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Higher Order Chromatin Structures in Maize and ArabidopsisAnna-Lisa Paula and Robert J. Ferlaa Program in Plant Molecular and Cellular Biology, Department of Horticultural Sciences, University of Florida, Gainesville, Florida 32611 Correspondence to: Robert J. Ferl, robferl{at}nervm.nerdc.ufl.edu (E-mail), 352-392-4072 (fax).
We are investigating the nature of plant genome domain organization by using DNase I– and topoisomerase II–mediated cleavage to produce domains reflecting higher order chromatin structures. Limited digestion of nuclei with DNase I results in the conversion of the >800 kb genomic DNA to an accumulation of fragments that represents a collection of individual domains of the genome created by preferential cleavage at super-hypersensitive regions. The median size of these fragments is ~45 kb in maize and ~25 kb in Arabidopsis. Hybridization analyses with specific gene probes revealed that individual genes occupy discrete domains within the distribution created by DNase I. The maize alcohol dehydrogenase Adh1 gene occupies a domain of 90 kb, and the maize general regulatory factor GRF1 gene occupies a domain of 100 kb in length. Arabidopsis Adh was found within two distinct domains of 8.3 and 6.1 kb, whereas an Arabidopsis GRF gene occupies a single domain of 27 kb. The domains created by topoisomerase II–mediated cleavage are identical in size to those created by DNase I. These results imply that the genome is not packaged by means of a random gathering of the genome into domains of indiscriminate length but rather that the genome is gathered into specific domains and that a gene consistently occupies a discrete physical section of the genome. Our proposed model is that these large organizational domains represent the fundamental structural loop domains created by attachment of chromatin to the nuclear matrix at loop basements. These loop domains may be distinct from the domains created by the matrix attachment regions that typically flank smaller, often functionally distinct sections of the genome.
The genome of eukaryotes is thought to be organized into topologically independent, supercoiled loop domains of chromatin anchored by attachments to a protein matrix in the nucleus (
The term "matrix association/attachment region" or MAR was coined to refer to the chromosomal loop attachments characterized in interphase nuclei (
Although it is widely accepted that the eukaryotic genome is organized into looped domains that are anchored by attachment to the nuclear matrix, there is not yet a consensus regarding the frequency of MAR distribution in the genome and the in vivo role of MARs in genome organization. This contraposition is partly due to the fact that the type of MAR isolation method used for in vitro assays may influence the estimated number, placement, and type of MAR identified for a given system (e.g.,
Figure 1 shows an ethidium bromide–stained contour-clamped homogeneous electric field (CHEF) gel of limited DNase I digestion of maize nuclei. The pulsed field electrophoresis parameters for the CHEF gel shown in Figure 1A created a region of compression that migrates behind the 800-kb limit of the size markers (the "parent" genomic DNA band; this band represents the intact, unfragmented genome that is >800 kb in length) and allowed for resolution of fragments ranging from ~400 to 5 kb. Increasing the concentration of DNase I converted the parent band into an accumulation of a specific set of subgenomic fragments. It can be seen from the stained gel that the parent band was completely converted to a set of fragments that have a median size of 45 kb, without first creating a larger sized set at lower DNase I concentrations and without creating smaller sets of fragments at higher concentrations of DNase I.
Figure 1B shows a series of densitometric scans of selected lanes from the gel in Figure 1A. The black line is the 0.0 µg/mL DNase I control. The gray lines illustrate how the parent band is converted to the domain-sized fragments with an increase in DNase I concentration. Note that the peak, centered at ~45 kb, increases in proportion to the decrease of the peak centered over the compressed parent band at >800 kb, and no other peaks are formed. The control lanes in Figure 1A (the first two lanes are the untreated control and the 0.0 µg/mL DNase I control, respectively) and the black line in Figure 1B (0.0 µg/mL DNase I) indicate the levels of endogenous nuclease activity in the nuclei. The faint bands produced by endogenous nucleases correspond in size with the bands generated by exogenous DNase I in the subsequent lanes. The size distribution of domains among plant species is variable. However, a comparison of three species with widely different genome sizes indicates that genome size is not directly correlated with a median domain size. Figure 2 shows the domains created by DNase I digestion in lily, maize, and Arabidopsis by using CHEF gel running parameters designed to expand the resolution in the 10- to 100-kb range. Lily, with the largest genome size (~1011 bp), shows a median domain size of 35 kb, whereas maize (109 bp) has a median domain size of 45 kb. The median domain size for Arabidopsis is almost half that of maize at 25 kb, but the genome size (107 bp) is close to 100 times smaller than that of maize. These apparent domain size differences also indirectly suggest that the accumulation of fragments at approximately a median size is not a CHEF gel artifact, because each plant generates a different size class distribution.
The digestion of naked (protein-free) DNA with DNase I and subsequent resolution of the digestion products on a CHEF gel also address the possibility of gel artifacts as well as whether the accumulation of fragments is mediated by chromatin. These data are shown in Figure 3. It is common practice to generate naked DNA controls for in vivo and chromatin analyses (e.g.,
These problems were addressed by two different naked DNA digestions shown in Figure 3. For Arabidopsis, conventional bulk genomic DNA preparations yield DNA fragments greater than the 25-kb median domain generated with nuclear DNase I digestion. Direct DNase I digestion of purified Arabidopsis DNA with DNase I failed to show the accumulation of any specific size class of fragments (Figure 3A). The first lane in Figure 3A illustrates the degree to which genomic DNA is fragmented by a conventional isolation technique (CsCl density gradients; e.g., For maize, bulk genomic DNA preparations (such as the CsCl gradients used for the Arabidopsis DNA in Figure 3A) already are fragmented to a size range close to that of the nuclear domain size, so instead of using bulk DNA preparations, naked DNA digestions were performed on the parent-genomic band from untreated nuclei run on preparative CHEF gels. In this case, the control represents an agarose plug containing the parent-genomic DNA band excised from a preparative CHEF gel of untreated nuclei (see Methods) and rerun on the CHEF gel shown in Figure 3B. Lanes 2 and 3 in Figure 3B show the results of digesting a similar plug containing the parent genomic DNA band with 0.05 and 0.10 µg/mL DNase I. Digestion of embedded naked DNA results in a more general smear of fragments than is seen with DNase I digestions of nuclei. Hybridization with gene-specific probes from maize and Arabidopsis indicates that genes occupy discrete domains of defined length. The ethidium bromide–stained CHEF gel in Figure 4A shows the molecular length markers next to the lanes used for the subsequent hybridizations. Note that the CHEF gel running parameters for Figure 4A, and all subsequent CHEF gel figures, are such that the resolution between 5 and 100 kb is expanded significantly compared with the parameters used in the CHEF gels shown in Figure 1. The median domain fragment size is still 45 kb for maize, but these running parameters also illustrate that although most fragments ranged close to the median size, many were much larger or smaller than the median. The sizes of individual domains can be visualized by hybridizing with specific genes. Maize alcohol dehydrogenase (Adh1) was used as a probe in the blot shown in Figure 4B and hybridized with a 90-kb fragment. Stripping this blot and reprobing with the probe for maize general regulatory factor 1 (GRF1) (Figure 4C) illustrates that this gene resides on a 100-kb domain—a domain clearly distinct from the fragment occupied by Adh1. The size of individual gene domains is also apparent in Arabidopsis. Figure 5A shows the ethidium bromide–stained CHEF gel of domain fragments from the Arabidopsis genome used for the hybridization analyses. The Arabidopsis Adh gene was used as a probe in the blot shown in Figure 5B and shows hybridization with two bands—one of 8.3 kb and one of 6.1 kb. Reprobing this blot with the Arabidopsis GRF4 gene shows that this gene resides on a domain fragment of 27 kb (Figure 5C).
Domains liberated by topoisomerase II–mediated cleavage correlated in length with domains liberated by DNase I. The cytotoxic drugs VM26 and genistein create cleavable complexes at topoisomerase II sites, but the creation of the cleavable complex is an inefficient process. Nonetheless, drug-released domains were observed when VM26 and genistein were incubated with Arabidopsis protoplasts, and the resulting DNA was analyzed (Figure 6). The blot shown in Figure 6 was hybridized with Arabidopsis Adh and shows evidence of drug-dependent cleavage. VM26 and genistein both produced the same 8.3- and 6.1-kb bands that were generated by the DNase I treatments shown in Figure 5B.
Figure 7 demonstrates that the hybridizing bands illustrated in Figure 5 and Figure 6 are the result of chromatin-associated effects in the genome. Arabidopsis genomic DNA (CsCl gradient purified) was digested with increasing concentrations of DNase I or VM26, resolved by using conventional electrophoresis (Figure 7A) and CHEF analysis (Figure 7B), transferred to nylon membranes, and hybridized with the same Adh probe used in Figure 5 and Figure 6. No specific hybridizing bands were detected in naked genomic DNA after in vitro digestion with DNase I or treatment with VM26.
The hybridization data of Figure 4 and Figure 5 are summarized in Figure 8A and Figure 8B. Figure 8C and Figure 8D address the presence of a wide, hybridizing band averaging 45 kb for maize Adh1 and GRF1 and a similar smear centered at ~25 kb in the blots with Arabidopsis DNA. Densitometric scans of hybridized lanes were compared with a lane from the ethidium bromide–stained CHEF gel. Figure 8A shows the data for maize. The black line represents the densitometric scan of the bottom (ethidium bromide–stained) lane, the dark gray line represents the middle Adh1 lane, and the light gray line represents the top GRF1 lane. Note that each scan has a similar peak profile centered at ~45 kb, suggesting that nonspecific hybridization contributes to this peak. Figure 8B shows similar scans of the data for Arabidopsis. The black line represents the ethidium-stained lane on the bottom, the dark gray line represents the middle Adh lane, and the light gray line represents the top GRF4 lane. Again, the broad peak centered at ~25 kb is seen in all scans, whereas gene-specific bands rise above this profile. However, for Arabidopsis, the gene-specific bands rise more fully above the background hybridization than is the case for maize.
An additional experiment was conducted to approximate the relative contribution of nonspecific hybridization to this broad band. Figure 8C and Figure 8D compare the amount of background hybridization between the domain analysis of maize Adh1 and a simple restriction digest of embedded maize nuclei, respectively. Both blots were probed with a section of the Adh1 promoter. In Figure 8C, the region under the curve defining the hybridizing region of the scan profile was integrated (dark gray plus light gray) and divided into the integrated value of the area under the specific peaks (light gray). This value was compared with a similar calculation conducted on BamHI-digested DNA that was resolved on a CHEF gel (Figure 8D). The two hybridizing BamHI fragments can be seen to rise above the background in a fashion similar to the DNase I–liberated hybridizing fragments. In the case of the restricted DNA, all of the background signal can be attributed to nonspecific hybridization to random, probably repetitive sequences in the genome. A comparison of the signal-to-background ratios for the fragments created by DNase I (Figure 8C) and the BamHI fragments (Figure 8D) suggests that at least 40% of the broad-band signal seen with the DNase I experiments can be attributed to nonspecific hybridization.
The data presented here indicate that limited DNase I treatment of nuclei releases discrete, defined regions of chromatin that correlate with domains released by topoisomerase II poisons. This observation is consistent with observations from animal systems and with a model wherein domain release is due to super DNase I hypersensitivity at loop basement attachments. Extrapolation of this model suggests that plant genomes are organized into looped domains much like animal genomes. Moreover, these results show that specific genes can be localized to specific loop-sized fragments, suggesting that the organization imposed on the genome to facilitate condensation and packaging is not random. The idea of small-scale domains created by attachments to the matrix (in which specific MARs play a role in defining the functional domain of a gene) is well documented (e.g.,
Much of the evidence contributing to the hypothesis that the eukaryotic genome is organized into looped domains is derived from experiments designed to create scissions at putative loop basements; the premise is that supercoiled structures (such as those envisioned for the loops) are torsionally stressed and contain sections of DNA that are extremely hypersensitive to enzymatic reagents, such as DNase I, S1 nuclease, and Bal 31 nuclease, in the sequences associated with the attachment region. However, the relationship between loop basements and MARs has yet to be established. Many of the MARs that define topologically discrete sections in the genome contain topoisomerase II recognition motifs and subsequently are vulnerable to the actions of cytotoxic drugs (such as VM26) that generate a cleavable complex with topoisomerase II (
The current data from maize and Arabidopsis provide an opportunity to draw conclusions about higher order chromatin structure in plants in three areas: the contribution of looped domains in the global packaging of the genome, the domain loop size distribution among plants, and the gene distribution among individual loops. The first issue is addressed by the pattern of DNase I–mediated cleavage domain fragments described in Figure 1. These data suggest that the LBARs are intensely hypersensitive to DNase I and represent extreme hot spots of nuclease sensitivity in the genome that are more reactive than other hypersensitive sites, such as those in gene promoter regions that are not resolved under the conditions used in these experiments (
Second, the median size of the chromatin loops that organize the genome appears to be variable among plants. This is an especially striking feature in the comparison of maize and Arabidopsis because the median size of chromatin loops in these plants varies by almost twofold (45 and 25 kb, respectively). It is tempting to speculate that this difference reflects the disparity in the sizes and repetitive nature of the maize and Arabidopsis genomes; however, because a representative from the genus Lilium (whose members contain extremely repetitive genomes as large as 1011 bp) was shown to be organized into loops averaging 35 kb (Figure 2), this generalization cannot be applied to all plants. There is (to our knowledge) only one other example of a characterization of chromatin loops in plants.
The third and most important implication from the work presented in this study is that the genome is not organized into random loops of chromatin but rather that a gene occupies an organizational loop of discrete and defined length within the genome. In maize, the Adh1 and GRF1 genes occupy loops of 90 and 100 kb, respectively. In Arabidopsis, the Adh gene is found within two distinct loops at 8.3 and 6.1 kb, whereas the GRF4 gene occupies a single loop of 27 kb. If the loop sizes were random in the genomes of these plants, individual loops would not have been detected as hybridizing bands. This conclusion is supported by the fact that different genes occupy loops of different sizes. Thus far, there are no other examples of single-copy genes that have been identified with a discrete loop size in vivo with which these data can be compared. However, in an example of direct hybridization of CHEF-resolved loops from a human cell line, it was found that the c-myc amplicon fell within a range of fragments between 80 and 110 kb ( LBARs, then, are areas of extreme hypersensitivity to DNase I that likely mark the boundaries of structural loops within the chromatin structure of the genome. This conclusion is supported by control digestions of naked genomic DNA, which fail to produce discrete domains. The potential co-residence at LBARs of DNase I hypersensitivity and topo-isomerase poison cleavage suggests that LBARs are sites of direct attachment to the matrix and that this attachment forms the basis for loop domains. The discrete hybridization of genes to individual loop domains suggests that the LBAR-mediated attachments are fundamentally stable within the genome. However, not all of the gene-specific hybridization is within the liberated specific domains. In these experiments, there is hybridization associated with the broad distribution of DNA characteristic of that species. This background hybridization may be artifactual, because a large portion of the broad-band signal can be attributed to nonspecific hybridization to high concentrations of DNA and because the broad-band signal is reduced in Arabidopsis compared with maize. It is also possible that the specific domains identified here represent only the most stable loop configuration within the population of cells and that a broad range of loop sizes also exists at lower frequencies. These data extend the model that genomes are organized into anchored loops in eukaryotes in general. Thus far, however, the implication that the global packaging of the eukaryotic genome is not through random condensation and that genes occupy a loop of discrete and defined length within the genome is limited to these plant systems.
Preparation of Nuclei
DNase I Treatments
Naked DNA Control for DNase I Digestions
An additional naked DNA control was conducted with CsCl density gradient–purified Arabidopsis genomic DNA. This method (previously described in
Cytotoxic Drug Treatments
Pulsed-Field Electrophoresis Conditions
We thank Dr. William T. Garrard for helpful discussions of this work and Dr. Korby Kistler for initial advice and help with CHEF analysis. This work was supported by grants from the U.S. Department of Agriculture National Research Initiative (No. 94-37301-0565) and National Institutes of Health (No. ROI GM 40061). This report is journal series number R-06339 of the Florida Agricultural Experiment Station. Received January 30, 1998; accepted May 18, 1998.
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-globin gene domain by nuclease S1 and characterization of the framing structures. Proc. Natl. Acad. Sci. USA 91:4422-4426
