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A Spontaneously Opened Ring Chromosome of Drosophila

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A Spontaneously Opened Ring Chromosome of Drosophila Proc. Nati. Acad. Sci. USA Vol. 85, pp. 8116-8120, November 1988 Genetics A spontaneously opened ring chromosome of Drosophila melanogaster has acquired He-T DNA sequences at both new telomeres (heterochromatin/polytene chromosomes/repeated DNA) KAREN LAHEY TRAVERSE AND MARY Lou PARDUE Department of Biology, Massachusetts Institute of Technology, Cambridge, MA 02139 Contributed by Mary Lou Pardue, July 5, 1988 ABSTRACT Ring chromosomes that have been opened to vary even among individuals of the same species. The give linear chromosomes offer an opportunity to study the DNA sequences in this second class are now considered to be sequences associated with new chromosome ends. The Dro- mobile elements (13). Some families ofthese mobile elements sophila melanogaster chromosome C(1)A was originally a ring have terminal repeat structures resembling those of retrovi- chromosome, consisting of two linked X chromosomes, and ruses; others do not. The common feature of mobile se- thus had no telomeres. This chromosome has spontaneously quences is that each site occupied by one of these sequences opened in polytene region 13, a region near the middle of the (a "full" site) can also be found "empty" in other individ- euchromatic arm ofthe X chromosome. The opening ofthe ring uals. has produced two new telomeres on the C(l)A chromosome. The first class of repeated sequences, those with well- Each of the new telomeres has acquired He-T DNA sequences. defined chromosome sites, must also have some degree of He-T DNA is a complex family of repeated sequences found in mobility to account for the dispersion and the continued the telomeric and pericentric heterochromatin of D. melano- co-evolution of the sequences. (This "mobility" could be by gaster chromosomes. He-T DNA sequences are detected, at actual transposition or by gene conversion.) It seems likely various levels, in the most distal band on the end of each that the chromosomal distribution of this class is limited by polytene chromosome in all D. melanogaster stocks. To our some mechanism. Perhaps the sequences have a function that knowledge, these sequences have never been detected within is disruptive within the chromosome arms, leading to rapid the euchromatic chromosomal regions in any stock. The strong loss ofchromosomes (and cells) ifthe sequence is transferred correlation between He-T DNA sequences and telomeric re- to a position in the euchromatic arm. Alternatively, the gions suggests that He-T sequences may have a role in orga- movement of the sequences might be limited by the trans- nizing or maintaining the ends of chromosomes. The associa- position mechanism itself. Perhaps transposition can occur tion of He-T DNA with newly acquired telomeres in a formerly only between two chromosome regions that are physically euchromatic region, polytene region 13, strengthens this cor- associated at the appropriate time in the cell cycle. It seems relation. probable that each of these mechanisms limits some families of repeated sequences and not others. The genomes of eukaryotes contain several classes of re- Although it is now possible to construct minichromosomes peated sequences. For example, some families of repeated in yeast to test questions of chromosome structure (14), this DNA have well-defined chromosome positions, and these can not yet be done for the much larger, and probably more positions are at equivalent sites on multiple chromosomes. complex, chromosomes of higher eukaryotes. Tests of The best-known members ofthis class are the highly repeated hypotheses about chromosome structure in higher eukary- "satellite" DNAs that are found in the centromeric hetero- otes can, however, be made by using some fortunate chro- chromatin of chromosomes from most organisms (1). Other mosomal rearrangements. One such chromosome is the families have also been found to be limited to particular C(1)A chromosome of D. melanogaster. The C(1)A chromo- chromosomal regions. These include families of repeats in some was synthesized by Armentrout in 1964 as a ring with yeast (2), rye (3), Allium cepa (4), and Tetrahymena mito- no telomeres (15). Since that time, C(1)A has opened into a chondrial DNA (5) that are found only adjacent to telomeres. linear chromosome and thus provides an opportunity to In Drosophila melanogaster a family of repeated sequences, analyze two recently acquired telomeres. called He-T DNA, is limited to the regions around the telomeres and the centromeres (6). In Xenopus laevis, the large family of genes encoding the 5S ribosomal RNA genes MATERIALS AND METHODS is found at the telomeres ofthe long arms of all but two ofthe Drosophila Stocks. C(1)A stock S10 and C(J)RM stock S12 chromosomes (7, 8). [This discussion omits the very simple were the kind gift of the late L. Sandler (University of C18(T/A)lA4 repeats that have been found at the ends of Washington). Other stocks are described by Young et al. (6). chromosomes from several lower eukaryotes (9) and, more Recombinant Phage and Plasmids, Probe Preparation, and recently, from Arabidopsis thaliana (10) and humans (11). in Situ Hybridization. All methods are as described by Young Repeats of the Cl18(T/A)1 4 type are thought to be added to et al. (6). the ends of DNA by a template-independent terminal trans- Mitotic Chromosome Preparation. Mitotic chromosomes ferase activity (12) and thus may have a very different origin from brains of third-instar larvae were prepared and stained from the sequences being considered here.] with Hoechst 33258 as described by Gatti and Pimpinelli (16). A second class of repeated sequences in eukaryotes is also found at multiple sites, but the exact positions of these sites RESULTS The publication costs of this article were defrayed in part by page charge The C(1)A Chromosome Has Opened in Polytene Region payment. This article must therefore be hereby marked "advertisement" 13E. The C(J)A chromosome was a spontaneous derivative of in accordance with 18 U.S.C. §1734 solely to indicate this fact. C(J)TR94, a ring composed of two X chromosomes joined at 8116 Downloaded by guest on September 26, 2021 Genetics: Traverse and Pardue Proc. Natl. Acad. Sci. USA 85 (1988) 8117 13 - 7 -.20 1-46.-1 20O-13 mitotic B20 \ 00/ 14 A18A polytene 206( Of1,_,2013 ) 1 2 -,13 13 FIG. 1. Diagram showing the C(1)A ring, as well as the config- uration of the sequence of the opened ring in mitotic and polytene 13E *- e chromosomes. None of the chromosomes is drawn to scale. To compare sizes ofmitotic and polytene chromosomes, see Figs. 2 and 3. Thin lines indicate euchromatic regions. Heavier lines indicate 18A heterochromatin. Relative sizes within each diagram are only ap- .20 proximate. The numbers indicate polytene regions or the equivalent positions on the mitotic chromosome. The mitotic chromosome FIG. 3. Polytene C(I)A chromosome asynapsed in region 20- contains two sister chromatids after DNA replication. The polytene 13E. The chromosome runs from the chromocenter (region 20) out to chromosome is shown with a single chromatid. In the polytene 7A, then folds back on itself and continues to the break in 13E. The chromosome, homologous regions of the chromatid are intimately second segment 20-13E has broken away from the chromocenter and paired; in the diagram these regions are slightly separated for clarity. was lying nearby. It is shown in the Inset. (Giemsa stain; x 950.) The circle near the center ofthe polytene chromosome represents the fused heterochromatin of all of the chromosomes that makes up the seen in preparations of mitotic chromosomes from larval chromocenter. The broken lines in the circle indicate that the C(1)A brain cells (Fig. 2). The C(I)A chromosome is approximately chromatid continues through the chromocenter. In a fraction of the twice the size of the X in to polytene nuclei the homologues are not paired in region 20-13E (as normal and, addition the in Fig. 3). Such asynapsis is indicated in the diagram to emphasize pericentric heterochromatin, it has a region of heterochro- the new telomeres. matin near the middle of one of the arms, an unusual feature for a Drosophila chromosome. In polytene nuclei, the pairing both ends. The derivative was apparently produced by a of homologous regions caused the original C(1)A ring to reverse crossing-over in polytene region 6F2-7A1. The new collapse into a rod with the two regions 1A-6F2 paired to order of polytene bands was /1A-6F2/6F2-1A/20-7A1/ form a single chromosome arm, separated by the chromo- 7A1-20/. At both of the junctions between 1A and 20, center from the two regions 7A-20, which also paired to yield heterochromatic DNA sequences joined the two chromo- a single chromosome arm (Fig. 1). The heterochromatin of somes (15). The new chromosome order yields an unusually the two 1A/20junctions is fused into the chromocenter. The stable compound-ring X chromosome because exchange opened ring C(I)A gives essentially the same polytene con- within the heterochromatin cannot produce a single X with a figuration as the closed ring; however, regions 20-13E do not full complement of genetic material (Fig. 1). The rearrange- pair in a fraction of the nuclei (Figs. 3, 6 a and b). ment that produced C(J)A ensured that either single X The fraction ofnuclei showing asynapsis ofregions 20-13E produced by detachment at the heterochromatin would be varies somewhat from experiment to experiment and may duplicated for some genes and deficient for others and thus, reflect larval growth conditions. Nuclei in which regions 20- if detachment occurred, the resulting single X chromosome 13E do not synapse show that the linearization of C(J)A, would not be able to produce a viable individual.
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