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Histone Genes Are Clustered but Not Tandemly Repeated in the Chicken Genome (Recombinant DNA/DNA Sequence Analysis/Development) JAMES DOUGLAS ENGEL* and JERRY B

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Histone Genes Are Clustered but Not Tandemly Repeated in the Chicken Genome (Recombinant DNA/DNA Sequence Analysis/Development) JAMES DOUGLAS ENGEL* and JERRY B Proc. NatI. Acad. Sci. USA Vol. 78, No. 5, pp. 2856-2860, May 1981 Biochemistry Histone genes are clustered but not tandemly repeated in the chicken genome (recombinant DNA/DNA sequence analysis/development) JAMES DOUGLAS ENGEL* AND JERRY B. DODGSONt *Department of Biochemistry and Molecular Biology, Northwestern University, Evanston, Illinois 60201; and tDepartment of Microbiology and Public Health and Department of Biochemistry, Michigan State University, East Lansing, Michigan 48824 Communicated by Emanuel Margoliash, February 5, 1981 ABSTRACT: The recombinant chicken DNA library was MATERIALS AND METHODS screened for histone genes by using pSpl7, a recombinant sea urchin DNA probe containing the H2a and H3 genes of Stron- Isolation and Characterization of Histone Gene Recombi- gylocentrotus purpuratus. Three of the isolated A recombinants nants. Isolation of histone-encoding recombinants was accom- have been analyzed by restriction enzyme mapping and Southern plished by screening the previously described A Charon 4A/ blotting; one histone H3 gene-encoding recombinant was further chicken recombinant DNA library (14) by hybridization to the analyzed by DNA sequence determination. These studies reveal 1.9-kilobase pair (kbp) EcoRI fragment of the Strongylocentro- that the chicken histone genes are not tandemly reiterated, but tus purpuratus pSpl7 histone recombinant, which contains the that, atthe least, several histone genes are physically closely linked coding information for the H2a and H3 histone genes (15). in a nonrepetitive arrangement within the chicken genome. The Hybridization was done as described below for nitrocellulose evolutionary implications of this arrangement versus that seen in filters except that the NaCl concentration was 0.75 M, 10% Drosophila and sea urchins is discussed. dextran sulfate was included, and the temperature was 37°C. Competitor nucleic acids were poly(rA) at 10 ,ug/ml, poly(rC) The histone proteins are collectively responsible for the main- at 10 ,Ag/ml, heat-denatured Escherichia coli DNA at 5 ,Ag/ tenance of the primary eukaryotic nuclear DNA structure (1). ml, and E. coli rRNA or tRNA at 10 ,ug/ml. Washes were done The physical organization, replication, and expression of the as described below for nonhomologous hybridizations. Phages eukaryotic genome is controlled, to a greater or lesser degree, forming positive plaques were purified to homogeneity, grown by histone gene expression and histone organization in chro- in liquid culture, and further characterized by analysis ofmap- matin in concert with nonhistone chromosomal proteins (2). ping blots (16) of the individual A recombinants that had been Therefore, histone gene organization and its influence on the hybridized to specific S. purpuratus or D. melanogaster histone expression of those histone genes are of considerable impor- gene-coding fragments (6, 15). tance to an overall view of eukaryotic gene regulation. A recombinants containing pSpl7-complementary DNA se- Although our understanding of histone gene expression has quences were digested with commercial restriction endonu- been facilitated by elegant studies on the organization, arrange- cleases [New England BioLabs, Biotec (Madison, WI), or Be- ment, and developmental shifts of these genes in various sea thesda Research Laboratories (Rockville, MD)], electrophoresed urchin species (3-5) and in Drosophila (6), comparatively little on agarose gels, stained with ethidium bromide, photographed, is known about histone gene arrangement and expression in and blotted to nitrocellulose BA85 (Schleicher and Schuell) as the are re- described (14). Homologous probes (e.g., those isolated from higher eukaryotes. In the former organisms genes chicken DNA) were hybridized to DNA on the filters in a so- peated from about 100 to perhaps 1000 times per haploid ge- lution containing 1 M NaCl, 50 mM Tris-HCl at pH 8.2, 1 mM nome (6-9), whereas in higher eukaryotes the number of gene EDTA, lOx Denhardt's solution, 0.1% sodium dodecyl sulfate, repeats appears to be on the order of 10-50 copies (10-12). sonicated heat-denatured E. coli DNA at 50 ,ug/ml, and 50% The histone genes of the chicken are each represented ap- (vol/vol) formamide at 42°C for at least 3 X Cot,,, for filters (17) proximately 10 times in the genome, reportedly in a tandemly (Cot,12 being the product of DNA concentration and incubation duplicated array (10), as are those in Drosophila and sea urchin. time for 50% hybridization). The filters were then washed twice We were interested in how the normal chicken histone genes at ambient temperature for 5 min in 3 M NaCl/0.3 M sodium were arranged with respect to the erythropoiesis-specific hi- citrate, followed by four 15-min washes in 20 mM Tris1HCl, pH stone H5 genes [which also appear to be repeated 10 times 8.2/1 mM EDTA/1 x Denhardt's solution/0. 1% sodium do- within the genome (13)]. In order to address this question, we decyl sulfate/i mM sodium pyrophosphate at 60°C. Heterol- initiated experiments to isolate and investigate the arrangement ogous hybridizations (e.g., those performed using sea urchin or of the standard histone genes of the chicken. In this paper, we Drosophila clone probes) were performed identically, except describe the initial results ofthese studies and show that: (i) the that 1.5 M NaCl was used in the hybridization buffer and histone genes are clustered (i.e., present within definite groups 0.1-0.3 M NaCl was added to the second filter wash buffer. within the genome), and (ii) the histone genes of the chicken Positions of labeled complementary fragments were deter- are not repeated in tandem arrays. This substantial difference mined by autoradiography (16). between sea urchin and Drosophila as compared to chicken Restriction Enzyme Mapping. Ambiguities apparent in sin- histone gene arrangement may be reflective of some aspects of gle or combined digestion restriction enzyme cleavage maps early embryonic development in these various species. were resolved by a modification of the method of Smith and Birnsteil (18). Singly end-labeled fragments (isolated as outlined The publication costs ofthis article were defrayed in part by page charge below) were digested in the following reaction mixtures: 1-105 payment. This article must therefore be hereby marked "advertise- ment" in accordance with 18 U. S. C. §1734 solely to indicate this fact. Abbreviation: bp, base pair(s). 2856 Downloaded by guest on October 5, 2021 Biochemistry: Engel and Dodgson Proc. Natl. Acad. Sci. USA 78 (1981) 2857 A .1, \I1TT1l 6- rX7 'I/ cpm of end-labeled fragment, 1 Aug of pBR322 DNA (19), plus A Abrlial v Xf o/////zZ//z/asss:A 2 (1-hr) units of restriction endonuclease in 30 A1l. Aliquots (5 ILx /.d) were withdrawn after 2, 4, 6, 8, 10, and 12 min ofdigestion, AUtizelou'- 41--vxx ejw+#ki#MvvL pooled, extracted once with CHClJisoamyl alcohol (24:1, volV 1 'II vol), and precipitated with 0.1 vol of 3 M sodium acetate/0. ACHMd k~ M EDTA. The sample was resuspended in 10 Al of loading ki 1\ buffer and electrophoresed. The agarose or polyacrylamide gels B Hybridization to H2a R\ H3 / were then dried and film was exposed to them (18). Exposure histone gene probes: H2b H4 times were between 15 min and 18 hr, depending on the initial specific activity of the end-labeled DNA fragment. FIG. 1. Restriction enzyme maps of three chicken histone recom- DNA Fragment Isolation. Individual sea urchin or Dro- binants. The maps and positions of hybridization to heterologous sea sophila histone gene DNA sequences to be used as probes were urchin and Drosophila histone gene probes are depicted. (A) Restric- isolated by excision of specific restriction fragments of pSpl7, tion enzyme maps of three separate recombinants. ', EcoRI linkers pSp2, or cDm 500 from gels and hybridized with the chicken/ (14); 1 ,EcoRI; ,BamHI; v,Hindfll; A,Kpn I. (B) Key forprobes used A recombinant blots (above). Specifically, the sea urchin probes to demonstrate the presence of histone genes on the mapped recom- from pSpl7 (15) di- binants shown in A. The determination of the loci of hybridization to prepared were as follows: the H2a gene specific histone gene probes is given in the text and exemplified by the gested with Hha I plus HindIII [yielding an internal (coding) data shown in Fig. 2. fragment], the H2b gene from pSp2 (15) (after subcloning the two Sp2 BamHI/EcoRI fragments in pBR322) digested with BamHI plus Kpn I (yielding a 456-bp 5' end plus internal frag- aged by prior chromosomal blotting data which indicated that ment), the H3 gene from pSpl7 digested with Hha I (yielding the 1.9-kbp EcoRI fragment of pSpl7 (the S. purpuratus re- a 562-bp 5' end plus internal fragment), and the H4 gene from combinant containing the sea urchin H2a and H3 genes) hy- pSp2 digested with Hha I (yielding a 1-kbp 5' end-internal-3' bridized to only a small number ofchromosomal chicken DNA end fragment). These fragments were isolated from the gels by fragments (approximately 10; data not shown). In the first electrophoresis into Whatman 3 MM paper (20), recovered, and screening attempt of the A/chicken library (2 X 105 plaque- then nick-translated (21). The Drosophila histone gene probes forming units) approximately 50 plaques were selected that con- were derived from cDm500 restriction fragments (6, 22) as fol- tinually yielded phage that hybridized to the pSpl7 probe lows: cDm500 DNA was digested with restriction enzyme, through the plaque purification procedures to phage homo- treated with gel-purified calfintestine alkaline phosphatase, and geneity. then labeled at the 5' ends with 32P by using phage T4 polynu- The putative histone gene recombinant DNAs were digested cleotide kinase. The digests were then electrophoresed on 5% with EcoRI, BamHI, HindIII, and Kpn I (as well as all paired polyacrylamide gels (23).
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