Genetic studies on heterochromatin in Drosophila melanogaster and their implications for the functions of satellite DNA

Abstract

In Drosophila melanogaster the centromeric heterochromatin of all chromosomes consists almost entirely of several different satellite DNA sequences. In view of this we have examined by genetic means the meiotic consequences of X chromosomes with partial deletions of their heterochromatin, and have found that the amount and position of recombination on each heterochromatically deleted X is substantially different from that of a normal X. It appears that the amount of heterochromatin is important in modifying the "centromere effect" on recombination.--In all the deleted Xs tested, chromosome segregation is not appreciably altered from that of a nondeleted control chromosome. Thus satellite DNA does not appear to be an important factor in determining the regular segregation of sex chromosomes in Drosophila. Additionally, since X chromosomes with massive satellite DNA deficiencies are able to participate in a chromocenter within salivary gland nuclei, a major role of satellite DNA in chromocenter formation in this tissue is also quite unlikely.--In order to examine the mechanisms by which the amount of satellite DNA is increased or decreased in vivo, we have measured cytologically the frequency of spontaneous sister chromatid exchanges in a ring Y chromosome which is entirely heterochromatic and consists almost exclusively of satellite DNA. In larval neuroblast cells the frequency of spontaneous SCE in this Y is approximately 0.3% per cell division. Since there is no meiotic recombination in D. melanogaster males and since meiotic recombination in the female does not occur in heterochromatin, our results provide a minimum estimate of the in vivo frequency of SCE in C-banded heterochromatin (which is predominantly simple sequence DNA), without the usual complications of substituted base analogs, incorporated radioactive label or substantial genetic content.--We emphasise that: (a) satellite DNA is not implicated in any major way in recognition processes such as meiotic homologue recognition or chromocenter formation in salivaries, (b) there is likely to be continuous variation in the amount of satellite DNA between individuals of a species; and (c) the amount of satellite DNA can have a crucial functional role in the meiotic recombination system.

Heterozygous Insertions Alter Crossover Distribution but Allow Crossover Interference in Caenorhabditis elegans

“…Repetitive sequences cause formation of heterochromatin, which might spread to nearby regions and be a source of reduced crossovers in paired DNA (Yamamoto and Miklos 1978;Wu and Lichten 1994;Kagawa et al 2002). To test this possibility, we introgressed the oxIs12 insertion into the Hawaiian background, which allowed us to measure crossover frequency in the oxIs12 homozygous state.…”

Physical and Genetic Mapping of the Human X Chromosome Centromere: Repression of Recombination

“…This repression of recombination persists in Drosophila when adjacent heterochromatin is deleted (Yamamoto and Miklos 1978) and is generated de novo in yeast when a centromere is integrated into a new site on the chromosome (Nakaseko et al 1986). In humans, chiasmata are found infrequently near chromosome centromeres (Hulten 1974;Hulten et al 1982), but definitive studies of recombination rates across measured physical distances at human centromeres have only become available recently.…”

“…Some of this repression of exchange is caused by the large blocks of heterochromatin present at the centromeres of higher eukaryotes (Willard 1990;Murphy and Karpen 1995), because heterochromatin, at least in Drosophila, is a poor substrate for recombination regardless of chromosomal location (Baker 1958). Because deletions of centric heterochromatin result in lowered levels of meiotic exchange in centromere-adjacent euchromatin (Yamamoto and Miklos 1978), the presence alone of heterochromatin at Drosophila centromeres does not fully explain the centromere effect. Rather, the centromere seems to exert a suppression of recombination that spreads to adjacent DNA.…”

Why Is the Centromere So Cold?

“…However, evidence indicating that influences other than heterochromatinization may be involved has come from study of the budding yeast, in which a cloned centromere, although lacking any visible form of heterochromatin, shows decreased recombination when it is artificially integrated into new sites in the genome (Lambie and Roeder 1986). Further evidence has come from observation of the persistence of recombination suppression of centromereadjacent euchromatin in Drosophila even when centromeric heterochromatin is deleted (Yamamoto and Miklos 1977).…”