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Cold Spring Harb Symp Quant Biol 42 Pt 2: 1137-46 (1978)[78237819]

DNA sequence organization in Drosophila heterochromatin.

D. Brutlag, M. Carlson, K. Fry & T. S. Hsieh

Drosophila melanogaster is an ideal organism for the study of the structure and function of heterochromatin because it has only four chromosomes and 25% of its genome is heterochromatic. All of the heterochromatin is constitutive and much of it is located in the sex chromosomes, which have been well characterized genetically and cytogenetically (Cooper 1959; Ashburner and Novitski 1976). The study of Drosophila heterochromatin is also attractive at the molecular level since the bulk of the DNA of these regions can be isolated as several discrete satellite DNAs in CsCI equilibrium gradients (Peacock et al. 1974; Endow et al. 1975; Brutlag at al. 1977a). These unusual DNAS consist of short nucleotide sequences (5878 base pain [bp] repeated in tandem arrays over 1,000,000 bp long (Goldring at 83.1975; Brutlag et al., 1977a).

The biological roles of satellite DNA and heterochromatin have long been controversial. The molecular properties of satellite DNA make it unlikely that it is involved in transcription or the normal regulation of genetic expression. The misconception that satellite DNA has no essential function is based on the lack of genes in heterochromatin and on the viability of individuals with large heterochromatic deletions. However, individual Drosophila males carrying deletions of heterochromatin have abnormal meiosis, defective spermatogenesis, and a markedly reduced fertility (Gershenson 1983; Sandler and Braver 1958; Peacock et al. 1975). These germ-line aberrations are directly correlated with the failure of deficient X chromosomes to pair properly during meiosis. Recent evidence shows that females carrying heterochromatic deletions also have a defective meiotic mechanism resulting in a reduced level of recombination (Yamamoto and Miklos 1977). These results indicate a strong selective pressure against chromosomes carrying heterochromatic deletions. They also argue strongly for a role of heterochromatin in the germ line rather than in somatic cells. Heterochromatin, therefore, may be dispensable for the survival of a cell or an individual, but it is essential for the survival of a chromosome in the germ line. A germ-line function is also consistent with the large variations of heterochromatin and satellite DNA between closely related species (Hennig and Walker 1970; Sutton and McCallum 1972; Gall at al. 1974). Indeed, the necessity for proper meiotic pairing of heterochromatin for successful gametogenesis or recombination suggests that variations in satellite DNA could lead to speciation.

To begin an analysis of these meiotic functions at the molecular level, we have studied the organization of the satellite DNA sequences that compose the bulk of the heterochromatin of D. melanogaster. We describe here the properties of two simple-sequence satellites (1.705 and 1.672 g/cm3) and of a complex satellite (1.688 g/cm3) which has been located primarily in the regions of the X and Y chromosomes essential for proper meiotic pairing (Gershenson 1940; Peacock et al., this volume).

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