve in sistercentromere cohesion.

Histone acetylation at specific lysine positions correlates

with replication of euchromatic and heterochromatic

domains

The N-terminal lysines 5, 8, 12, 16, 20 of H4 and 9, 14, 18,23 of H3 are acetylatable by histone acetyltransferases(HAT) and deacetylatable by deacetylases (HDAC) inplants [69,70]. Decondensation of the nucleosome struc-ture mediated by histone acetylation renders chromatinmore accessible to nuclear protein complexes and, thus,contributes to the ‘epigenetic’ or ‘histone code’ [71–73]. Acorrelation with potential transcriptional activity wasproposed more than 40 years ago [74]. Locus-specificassociation of histone acetylation with transcriptionalactivation of promoters, and of deacetylation withsilencing of repetitive transgenes and rDNA has beenconfirmed for plants [75–77]. Histone acetylation alsofacilitates DNA repair and recombination [78–81].

Mammalian mitotic chromosomes revealed intenseacetylation of H3 and H4 lysines at early replicatingeuchromatin (R bands) and less intense acetylation at


constitutive and facultative heterochromatin [82–84].Drosophila polytene chromosomes show H4K5ac andH4K8ac preferentially at euchromatin and H4K12ac atheterochromatin, whereas H4K16ac is enriched onlyalong the X chromosome of males [85]. Plant chromo-somes, depending on the acetylated isoform tested,displayed a more-or-less uniform distribution (H3K23ac[86]) or, more often, a reduced abundance of acetylatedhistone(s) at heterochromatin and a clustering at nucleo-lar organizing regions (NORs) (Figure 3b,e) [21,87–91].Contrary to the situation in mammals, the patterns ofacetylated H3 and H4 isoforms often do not coincide inplants. For example, H3K9ac, H3K14ac and H3K18ac areunderrepresented in some and overrepresented in otherheterochromatic regions (in addition to the NOR) of thefield bean (Figure 3d) [86]. H4K5 and H4K12 show adeposition-related increase of acetylation during S-phasein Drosophila and HeLa cells [92]. The switch from abelow-average to an above-average acetylating intensityof H4K5, H4K12 and H4K16 (but not of H3 isoforms)observed after treatment with the HDAC inhibitortrichostatin A within the heterochromatin of field beanchromosomes (Figure 3b,c) [87] is another indication for acell-cycle-dependent modulation of H4 acetylation. Theacetylation intensity at euchromatin and heterochromatinincreases during replication for H4K5, H4K12 and H4K16in field bean [90], for H4K5, H4K8 and H4K12 in barley[91], for H4K5 in onion [93] and for H3K18 and H4K16 inArabidopsis [21] (Figure 3a). In several plants, NORsshow most intense histone acetylation around mitosis andlowest acetylation during S-phase, independent of theirability to form a nucleolus (Figure 3i) [91]. Towardsmitosis, heterochromatin becomes deacetylated mostly toa level below that of euchromatin. Only occasionally doesdeacetylation last up to early G1-phase (H4K5ac andH4K12ac in barley [91]). Deacetylation of H4K16ac atheterochromatic chromocentres is slowed down in hypo-methylation mutants (in particular, in ddm1) ofArabidopsis [17].

In field bean and barley nuclei, no correlation wasobserved between the distribution of immunosignals foracetylated H4 isoforms and transcriptional activity(Figure 3g,h) [90,91]. Thus, at the chromosomal level,histone acetylation at some lysine residues might berelated to replication rather than to transcription. Thereplication-associated stronger acetylation, which alsooccurs at mammalian heterochromatin [94], might berequired for post-replicational repair and possibly forDNA maintenance methylation.

Concluding remarks

The comparison of subnuclear and chromosomal distri-bution of methylated, phosphorylated and acetylatedhistones H3 and/or H4 within and between differenteukaryotic groups revealed divergent patterns for severaltypes of modifications. Although the components of theepigenetic code are largely conserved, their functionsmight have evolved divergently in different organisms.This is indicated by, for example, phosphorylated H3S10and H3S28 versus H3T11ph, which are involved in sistercentromere cohesion and chromosome condensation,


M G1 S M

Heterochromatin

Euchromatin

NOR or nucleolus

Heterochromatin

Euchromatin

NOR or nucleolus

Heterochromatin

Euchromatin

Nucleolus

(a)

(b)

(c)

(d)

(e) (f) (g) (h) (i)

V. faba H4K5,H4K12H4K16

H. vulgare H4K8H4K5, H4K12

H3K18 and H4K16

H3K18

A. thaliana

G2

H4K5ac

H4K5ac+TSA

H3K14ac

NOR7(inactive)

NOR6(active)

Acetylation marks

Figure 3. Cell-cycle dependence and subnuclear distribution patterns of histone acetylation in plants. (a) Cell-cycle dynamics and intensity of acetylation at various H3 and H4

lysine residues within distinct chromatin domains of Vicia faba, Hordeum vulgare and Arabidopsis thaliana. (The acetylation intensity patterns show no clear cell-cycle

dependency for H3K9 and/or K18, H3K14, H3K23 and H4K8 of V. faba, for H3K9 and/or K18, H3K14 and H4K16 of H. vulgare and for H3K9, H3K14, H4K5, H4K8 and H4K12 of

Arabidopsis, not shown.) (b) Distribution of H4K5ac along V. faba metaphase chromosomes; scheme of karyotype ACB with heterochromatin marked is shown above (scale

barZ10 mm). (c) Distribution of H4K5ac along V. faba metaphase chromosomes after treatment of root tips with the HDAC inhibitor trichostatin A for 2 h before fixation (scale

barZ10 mm). Note the reverse signal pattern at heterochromatin compared with that shown in (b). (b,c) modified from [87]. (d) Distribution of H3K14ac along V. faba

chromosomes reveals clustering at the NOR and some heterochromatic regions, whereas other heterochromatin positions are less labelled than the euchromatin positions

(scale barZ10 mm) (modified from [86]). (e) V. faba G1-nucleus showing enrichment of H4K5ac (green) within the nucleolus, whereas euchromatin shows moderate signals

and heterochromatin (represented by tandem-repetitive FokI-elements, red) no signals (scale barZ10 mm). (f) V. faba nucleus in late S to early G2 showing clustering of

H4K5ac (green) at late replicating heterochromatin (represented by tandem-repetitive FokI-elements, red) (scale barZ10 mm). (g) V. faba nucleus in early S phase after ‘run on

transcription’ showing BrUTP signals (red) mainly within the nucleolus and less dense signals across the euchromatin; the nucleolus and heterochromatin domains are free

of H4K5ac (green) (scale barZ10 mm). (h) V. faba nucleus in early G2 phase with BrUTP signals (red) over the nucleolus and the euchromatin, whereas H4K5ac is clustered at

heterochromatic domains that do not coincide with BrUTP signals (scale barZ10 mm). Note the rare overlap of red and green signals within the euchromatin in (g) and (h).

(a and e–h) reproduced from [90]. (i) A barley translocation chromosome with both NORs on one chromosome; both are enriched with H4K5ac (right), but only NOR6 forms a

nucleolus (modified from [91]) (scale barZ5 mm).


respectively, during plant nuclear divisions and haveapparently inverse functions in mammals. Species-specific cell-cycle modulation of acetylation at differentH3 and/or H4 lysine residues and variable distributionbetween euchromatin and heterochromatin of H3 and H4lysine methylation ‘trilogies’ in mammals and plants stillawait an interpretation. Some modifications, for instance,acetylation, apparently correlate at the level of genes withother processes (transcription) rather than at the


chromosomal or subnuclear level (replication and/orpost-replication repair, maintenance methylation, chro-matin modelling). Contrary to histone acetylation andphosphorylation, which display cell-cycle-dependentchromosomal distribution patterns, histone methylationseems to be a rather robust mark. More and more cross-talks between modifications during and after the estab-lishment of individual marks have emerged recently. Forexample: the ubiquitination of histone H2B regulates H3



methylation and gene silencing in budding yeast [95];ubiquitin ligase is required for histone methyltransferaselocalization in fission yeast [96]; acetylation of H3K18stimulates the association of arginine methyltransferaseCARM1 and the methylation of H3R17 in humans [97];and H3S10ph and H3K14ac together mediate transcrip-tional activation of mammalian genes in ovary differen-tiation [98]. Much about these cross-talks and theirimmediate functional importance remains to be deter-mined, particularly because some findings seem to becontradictory (e.g. the requirement of a HDAC homologueto recruit the SUV39h homologue for H3K9methylation inyeast [99] versus the increase in H3K9ac, H3K4me2 andH3K9me2 after HDAC inhibition in humans [100]; orH3K9me3 association with transcription elongation inmammals [101], although this modification is usually amark for repressed mammalian chromatin). Another openquestion is whether the accumulation of individualacetylation or methylation marks (e.g. H3K9ac,H3K14ac, H3K18ac, H3K9me1 and H3K27me2,3) atdistinct chromosomal regions of specific genomes such asthat of V. faba is correlated with particular DNAsequences, and what is the functional meaning if any.The chromosomal distribution of chromatin modificationsin wild type and relevant mutant organisms might forinstance, in combination with immunoprecipitation andmass spectroscopy data, provide further insights intoepigenetic regulation and the interplay of life processes.

Acknowledgements

This work was supported by grants of the Land Sachsen-Anhalt and of theDFG to J.F., A.H. and I.S. We thank Rigomar Rieger for critically readingthe manuscript. We apologize to all our colleagues that contributed to thefield but could not be cited because of space limitation.

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103 Tamaru, H. and Selker, E.U. (2001) A histone H3 methyltransferasecontrols DNA methylation in Neurospora crassa. Nature 414,277–283

104 Adhvaryu, K.K. et al. (2005) Methylation of histone H3 lysine 36 isrequired for normal development in Neurospora crassa. Eukaryot.Cell 4, 1455–1464

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