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Plant Biology
Interphase chromosomes in Arabidopsis are organized as well defined chromocenters from which euchromatin loops emanate

Paul Fransz ^* , J. Hans de Jong , Martin Lysak ^*, Monica Ruffini Castiglione , and Ingo Schubert ^*

^*Institute of Plant Genetics and Crop Plant Research (IPK), D-06466 Gatersleben, Germany; Laboratory of Genetics, Wageningen University, Arboretumlaan 4, 6703 BD, Wageningen, The Netherlands; and Department of Plant Sciences, Istituto di Mutagenesi e Differenziamento, Consiglio Nazionale delle Ricerche, 56100 Pisa, Italy

Edited by Mark T. Groudine, Fred Hutchinson Cancer Research Center, Seattle, WA, and approved August 26, 2002 (received for review May 31, 2002)

	Abstract

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Heterochromatin in the model plant Arabidopsis thaliana is confined to small pericentromeric regions of all five chromosomes and to the nucleolus organizing regions. This clear differentiation makes it possible to study spatial arrangement and functional properties of individual chromatin domains in interphase nuclei. Here, we present the organization of Arabidopsis chromosomes in young parenchyma cells. Heterochromatin segments are organized as condensed chromocenters (CCs), which contain heavily methylated, mostly repetitive DNA sequences. In contrast, euchromatin contains less methylated DNA and emanates from CCs as loops spanning 0.2–2 Mbp. These loops are rich in acetylated histones, whereas CCs contain less acetylated histones. We identified individual CCs and loops by fluorescence in situ hybridization by using rDNA clones and 131 bacterial artificial chromosome DNA clones from chromosome 4. CC and loops together form a chromosome territory. Homologous CCs and territories were associated frequently. Moreover, a considerable number of nuclei displayed perfect alignment of homologous subregions, suggesting physical transinteractions between the homologs. The arrangement of interphase chromosomes in Arabidopsis provides a well defined system to investigate chromatin organization and its role in epigenetic processes.

Abbreviations: NOR, nucleolus organizing region; FISH, fluorescence in situ hybridization; BAC, bacterial artificial chromosome; CC, chromocenter

A positional relationship between heterochromatinization and gene silencing was shown earlier in flies (11, 12) and mammals (13, 14). Silencing of certain genes seems to be correlated with sequestration of the gene to a heterochromatic compartment involving specific proteins (13), whereas activated enhancers suppress silencing of genes by preventing their localization at heterochromatin (14). To understand how chromosomes function within interphase nuclei, it is essential to investigate individual chromatin domains in a well defined system. Microscopic studies of human nuclei have revealed chromosome-specific domains or territories, in which transcription appears to take place predominantly at or near the surface of compact chromatin domains (15). However, because of the complex nature of human chromosomes, it remains difficult to establish a clear relationship between DNA sequence, the higher-order structure of chromosomes, and gene regulation. Arabidopsis thaliana (n = 5) may provide an appropriate system to study large-scale organization of chromatin domains. Its chromosomes display small, conspicuous heterochromatin segments that mark the position of each centromere and of the NORs of chromosomes 2 and 4 (Fig. 1A; see ref. 16). They contain most of the repetitive DNA sequences, comprising 15% of the entire genome (17). The centromere core consists predominantly of a 180-bp tandem repeat and several transposon-like sequences (18, 19). The flanking heterochromatin regions are enriched in dispersed, repetitive transposon sequences and differ structurally and functionally from the centromere core (20).

View larger version (31K): [in this window] [in a new window]   Fig 1. Heterochromatin distribution in A. thaliana. (A) Ideogram showing the five chromosomes with 5S and 45S loci. (B) Three optical sections of a paraformaldehyde-fixed interphase nucleus stained with 4',6-diamidino-2-phenylindole showing CCs near the periphery and the nucleolus. (Bar = 2 µm.) (C) Distribution of the number of CCs per nucleus.

	Materials and Methods

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Plant Material. Young rosette leaves and immature flower buds were harvested from A. thaliana accessions Wassileskija, C24, Zurich, and Landsberg and fixed in ethanol/acetic acid (3:1).

Probe Labeling. The following DNA clones were used: 25S rDNA (22), 5S rDNA (23), pAL1 (18), CIC yeast artificial chromosome clones (24), IGF and TAMU bacterial artificial chromosomes (BACs) (25, 26), and pAtT4 (27). BACs from the long-arm 4L were pooled into eight groups as described in ref. 28. All DNA clones were labeled individually with either biotin-dUTP or digoxigenin-dUTP by using a nick translation kit (Boehringer Mannheim).

FISH Analysis. FISH experiments were carried out as described (16, 28). FISH preparations were examined on a Zeiss Axioplan by using 4',6-diamidino-2-phenylindole, FITC, and Texas red fluorescence filter blocks. Images were recorded with a conventional camera or charge-coupled device camera (Photometrics) by using IP-LABS software and digitally processed with Adobe PHOTOSHOP software. The positions of hybridization signals and CCs were analyzed in relation to each other. Partly or completely overlapping fluorescent foci were interpreted as colocalizing or associating, whereas other situations were considered as separate positions of the regions.

Immunolabeling of Methylated DNA. Slide preparations were baked at 60°C for 30 min, denatured in 70% formamide, 2x SSC, and 50 mM sodium phosphate, pH 7.0, washed in ice-cold PBS 2 x 5 min, incubated in 1% BSA in PBS (10 mM sodium phosphate, pH 7.0/143 mM NaCl) for 30 min at 37°C, and subsequently incubated with mouse antiserum (1:50) raised against 5-methylcytosine (29) in the same buffer for 30 min at 37°C. Mouse antibodies were detected as described for FISH detection.

Immunolabeling of Histone Isoforms H4Ac5 and H4Ac8. Nuclei were isolated from 500 mg of leaves by chopping the tissue with a razor blade in 1 ml of ice-cold 10 mM Tris•HCl, pH 9.5/10 mM EDTA/100 mM KCl/0.5 M sucrose/4 mM spermidine/1.0 mM spermine/0.1% (vol/vol) 2-mercaptoethanol (NIB). The homogenate was filtered through 20-µm mesh nylon and fixed by adding an equal amount of 4% paraformaldehyde in PBS. After 30 min, the suspension was centrifuged in an Eppendorf centrifuge at 2,500 rpm for 4 min at 4°C, and the pellet was resuspended in 50 µl of NIB. Three microliters of suspension was pipetted to a clean slide, dried at 4°C, and postfixed in 4% paraformaldehyde in PBS for 30 min at room temperature. Slides were incubated in 1% BSA in PBS at 37°C for 30 min followed by incubation with rabbit antisera R41 and R232 (30) raised against histone H4, which was acetylated at lysines 5 and 8, respectively, in the same buffer (31). Rabbit antibodies were detected with antiserum conjugated with fluorescein as described for FISH detection.

	Results

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CCs Contain Major Tandem Repeats. Interphase nuclei from immature parenchyma cells contain up to 10 conspicuous CCs, located near the nuclear periphery and the nucleolus (Fig. 1 B and C). FISH with the probes pAL1 and F17A20, containing centromeric and pericentromeric repeats (16, 32), yielded signals exclusively at all CCs (Fig. 2A), indicating that CCs represent the nuclear domains of (peri-)centromeric heterochromatin. FISH with 45S rDNA, which maps to NOR2 and NOR4, and with 5S rDNA, which maps to CEN4 and CEN5 (see Fig. 1A), revealed nearly all 5S (99%, n = 427) and 45S (97%, n = 353) signals at CCs. The occurrence of two green (45S), two red-green (5S + 45S), and two red signals (5S) in many nuclei (Fig. 2B) suggests compartmentalization of the terminal 45S rDNA segments of chromosome arms 2S and 4S together with the centromeres of the corresponding chromosomes. The compartmentalization of NOR4 and CEN4 also was confirmed by FISH with unique DNA clones that flank NOR4 (see below and Fig. 3D). Unlike (peri-)centromeric and ribosomal repeats, most telomeric sequences hybridized outside CCs, in the vicinity of nucleoli (Fig. 2C). Only two to four telomere signals colocalized with CCs and most likely represent the ends of chromosome arms 2S and 4S, which contain the NORs. Hence, Arabidopsis chromosomes do not expose a "Rabl" orientation, with telomeres and centromeres at opposite nuclear poles as observed in many plant species (33, 34).

View larger version (29K): [in this window] [in a new window]   Fig 2. Identification and characterization of CCs by FISH and immunolabeling to nuclei of the accession Wassileskija. All preparations were counterstained with 4',6-diamidino-2-phenylindole (blue). (A) FISH with centromeric pAL1 (red) and pericentromeric F17A20 repeats (green). (B) FISH with 5S (red) and 45S rDNA (green). Numbers correspond to chromosomes. (C) FISH with the telomeric sequence (red) yielded clustered signals around the nucleolus (n). (D) Immunolabeling with antibodies against 5-methylcytosine (green). (E) Immunolabeling with antibodies against histone H4Ac5 (green) and FISH with the centromeric pAL1 (red). [Bar = 2 µm (E) and 5 µm (A–D).]

View larger version (85K): [in this window] [in a new window]   Fig 3. FISH localization of chromosome 4 regions in nuclei of the accessions Landsberg (A and B), Wassileskija (C and J), Zurich (D), and C24 (E– I, K, and L). Diagrams on the left indicate the map position of the DNA clones in chromosome 4. Solid circle and rectangle represent NOR4 and pericentromere 4, respectively. (A) BAC clone T4B21 (green) is outside CC4, whereas 5S rDNA (red) colocalizes with CC4 and CC5. (B) Two contiguous BAC clones T4B21 (green) and T1J1 (red). Note the position of the distal T1J1 relative to T4B21 and CC4. B2 shows a FISH signal of aligned, homologous regions. Note the inverse order of centromere-T1J1-T4B21 signals. (C) Two contiguous yeast artificial chromosome clones, 8B1 (green) and 7C3 (red), localize close to CC4. 8B1 (980 kb) covers the heterochromatic knob hk4S, whereas the adjacent 7C3 (480 kb) is located in the proximal euchromatin. The difference in chromatin density between the two regions is illustrated by the length of the signals. (D) Two contiguous BACs, F5J10 (green) and F6N15 (red), from the distal end of chromosome arm 4S, showing separate (Left) and associated (Right) homologous regions. Note the loop structure in one of the homologs. (E) Two adjacent BACs, T19B17 (green) and the proximal T27D20 (red), form a small loop structure (see magnification). Note the difference in array position between the signals of the two homologs. (F) Pools of five BACs from the short (red) and long (green) arm adjacent to the pericentromere. The interrupted and uninterrupted white lines represent the hybridization patterns of the homologous regions. (G and H) Pachytene chromosome and interphase nuclei hybridized with a mix of 18 BACs covering 2 Mbp of chromosome arm 4S. During interphase, chromosome arm 4S forms either a cloud of small loops (G2) or a single giant loop (H). The arrows indicate corresponding nonlabeled regions in the nucleus and the pachytene chromosome. (I) Pachytene chromosome and interphase nucleus hybridized with a mix of 17 BACs that differs from G in labeling pattern. Note that the homologous arms, 4S, in H and I are perfectly aligned. (J) Pachytene chromosome and interphase nucleus hybridized with a mix of 113 BACs from the long-arm 4L. (K) Twelve long-arm BACs are labeled in green and map to the distal end. In interphase nuclei, this region may associate with CC4, which supports the conclusion that loop formation also occurs in the long arm. The short arm is visualized by 13 BACs in red and 1 distal BAC in green. (L) The middle region of the long arm (10 red BACs) may also associate with CC4, which is identified by 5S (green) and 45S rDNA (red) probes. CC2 and CC5 are identified by 45S and 5S rDNA, respectively. In this case, one CC2 colocalizes with its homolog or with CC4. (Bar = 5 µm.)

Euchromatic Loops Emanate from the CC. Compartmentalization of the distal NORs 2 and 4 with the corresponding centromeres raised the question of whether the interstitial euchromatin domains also are closely associated with the centromere. We therefore hybridized BACs from the short arm of chromosome 4 and established their position relative to CC4. With BAC T4B21, which maps to the proximal euchromatin (20), the majority of the signals (84%, n = 58) were outside the CCs (Fig. 3A), whereas only 16% colocalized with CC4. BACs from other euchromatin regions, including those flanking the NOR and the pericentromere, yielded comparable results (Fig. 3 B–F), although the frequency of colocalization with CC4 varied between the regions (unpublished data). We concluded that the short arm of chromosome 4 forms at least one euchromatic loop. To investigate whether more than one loop indeed may emanate from the CC, we studied the nuclear positions of the BACs T4B21 and T1J1, the latter mapped distally from T4B21 in the accession Landsberg (19). If the short arm consists of a single loop, we expect a positional array of CC-T4B21-T1J1. This was observed for 38% (n = 50) of the signals (Fig. 3B). However, 30% showed the reversed order, indicating the presence of more than one euchromatic loop between NOR4 and CEN4. In the remaining 32%, the order of signals could not be determined, because of equal distances of both signals to CC4. Similar results were obtained with other DNA probes (Fig. 3C). Occasionally, DNA loops spanning up to 185 kb, with a condensation degree of approximately 55 kb/µm, could be observed (Fig. 3 D and E). Thus, we conclude that the short arm 4S is organized in one or more loops around CC4.

CC and Euchromatic Loops Form a Chromosome Territory. To determine the nuclear position of the entire chromosome arm 4S in relation to CC4, we simultaneously hybridized 18 BACs covering 2 Mbp. In most cases (83%, n = 64), this hybridization yielded a dispersed pattern of signals around CC4, suggesting an arrangement of euchromatin into several small loops (Fig. 3G). However, in the remaining 17%, we observed a single loop spanning the major part of this arm (Fig. 3H). The looped arrangement was easily deduced from the pattern of red-green signals, which corresponded with the FISH pattern on pachytene chromosomes. Similar loops were detected with another BAC mix from the same arm (Fig. 3I). This supports the conclusion that chromosome arm 4S is arranged as one or multiple euchromatin loops.

We also investigated the position of the long arm 4L by using 113 individually labeled BACs and observed dispersed signals, representing either separated (79%, n = 52 nuclei) or associated (21%) territories of 4L homologs (Fig. 3J), which is in accordance with the association frequency of homologous CC4s (see below). The dispersed pattern of hybridization signals suggests multiple loop structures. We could not trace megabase-sized loops spanning the entire long arm. However, when we probed the distal 12 BACs of 4L, we found 29% (n = 68) of the signals closely associated with CC4 that was identified by short-arm BACs (Fig. 3K). BACs from the middle of the long arm gave similar results (Fig. 3L). This implies that compartmentalization of euchromatic segments with CCs may occur along the entire chromosome 4, forming loop structures around its CC (Fig. 4). FISH experiments with DNA sequences from other chromosomes also showed hybridization signals at and outside the CCs, suggesting a similar CC–loop organization. Within the loops, the degree of chromatin condensation may vary. For example, yeast artificial chromosome 8B1, which covers the heterochromatic knob hk4S of the accession Wassileskija (20), is highly condensed (1 Mbp/µm), compared with the adjacent yeast artificial chromosome 7C3 (180 kb/µm) (Fig. 3C).

View larger version (29K): [in this window] [in a new window]   Fig 4. CC–loop model for the organization of chromosome 4 in Arabidopsis nuclei. Heterochromatic regions compartmentalize into one CC, whereas euchromatin forms 0.2- to 2-Mbp loops around this CC. CCs contain heavily methylated DNA (Me), whereas euchromatin loops are enriched in acetylated histone H4 (Ac). The colored blocks represent interstitial, contiguous BACs that show different positions relative to the CC depending on the loop organization.

View larger version (53K): [in this window] [in a new window]   Fig 5. Histogram showing the percentage of separate homologous CCs. CC1 and CC3, which could not be distinguished from each other, are combined as one group.

	Discussion

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Our study revealed a relatively simple organization of chromosomes within Arabidopsis nuclei with chromosome territories consisting of a single repeat-rich, heterochromatic CC, from which gene-rich, euchromatic loops emanate, spanning 0.2–2 Mbp. CCs and loops differ as to the level of DNA methylation and histone H4 acetylation, reflecting the transcriptional inactivity of CCs. This also is supported by strong methylation of lysine 9 of histone H3 only at CCs and of lysine 4 of H3 outside CCs (Z. Jasencakova and W. Soppe, personal communication). The simple arrangement of chromatin and the ability to identify individual CCs and loops makes the Arabidopsis nucleus an attractive model with which to study eukaryotic chromosome organization in relation to genomic functions.

Several models of higher-order chromatin structures have been proposed based on microscopic investigation of human interphase chromosomes (2, 15, 35–38). Chromosomes occupy a discrete territory, within which compact chromatin domains are distinguishable from less condensed ones (2, 39, 40). Gene-rich regions are preferentially at the periphery of a chromosome territory, but transcription appears to take place especially at or near the surface of the compact domains (15). It is assumed that 30-nm chromatin fibers emanate as loops from a flexible backbone. How these loops correspond with euchromatin and heterochromatin regions within chromosome territories remains elusive, because of the complex architecture of the human nucleus. A 3-D analysis of the major histocompatibility complex locus on chromosome 6 revealed megabase-sized loops containing active genes extruding from the chromosome 6 territory (41). Because of structural differences between both genomes, it is yet unclear whether these loops are equivalent to the loops found in Arabidopsis nuclei. Based on the genomic sequence (17, 42), we estimate the content of the average chromosome territory of Arabidopsis at 25 Mbp of DNA with 5,200 genes, which is strikingly contrasting with the average human chromosome territory, which contains five times more DNA (130 Mbp) but only 1,700 genes.

According to the CC–loop model, some euchromatin regions compartmentalize with CCs, which may affect transcriptional activity in these regions. Heterochromatin-mediated gene silencing is known for Drosophila (11, 12), involving Su(var) proteins, and for mammals (13), involving Ikaros proteins. It is tempting to speculate that physical association of gene regions with heterochromatic CCs in Arabidopsis may lead to transcriptional inactivation of the corresponding genes.

We observed frequent association of CCs in Arabidopsis nuclei, a phenomenon that has been observed in many species, including mammals. In fact, CCs may represent nonrandom spatial association of certain centromeres (39). Furthermore, homologous association of human chromosome territories occurs more frequently for gene-dense, small chromosomes (40). By differential chromosome painting with BAC contigs, we demonstrated homologous association of CCs and chromosome territories. Strikingly, the FISH images revealed perfect alignment of homologous subregions up to a few megabases, possibly controlled by heterochromatin. Heterochromatin has been proposed to play a role in long-range interactions as a matchmaker to promote mitotic alignment of homologs or homologous chromosome regions in Drosophila (43), where somatic pairing of homologs seems to be a general phenomenon. Somatic pairing of homologs has been implicated in at least one example of allelic DNA interaction, in this case, tobacco (44), of which there are many examples in plants. Whether heterochromatin generally is involved in somatic transinteraction of homologous DNA sequences remains to be investigated. The Arabidopsis nucleus may prove a valuable system with which to investigate these and other fundamental questions on chromosome dynamics and epigenetic regulation mechanisms in plants.

	Acknowledgements

 
We thank R. van Driel and B. van Steensel for critically reading the manuscript, P. Zabel for valuable discussions, and B. M. Turner (University of Birmingham Medical School, Birmingham, U.K.) for providing antibodies against acetylated histones. This project was supported by grants from the Deutsche Forschungsgemeinschaft (FR 1497/1-1 to P.F.) and the Land Sachsen-Anhalt (3035A/0088B and 2333A/0020B to I.S.).

	Footnotes

 
To whom correspondence should be sent at the present address: Swammerdam Institute for Life Sciences, University of Amsterdam, Kruislaan 318, 1098 SM, Amsterdam, The Netherlands. E-mail: fransz{at}science.uva.nl.

This paper was submitted directly (Track II) to the PNAS office.

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				A. Berr and I. Schubert Interphase Chromosome Arrangement in Arabidopsis thaliana Is Similar in Differentiated and Meristematic Tissues and Shows a Transient Mirror Symmetry After Nuclear Division Genetics, June 1, 2007; 176(2): 853 - 863. [Abstract] [Full Text] [PDF]

				C. Baroux, A. Pecinka, J. Fuchs, I. Schubert, and U. Grossniklaus The Triploid Endosperm Genome of Arabidopsis Adopts a Peculiar, Parental-Dosage-Dependent Chromatin Organization PLANT CELL, June 1, 2007; 19(6): 1782 - 1794. [Abstract] [Full Text] [PDF]

				F. Tessadori, M.-C. Chupeau, Y. Chupeau, M. Knip, S. Germann, R. van Driel, P. Fransz, and V. Gaudin Large-scale dissociation and sequential reassembly of pericentric heterochromatin in dedifferentiated Arabidopsis cells J. Cell Sci., April 1, 2007; 120(7): 1200 - 1208. [Abstract] [Full Text] [PDF]

				R. B. Deal, C. N. Topp, E. C. McKinney, and R. B. Meagher Repression of Flowering in Arabidopsis Requires Activation of FLOWERING LOCUS C Expression by the Histone Variant H2A.Z PLANT CELL, January 1, 2007; 19(1): 74 - 83. [Abstract] [Full Text] [PDF]

				A. Kirik, A. Pecinka, E. Wendeler, and B. Reiss The Chromatin Assembly Factor Subunit FASCIATA1 Is Involved in Homologous Recombination in Plants PLANT CELL, October 1, 2006; 18(10): 2431 - 2442. [Abstract] [Full Text] [PDF]

				R. DeCook, S. Lall, D. Nettleton, and S. H. Howell Genetic Regulation of Gene Expression During Shoot Development in Arabidopsis Genetics, February 1, 2006; 172(2): 1155 - 1164. [Abstract] [Full Text] [PDF]

				V. Schubert, M. Klatte, A. Pecinka, A. Meister, Z. Jasencakova, and I. Schubert Sister Chromatids Are Often Incompletely Aligned in Meristematic and Endopolyploid Interphase Nuclei of Arabidopsis thaliana Genetics, January 1, 2006; 172(1): 467 - 475. [Abstract] [Full Text] [PDF]

				R. T. GRANT-DOWNTON and H. G. DICKINSON Epigenetics and its Implications for Plant Biology. 1. The Epigenetic Network in Plants Ann. Bot., December 1, 2005; 96(7): 1143 - 1164. [Abstract] [Full Text] [PDF]

				A. J.M. Matzke, B. Huettel, J. van der Winden, and M. Matzke Use of Two-Color Fluorescence-Tagged Transgenes to Study Interphase Chromosomes in Living Plants Plant Physiology, December 1, 2005; 139(4): 1586 - 1596. [Abstract] [Full Text] [PDF]

				Y. Fang and D. L. Spector Centromere Positioning and Dynamics in Living Arabidopsis Plants Mol. Biol. Cell, December 1, 2005; 16(12): 5710 - 5718. [Abstract] [Full Text] [PDF]

				A. M. Boutanaev, L. M. Mikhaylova, and D. I. Nurminsky The Pattern of Chromosome Folding in Interphase Is Outlined by the Linear Gene Density Profile Mol. Cell. Biol., September 15, 2005; 25(18): 8379 - 8386. [Abstract] [Full Text] [PDF]

				E. V. Shakirov, Y. V. Surovtseva, N. Osbun, and D. E. Shippen The Arabidopsis Pot1 and Pot2 Proteins Function in Telomere Length Homeostasis and Chromosome End Protection Mol. Cell. Biol., September 1, 2005; 25(17): 7725 - 7733. [Abstract] [Full Text] [PDF]

				A. Pecinka, N. Kato, A. Meister, A. V. Probst, I. Schubert, and E. Lam Tandem repetitive transgenes and fluorescent chromatin tags alter local interphase chromosome arrangement in Arabidopsis thaliana J. Cell Sci., August 15, 2005; 118(16): 3751 - 3758. [Abstract] [Full Text] [PDF]

				A. Zemach, Y. Li, B. Wayburn, H. Ben-Meir, V. Kiss, Y. Avivi, V. Kalchenko, S. E. Jacobsen, and G. Grafi DDM1 Binds Arabidopsis Methyl-CpG Binding Domain Proteins and Affects Their Subnuclear Localization PLANT CELL, May 1, 2005; 17(5): 1549 - 1558. [Abstract] [Full Text] [PDF]

				K. Bystricky, T. Laroche, G. van Houwe, M. Blaszczyk, and S. M. Gasser Chromosome looping in yeast: telomere pairing and coordinated movement reflect anchoring efficiency and territorial organization J. Cell Biol., January 31, 2005; 168(3): 375 - 387. [Abstract] [Full Text] [PDF]

				B. Arnholdt-Schmitt Stress-Induced Cell Reprogramming. A Role for Global Genome Regulation? Plant Physiology, September 1, 2004; 136(1): 2579 - 2586. [Full Text] [PDF]