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Genetics. Oct 1988; 120(2): 519–532.
PMCID: PMC1203529

Genetic Analysis of the Heterochromatin of Chromosome 3 in Drosophila Melanogaster. II. Vital Loci Identified through Ems Mutagenesis


Chromosome 3 of Drosophila melanogaster contains the last major blocks of heterochromatin in this species to be genetically analyzed. Deficiencies of heterochromatin generated through the detachment of compound-3 chromosomes revealed the presence of vital loci in the heterochromatin of chromosome 3, but an extensive complementation analysis with various combinations of lethal and nonlethal detachment products gave no evidence of tandemly repeated vital genes in this region. These findings indicate that the heterochromatin of chromosome 3 is genetically similar to that of chromosome 2. A more thorough genetic analysis of the heterochromatic regions has been carried out using the chemical mutagen ethyl methanesulfonate (EMS). Seventy-five EMS-induced lethals allelic to loci uncovered by detachment-product deficiencies were recovered and tested for complementation. In total, 12 complementation groups were identified, ten in the heterochromatin to the left of the centromere and two to the right. All but two complementation groups in the left heterochromatic block could be identified as separate loci through deficiency mapping. The interallelic complementation observed between some EMS-induced lethals, as well as the recovery of a temperature-sensitive allele for each of the two loci, provided further evidence that single-copy, transcribed vital genes reside in the heterochromatin of chromosome 3. Cytological analysis of three detachment-product deficiencies provided evidence that at least some of the genes uncovered in this study are located in the most distal segments of the heterochromatin in both arms. This study provides a detailed genetic analysis of chromosome 3 heterochromatin and offers further information on the genetic nature and heterogeneity of Drosophila heterochromatin.

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Selected References

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  • Appels R, Hilliker AJ. The cytogenetic boundaries of the rDNA region within heterochromatin in the X chromosome of Drosophila melanogaster and their relation to male meiotic pairing sites. Genet Res. 1982 Apr;39(2):149–156. [PubMed]
  • Appels R, Peacock WJ. The arrangement and evolution of highly repeated (satellite) DNA sequences with special reference to Drosophila. Int Rev Cytol Suppl. 1978;Suppl 8:69–126. [PubMed]
  • Arrighi FE, Hsu TC, Pathak S, Sawada H. The sex chromosomes of the Chinese hamster: constitutive heterochromatin deficient in repetitive DNA sequences. Cytogenet Cell Genet. 1974;13(3):268–274. [PubMed]
  • Biessmann H, Kuger P, Schröpfer C, Spindler E. Molecular cloning and preliminary characterization of a Drosophila melanogaster gene from a region adjacent to the centromeric beta-heterochromatin. Chromosoma. 1981;82(4):493–503. [PubMed]
  • Bishop JB, Lee WR. Chromosome breakage in Drosophila melanogaster induced by a monofunctional alkylating agent (EMS). Mutat Res. 1973 Dec;21(6):327–333. [PubMed]
  • Cantú ES, Gay H. Localization of chromosomal DNA sequences homologous to ribosomal gene type I insertion DNA in Drosophila melanogaster. Mol Gen Genet. 1984;196(2):345–349. [PubMed]
  • Cooper JE. Chromosomes and DNA of Microtus. III. Heterochromatin rearrangements in M. agrestis bone marrow clones. Chromosoma. 1977 Jul 8;62(3):269–278. [PubMed]
  • Cordeiro M, Wheeler L, Lee CS, Kastritsis CD, Richardson RH. Heterochromatic chromosomes and satellite DNAs of Drosophila nasutoides. Chromosoma. 1975;51(1):65–73. [PubMed]
  • Craig-Holmes AP, Moore FB, Shaw MW. Polymporphism of human C-band heterochromatin. II. Family studies with suggestive evidence for somatic crossing over. Am J Hum Genet. 1975 Mar;27(2):178–189. [PMC free article] [PubMed]
  • Dawid IB, Long EO, DiNocera PP, Pardue ML. Ribosomal insertion-like elements in Drosophila melanogaster are interspersed with mobile sequences. Cell. 1981 Aug;25(2):399–408. [PubMed]
  • Flamm WG, Walker PM, McCallum M. Some properties of the single strands isolated from the DNA of the nuclear satellite of the mouse (Mus musculus). J Mol Biol. 1969 Mar 28;40(3):423–443. [PubMed]
  • Gall JG, Atherton DD. Satellite DNA sequences in Drosophila virilis. J Mol Biol. 1974 Jan 5;85(4):633–664. [PubMed]
  • Halfer C. Karyotypic evolution in an originally XY cell line of Drosophila melanogaster: a case of heterochromatin increase in vitro. Chromosoma. 1978 Aug 28;68(2):149–163. [PubMed]
  • Halfer C. Interstrain heterochromatin polymorphisms in Drosophila melanogaster. Chromosoma. 1981;84(2):195–206. [PubMed]
  • Hennig W. Highly repetitive DNA sequences in the genome of Drosophila hydei. I. Preferential localization in the X chromosomal heterochromatin. J Mol Biol. 1972 Nov 14;71(2):407–417. [PubMed]
  • Hilliker AJ. Genetic analysis of the centromeric heterochromatin of chromosome 2 of Drosophila melanogaster: deficiency mapping of EMS-induced lethal complementation groups. Genetics. 1976 Aug;83(4):765–782. [PMC free article] [PubMed]
  • Hilliker AJ, Appels R. Pleiotropic effects associated with the deletion of heterochromatin surrounding rDNA on the X chromosome of Drosophila. Chromosoma. 1982;86(4):469–490. [PubMed]
  • Hilliker AJ, Appels R, Schalet A. The genetic analysis of D. melanogaster heterochromatin. Cell. 1980 Oct;21(3):607–619. [PubMed]
  • Holmquist G. Organisation and evolution of Drosophila virilis heterochromatin. Nature. 1975 Oct 9;257(5526):503–506. [PubMed]
  • Hsieh T, Brutlag D. Sequence and sequence variation within the 1.688 g/cm3 satellite DNA of Drosophila melanogaster. J Mol Biol. 1979 Dec 5;135(2):465–481. [PubMed]
  • Hsu TC. Heterochromatin pattern in metaphase chromosomes of Drosophila melanogaster. J Hered. 1971 Sep-Oct;62(5):285–287. [PubMed]
  • Jockusch H. Relations between temperature sensitivity, amino acid replacements, and quaternary structure of mutant proteins. Biochem Biophys Res Commun. 1966 Aug 23;24(4):577–583. [PubMed]
  • Kuo MT, Hsu TC. Studies in heterochromatin DNA: characterization of transcripts synthesized in situ from C-banded preparations. Chromosoma. 1978 Feb 24;65(4):325–334. [PubMed]
  • Kurnit DM. Satellite DNA and heterochromatin variants: the case for unequal mitotic crossing over. Hum Genet. 1979 Mar 12;47(2):169–186. [PubMed]
  • Lakhotia SC, Jacob J. EM autoradiographic studies on polytene nuclei of Drosophila melanogaster. II. Organization and transcriptive activity of the chromocentre. Exp Cell Res. 1974 Jun;86(2):253–263. [PubMed]
  • Lefevre G, Watkins W. The question of the total gene number in Drosophila melanogaster. Genetics. 1986 Aug;113(4):869–895. [PMC free article] [PubMed]
  • Levinger L, Varshavsky A. Protein D1 preferentially binds A + T-rich DNA in vitro and is a component of Drosophila melanogaster nucleosomes containing A + T-rich satellite DNA. Proc Natl Acad Sci U S A. 1982 Dec;79(23):7152–7156. [PMC free article] [PubMed]
  • Lifschytz E. Fine-Structure Analysis and Genetic Organization at the Base of the X Chromosome in DROSOPHILA MELANOGASTER. Genetics. 1978 Mar;88(3):457–467. [PMC free article] [PubMed]
  • Lifschytz E, Hareven D. Heterochromatin markers: a search for heterochromatin specific middle repetitive sequences in Drosophila. Chromosoma. 1982;86(4):429–442. [PubMed]
  • Lim JK, Snyder LA. Cytogenetic and complementation analyses of recessive lethal mutations induced in the X chromosome of Drosophila by three alkylating agents. Genet Res. 1974 Aug;24(1):1–10. [PubMed]
  • Lis JT, Ish-Horowicz D, Pinchin SM. Genomic organization and transcription of the alpha beta heat shock DNA in Drosophila melanogaster. Nucleic Acids Res. 1981 Oct 24;9(20):5297–5310. [PMC free article] [PubMed]
  • Meneely PM, Herman RK. Lethals, steriles and deficiencies in a region of the X chromosome of Caenorhabditis elegans. Genetics. 1979 May;92(1):99–115. [PMC free article] [PubMed]
  • Miklos GL, Gill AC. The DNA sequences of cloned complex satellite DNAs from Hawaiian Drosophila and their bearing on satellite DNA sequence conservation. Chromosoma. 1981;82(3):409–427. [PubMed]
  • Mukherjee T, Lakhotia SC. 3H-uridine incorporation in the puff 93D and in chromocentric heterochromatin of heat shocked salivary glands of Drosophila melanogaster. Chromosoma. 1979 Sep 1;74(1):75–82. [PubMed]
  • Peacock WJ, Brutlag D, Goldring E, Appels R, Hinton CW, Lindsley DL. The organization of highly repeated DNA sequences in Drosophila melanogaster chromosomes. Cold Spring Harb Symp Quant Biol. 1974;38:405–416. [PubMed]
  • Peacock WJ, Appels R, Endow S, Glover D. Chromosomal distribution of the major insert in Drosophila melanogaster 28S rRNA genes. Genet Res. 1981 Apr;37(2):209–214. [PubMed]
  • Pimpinelli S, Gatti M, De Marco A. Evidence for heterogeneity in heterochromatin of Drosophila melanogaster. Nature. 1975 Jul 24;256(5515):335–337. [PubMed]
  • Pimpinelli S, Sullivan W, Prout M, Sandler L. On biological functions mapping to the heterochromatin of Drosophila melanogaster. Genetics. 1985 Apr;109(4):701–724. [PMC free article] [PubMed]
  • Southern EM. Base sequence and evolution of guinea-pig alpha-satellite DNA. Nature. 1970 Aug 22;227(5260):794–798. [PubMed]
  • Spradling AC, Rubin GM. Drosophila genome organization: conserved and dynamic aspects. Annu Rev Genet. 1981;15:219–264. [PubMed]
  • Spradling A, Penman S, Pardue ML. Analysis of drosophila mRNA by in situ hybridization: sequences transcribed in normal and heat shocked cultured cells. Cell. 1975 Apr;4(4):395–404. [PubMed]
  • Strauss F, Varshavsky A. A protein binds to a satellite DNA repeat at three specific sites that would be brought into mutual proximity by DNA folding in the nucleosome. Cell. 1984 Jul;37(3):889–901. [PubMed]
  • Suzuki DT. Temperature-sensitive mutations in Drosophila melanogaster. Science. 1970 Nov 13;170(3959):695–706. [PubMed]
  • Sved JA, Verlin D. Similarity of centromeric heterochromatin in strains of drosophila melanogaster which interact to produce hybrid dysgenesis. Chromosoma. 1980;78(3):353–363. [PubMed]
  • Wheeler LL, Arrighi F, Cordeiro-Stone M, Lee CS. Localization of Drosophila nasutoides satellite DNAs in metaphase chromosomes. Chromosoma. 1978 Dec 21;70(1):41–50. [PubMed]
  • Williamson JH. Ethyl methanesulfonate-induced mutants in the Y chromosome of Drosophila melanogaster. Mutat Res. 1970 Dec;10(6):597–605. [PubMed]
  • Wollenzien P, Barsanti P, Hearst JE. Location and underreplication of satellite DNA in Drosophila melanogaster. Genetics. 1977 Sep;87(1):51–65. [PMC free article] [PubMed]
  • Woodcock DM, Sibatani A. Differential variations in the DNA of Drosophila melanogaster during development. Chromosoma. 1975;50(2):147–183. [PubMed]
  • Wright TR. The genetics of embryogenesis in Drosophila. Adv Genet. 1970;15:261–395. [PubMed]

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