Analysis of Subtelomeric Heterochromatin in the Drosophila Minichromosome Dp1187 by Single P Element Insertional Mutagenesis

Overview

Journal Genetics

Publisher Oxford University Press

Specialty Genetics

Date 1992 Nov 1

PMID 1334894

Citations 174

Authors

G H Karpen

A C Spradling

Affiliations

Soon will be listed here.

Abstract

We investigated whether single P element insertional mutagenesis could be used to analyze heterochromatin within the Drosophila minichromosome Dp1187. Forty-five insertions of the P[lacZ,rosy+] element onto Dp1187 (recovered among 7,825 transpositions) were highly clustered. None was recovered in centromeric heterochromatin, but 39 occurred about 40 kb from the distal telomere within a 4.7-kb hotspot containing tandem copies of a novel 1.8-kb repetitive DNA sequence. The DNA within and distal to this region lacked essential genes and displayed several other properties characteristic of heterochromatin. The rosy+ genes within the inserted transposons were inhibited by position-effect variegation, and the subtelomeric region was underrepresented in polytene salivary gland cells. These experiments demonstrated that P elements preferentially transpose into a small subset of heterochromatic sites, providing a versatile method for studying the structure and function of these chromosome regions. This approach revealed that a Drosophila chromosome contains a large region of subtelomeric heterochromatin with specific structural and genetic properties.

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References

Henikoff S . Position-effect variegation after 60 years. Trends Genet. 1990; 6(12):422-6. DOI: 10.1016/0168-9525(90)90304-o. View

Hilliker A, Appels R . Pleiotropic effects associated with the deletion of heterochromatin surrounding rDNA on the X chromosome of Drosophila. Chromosoma. 1982; 86(4):469-90. DOI: 10.1007/BF00330122. View

Rubin G . Isolation of a telomeric DNA sequence from Drosophila melanogaster. Cold Spring Harb Symp Quant Biol. 1978; 42 Pt 2:1041-6. DOI: 10.1101/sqb.1978.042.01.104. View

Ronsseray S, Lehmann M, Anxolabehere D . The maternally inherited regulation of P elements in Drosophila melanogaster can be elicited by two P copies at cytological site 1A on the X chromosome. Genetics. 1991; 129(2):501-12. PMC: 1204639. DOI: 10.1093/genetics/129.2.501. View

Newlon C, Lipchitz L, Collins I, Deshpande A, Devenish R, Green R . Analysis of a circular derivative of Saccharomyces cerevisiae chromosome III: a physical map and identification and location of ARS elements. Genetics. 1991; 129(2):343-57. PMC: 1204628. DOI: 10.1093/genetics/129.2.343. View

Spradling A, Karpen G . Sixty years of mystery. Genetics. 1990; 126(4):779-84. PMC: 1204277. DOI: 10.1093/genetics/126.4.779. View

Misra S, Rio D . Cytotype control of Drosophila P element transposition: the 66 kd protein is a repressor of transposase activity. Cell. 1990; 62(2):269-84. DOI: 10.1016/0092-8674(90)90365-l. View

de Lange T, Shiue L, Myers R, Cox D, Naylor S, Killery A . Structure and variability of human chromosome ends. Mol Cell Biol. 1990; 10(2):518-27. PMC: 360828. DOI: 10.1128/mcb.10.2.518-527.1990. View

Fleming R, DeSimone S, White K . Molecular isolation and analysis of the erect wing locus in Drosophila melanogaster. Mol Cell Biol. 1989; 9(2):719-25. PMC: 362649. DOI: 10.1128/mcb.9.2.719-725.1989. View

10.

Ajioka J, Eanes W . The accumulation of P-elements on the tip of the X chromosome in populations of Drosophila melanogaster. Genet Res. 1989; 53(1):1-6. DOI: 10.1017/s0016672300027798. View

11.

Levis R . Viable deletions of a telomere from a Drosophila chromosome. Cell. 1989; 58(4):791-801. DOI: 10.1016/0092-8674(89)90112-8. View

12.

Robertson H, Engels W . Modified P elements that mimic the P cytotype in Drosophila melanogaster. Genetics. 1989; 123(4):815-24. PMC: 1203891. DOI: 10.1093/genetics/123.4.815. View

13.

Traverse K, Pardue M . Studies of He-T DNA sequences in the pericentric regions of Drosophila chromosomes. Chromosoma. 1989; 97(4):261-71. DOI: 10.1007/BF00371965. View

14.

Shevelyov YuYa , Balakireva M, Gvozdev V . Heterochromatic regions in different Drosophila melanogaster stocks contain similar arrangements of moderate repeats with inserted copia-like elements (MDG1). Chromosoma. 1989; 98(2):117-22. DOI: 10.1007/BF00291047. View

15.

Zakian V . Structure and function of telomeres. Annu Rev Genet. 1989; 23:579-604. DOI: 10.1146/annurev.ge.23.120189.003051. View

16.

Cooley L, Kelley R, Spradling A . Insertional mutagenesis of the Drosophila genome with single P elements. Science. 1988; 239(4844):1121-8. DOI: 10.1126/science.2830671. View

17.

Roiha H, Rubin G, OHare K . P element insertions and rearrangements at the singed locus of Drosophila melanogaster. Genetics. 1988; 119(1):75-83. PMC: 1203347. DOI: 10.1093/genetics/119.1.75. View

18.

Hawley R, Steuber R, Marcus C, Sohn R, Baronas D, CAMERON M . Molecular analysis of an unstable P element insertion at the singed locus of Drosophila melanogaster: evidence for intracistronic transposition of a P element. Genetics. 1988; 119(1):85-94. PMC: 1203348. DOI: 10.1093/genetics/119.1.85. View

19.

Biessmann H, Mason J . Progressive loss of DNA sequences from terminal chromosome deficiencies in Drosophila melanogaster. EMBO J. 1988; 7(4):1081-6. PMC: 454439. DOI: 10.1002/j.1460-2075.1988.tb02916.x. View

20.

Levis R, HAZELRIGG T, Rubin G . Effects of genomic position on the expression of transduced copies of the white gene of Drosophila. Science. 1985; 229(4713):558-61. DOI: 10.1126/science.2992080. View