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Two Distinct Domains in Drosophila Melanogaster Telomeres

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Two Distinct Domains in Drosophila Melanogaster Telomeres Copyright Ó 2005 by the Genetics Society of America DOI: 10.1534/genetics.105.048827 Two Distinct Domains in Drosophila melanogaster Telomeres Harald Biessmann,* Sudha Prasad,† Valery F. Semeshin,‡ Eugenia N. Andreyeva,‡ Quang Nguyen,§ Marika F. Walter* and James M. Mason†,1 *Developmental Biology Center, University of California, Irvine, California 92697, †Laboratory of Molecular Genetics, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina 27709, ‡Laboratory of Molecular Cytogenetics, Institute of Cytology and Genetics, Russian Academy of Sciences, Novosibirsk 630090, Russia and §Department of Biological Chemistry, University of California, Irvine, California 92697 Manuscript received July 27, 2005 Accepted for publication August 16, 2005 ABSTRACT Telomeres are generally considered heterochromatic. On the basis of DNA composition, the telomeric region of Drosophila melanogaster contains two distinct subdomains: a subtelomeric region of repetitive DNA, termed TAS, and a terminal array of retrotransposons, which perform the elongation function instead of telomerase. We have identified several P-element insertions into this retrotransposon array and compared expression levels of transgenes with similar integrations into TAS and euchromatic regions. In contrast to insertions in TAS, which are silenced, reporter genes in the terminal HeT-A, TAHRE,orTART retroelements did not exhibit repressed expression in comparison with the same transgene construct in euchromatin. These data, in combination with cytological studies, provide evidence that the subtelomeric TAS region exhibits features resembling heterochromatin, while the terminal retrotransposon array exhibits euchromatic characteristics. NA sequences at the ends of eukaryotic chromo- tandem repeats of 457 bp (Walter et al. 1995; Mason D somes are the products of a telomere elongation et al. 2003b). While the TAS array on other chromo- process. In most eukaryotes, these sequences are simple somes may be of similar size (Abad et al. 2004a), X TAS repeating units that are synthesized by telomerase, but is more complex with a 1.8-kb and a 0.9-kb repeat, which in Drosophila melanogaster they are tandem head-to-tail are related to each other (Karpen and Spradling 1992). arrays of three non-long terminal repeat retrotranspo- Drosophila telomeric regions are able to repress gene sons, HeT-A, TAHRE,andTART (Mason and Biessmann activity, resulting in partial silencing and variegated 1995; Pardue and DeBaryshe 2003; Abad et al. 2004b). expression of reporter genes (Karpen and Spradling Despite these differences, a common feature of eukary- 1992), referred to as telomeric position effect (TPE). otic chromosomes is a region of complex repeats located These repressed transgenes have inserted into or adja- adjacent to the terminal sequences. These complex cent to TAS (Levis et al. 1993; Cryderman et al. 1999; repeats are referred to as subtelomeric regions, or Golubovsky et al. 2001), suggesting that TAS regions of telomere-associated sequences (TAS), and differ in se- Drosophila telomeres are heterochromatic. quence, structure, and length among species and among No integrations into the terminal retrotransposon telomeres within an individual (Pryde et al. 1997). The array have been reported. There are several possible ex- repetitive nature and the high density of transposable planations for the absence of these integration events. elements in these subtelomeric regions (Mefford and First, the chromatin structure of the retrotransposon Trask 2002) are reminiscent of heterochromatin. In array may not allow integration of P elements, or if D. melanogaster, TAS consist of several kilobases of com- integrations do occur, they may be unstable. Second, plex repeats, which exhibit similarities between the dif- integration events may occur in the HeT-A/TART/ ferent chromosome ends. Sequences of the 2L and TAHRE array but are not detectable, because expression X TAS regions have been described in detail (Karpen of the reporter gene is completely repressed due to the and Spradling 1992; Walter et al. 1995), and in situ heterochromatic nature of the terminal array. Third, hybridizations to polytene chromosomes showed that integrations may occur, but expression is not repressed; 2L TAS share homology with 3L TAS, while X TAS share thus, insertion events are not distinguishable from homology with 2R and 3R TAS. The 2L TAS appear to integrations into euchromatic sites. To address this ques- be 15 kb in length and composed of relatively simple tion, we took advantage of the P-element mobilization screen performed by the Berkeley Drosophila Genome Project (BDGP) Gene Disruption Project to generate 1Corresponding author: Laboratory of Molecular Genetics, National ellen Institute of Environmental Health Sciences, 111 Alexander Dr., Research insertions at every Drosophila gene (B et al. 2004). Triangle Park, NC 27709-2233. E-mail: [email protected] This screen generated .30,000 independent P-element Genetics 171: 1767–1777 (December 2005) 1768 H. Biessmann et al. integrations using constructs SuPor-P and EPgy2. After expression of the transgene can be observed without further performing inverse PCR, the BDGP sequenced the 59- crosses. and 39-flanking regions to determine the genomic Flanking sequences were obtained from R. Levis and batch blasted (BlastN) (Altschul et al. 1997) against sequences location of each integration. We reasoned that among from HeT-A (GenBank U06920), TART-A (U02279), TART-B1 the large number of P-element integrations there might (U14101), TART-B2 (U14102), TART-C (U02279), 2LTAS be some that had inserted into the HeT-A/TAHRE/ (U35404), and 1.8-kb X-TAS (L03284). To identify potential TART array, unless this terminal region is refractory to telomeric insertions when both 39- and 59-flanking regions integration. Indeed, by screening genomic sequences of the P-element integration had been determined, we re- quired that both identified the same region in the telomeric flanking the P-element insertions for similarity to HeT-A retrotransposon and showed the 8-bp duplication generated and TART, several such integrations were identified. by the P element. In cases when only one of the flanking Extant strains were then subjected to molecular genetic regions was known, sequence identity to HeT-A, TART,orTAS analyses, and the phenotypic expression levels of the had to be at least 80% over a substantial part of the flank. In reporter genes were determined. addition to insertions identified in this manner, a SuPor-P element in 3R TAS, 316-1 (Roseman et al. 1995), was provided The experiments described in this article were per- by P. Geyer. SuPor-P (KG04716 at position 21A5–B1, KG00040 formed for several reasons: (a) to investigate the mor- at 60E1, and KG03807 at 60D15–16) and EPgy2 (EY00630 at phological characteristics of the terminal array and the 59D8, KG00487 at 62A6–7, and KG02201 at 62A11–12) in- TAS subterminal region in polytene chromosomes, (b) sertions into distal euchromatin were obtained from the to determine if P elements can integrate into the ter- Bloomington Stock Center (http://flystocks.bio.indiana.edu) and used as controls in gene expression studies. minal array of the Drosophila telomere, and (c) to in- Genetic isolation of P insertion chromosomes: Drosophila vestigate gene expression at the integration site. The stocks were maintained and crosses were performed at 25° on results show that the terminal array is not refractory to cornmeal, molasses medium with dry yeast added to the P-element insertions. Further, expression of transgenes surface. Genetic markers and special chromosomes are de- ly ase onsortium in the terminal transposon array is not reduced when scribed by FlyBase (F B C 2003). To identify the chromosome carrying the insertion, males carrying the the insertion is far from TAS. Thus, in contrast to TAS, transgene were crossed to yw67c23; Sco/SM1 or yw67c23; Sb/TM6, the terminal arrays do not appear to mediate hetero- 67c23 Ubx females. F1 males were then crossed to yw females, and chromatic gene silencing. However, the silencing effect segregation of the reporter genes was noted. Simultaneous of TAS spreads into the retrotransposon array and can backcrosses of F1 males to balancer females allowed new stocks 67c23 be detected over short distances. We, therefore, suggest to be formed with yw on the X chromosome and the marked element on an autosome. Insertions on the X and that there are two distinct chromatin domains within fourth chromosomes were not considered further. the Drosophila telomere, one consisting of the terminal In a similar fashion, su(Hw)8 was crossed into KG lines to retrotransposon array, which is transcriptionally active, render the SU(HW) binding sites nonfunctional as insulators. and the other containing TAS, which appear by genetic When the SuPor-P element was carried on chromosome 2, 67c23 67c23 assays to be heterochromatic. The chromosome cap may yw , homozygous transgene females were crossed to yw ; Sb/TM6 males, and F1 transgene/1; Sb/1 females crossed be a third telomeric domain that does not contain a spe- 2 8 8 iessmann ason with y sc v; su(Hw) /TM6 males. F2 transgene/1; su(Hw) /Sb cific DNA sequence (B and M 1988), but sons were then crossed with yw67c23; Sb/TM6 females. Transgene/ requires specific capping proteins (Fanti et al. 1998; 1; su(Hw)8/TM6 progeny from this cross were mated together Biessmann et al. 2005; Cenci et al. 2005). in single pairs, and transgene homozygotes were selected by monitoring segregation in subsequent generations. When the SuPor-P element was on chromosome 3, yw67c23, homozygous transgene males were crossed to y2 sc v; su(Hw)8/ 1 67c23 MATERIALS AND METHODS TM6 females, and Ubx F1 females crossed to yw ; Sb/TM6, 1 1 1 Ubx males. Ten F2 sc w v Ubx males were mated singly to P-element inserts and Blast screening: Two P-element yw67c23; Sb/TM6 females and stocks produced by brother-sister constructs were used in the mobilization screen by the BDGP. matings, as above. The resulting stocks were then tested for the SuPor-P (Roseman et al.
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