Skip to main content
PMC home page
Genetics logoLink to Genetics
. 2002 Feb;160(2):509–517. doi: 10.1093/genetics/160.2.509

Cytogenetic analysis of the third chromosome heterochromatin of Drosophila melanogaster.

Dmitry E Koryakov 1, Igor F Zhimulev 1, Patrizio Dimitri 1
PMCID: PMC1461961  PMID: 11861557

Abstract

Previous cytological analysis of heterochromatic rearrangements has yielded significant insight into the location and genetic organization of genes mapping to the heterochromatin of chromosomes X, Y, and 2 of Drosophila melanogaster. These studies have greatly facilitated our understanding of the genetic organization of heterochromatic genes. In contrast, the 12 essential genes known to exist within the mitotic heterochromatin of chromosome 3 have remained only imprecisely mapped. As a further step toward establishing a complete map of the heterochomatic genetic functions in Drosophila, we have characterized several rearrangements of chromosome 3 by using banding techniques at the level of mitotic chromosome. Most of the rearrangement breakpoints were located in the dull fluorescent regions h49, h51, and h58, suggesting that these regions correspond to heterochromatic hotspots for rearrangements. We were able to construct a detailed cytogenetic map of chromosome 3 heterochromatin that includes all of the known vital genes. At least 7 genes of the left arm (from l(3)80Fd to l(3)80Fj) map to segment h49-h51, while the most distal genes (from l(3)80Fa to l(3)80Fc) lie within the h47-h49 portion. The two right arm essential genes, l(3)81Fa and l(3)81Fb, are both located within the distal h58 segment. Intriguingly, a major part of chromosome 3 heterochromatin was found to be "empty," in that it did not contain either known genes or known satellite DNAs.

Full Text

The Full Text of this article is available as a PDF (294.1 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abad J. P., Agudo M., Molina I., Losada A., Ripoll P., Villasante A. Pericentromeric regions containing 1.688 satellite DNA sequences show anti-kinetochore antibody staining in prometaphase chromosomes of Drosophila melanogaster. Mol Gen Genet. 2000 Nov;264(4):371–377. doi: 10.1007/s004380000331. [DOI] [PubMed] [Google Scholar]
  2. Abad J. P., Carmena M., Baars S., Saunders R. D., Glover D. M., Ludeña P., Sentis C., Tyler-Smith C., Villasante A. Dodeca satellite: a conserved G+C-rich satellite from the centromeric heterochromatin of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1992 May 15;89(10):4663–4667. doi: 10.1073/pnas.89.10.4663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Adams M. D., Celniker S. E., Holt R. A., Evans C. A., Gocayne J. D., Amanatides P. G., Scherer S. E., Li P. W., Hoskins R. A., Galle R. F. The genome sequence of Drosophila melanogaster. Science. 2000 Mar 24;287(5461):2185–2195. doi: 10.1126/science.287.5461.2185. [DOI] [PubMed] [Google Scholar]
  4. Ashburner M., Misra S., Roote J., Lewis S. E., Blazej R., Davis T., Doyle C., Galle R., George R., Harris N. An exploration of the sequence of a 2.9-Mb region of the genome of Drosophila melanogaster: the Adh region. Genetics. 1999 Sep;153(1):179–219. doi: 10.1093/genetics/153.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Biggs W. H., 3rd, Zavitz K. H., Dickson B., van der Straten A., Brunner D., Hafen E., Zipursky S. L. The Drosophila rolled locus encodes a MAP kinase required in the sevenless signal transduction pathway. EMBO J. 1994 Apr 1;13(7):1628–1635. doi: 10.1002/j.1460-2075.1994.tb06426.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carmena M., González C. Transposable elements map in a conserved pattern of distribution extending from beta-heterochromatin to centromeres in Drosophila melanogaster. Chromosoma. 1995 Jul;103(10):676–684. doi: 10.1007/BF00344228. [DOI] [PubMed] [Google Scholar]
  7. Carvalho A. B., Lazzaro B. P., Clark A. G. Y chromosomal fertility factors kl-2 and kl-3 of Drosophila melanogaster encode dynein heavy chain polypeptides. Proc Natl Acad Sci U S A. 2000 Nov 21;97(24):13239–13244. doi: 10.1073/pnas.230438397. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Devlin R. H., Bingham B., Wakimoto B. T. The organization and expression of the light gene, a heterochromatic gene of Drosophila melanogaster. Genetics. 1990 May;125(1):129–140. doi: 10.1093/genetics/125.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dimitri P. Constitutive heterochromatin and transposable elements in Drosophila melanogaster. Genetica. 1997;100(1-3):85–93. [PubMed] [Google Scholar]
  10. Dimitri P. Cytogenetic analysis of the second chromosome heterochromatin of Drosophila melanogaster. Genetics. 1991 Mar;127(3):553–564. doi: 10.1093/genetics/127.3.553. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Eisen A., Sattah M., Gazitt T., Neal K., Szauter P., Lucchesi J. A novel DEAD-box RNA helicase exhibits high sequence conservation from yeast to humans. Biochim Biophys Acta. 1998 Apr 29;1397(2):131–136. doi: 10.1016/s0167-4781(97)00213-3. [DOI] [PubMed] [Google Scholar]
  12. Elgin S. C. Heterochromatin and gene regulation in Drosophila. Curr Opin Genet Dev. 1996 Apr;6(2):193–202. doi: 10.1016/s0959-437x(96)80050-5. [DOI] [PubMed] [Google Scholar]
  13. Gatti M., Bonaccorsi S., Pimpinelli S. Looking at Drosophila mitotic chromosomes. Methods Cell Biol. 1994;44:371–391. doi: 10.1016/s0091-679x(08)60924-3. [DOI] [PubMed] [Google Scholar]
  14. Gatti M., Pimpinelli S. Functional elements in Drosophila melanogaster heterochromatin. Annu Rev Genet. 1992;26:239–275. doi: 10.1146/annurev.ge.26.120192.001323. [DOI] [PubMed] [Google Scholar]
  15. Gatti M., Pimpinelli S., Santini G. Characterization of Drosophila heterochromatin. I. Staining and decondensation with Hoechst 33258 and quinacrine. Chromosoma. 1976 Sep 24;57(4):351–375. doi: 10.1007/BF00332160. [DOI] [PubMed] [Google Scholar]
  16. Gepner J., Hays T. S. A fertility region on the Y chromosome of Drosophila melanogaster encodes a dynein microtubule motor. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11132–11136. doi: 10.1073/pnas.90.23.11132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hanai S., Uchida M., Kobayashi S., Miwa M., Uchida K. Genomic organization of Drosophila poly(ADP-ribose) polymerase and distribution of its mRNA during development. J Biol Chem. 1998 May 8;273(19):11881–11886. doi: 10.1074/jbc.273.19.11881. [DOI] [PubMed] [Google Scholar]
  18. Hilliker A. J., Appels R., Schalet A. The genetic analysis of D. melanogaster heterochromatin. Cell. 1980 Oct;21(3):607–619. doi: 10.1016/0092-8674(80)90424-9. [DOI] [PubMed] [Google Scholar]
  19. Howe M., Dimitri P., Berloco M., Wakimoto B. T. Cis-effects of heterochromatin on heterochromatic and euchromatic gene activity in Drosophila melanogaster. Genetics. 1995 Jul;140(3):1033–1045. doi: 10.1093/genetics/140.3.1033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kay M. A., Zhang J. Y., Jacobs-Lorena M. Identification and germline transformation of the ribosomal protein rp21 gene of Drosophila: complementation analysis with the Minute QIII locus reveals nonidentity. Mol Gen Genet. 1988 Aug;213(2-3):354–358. doi: 10.1007/BF00339602. [DOI] [PubMed] [Google Scholar]
  21. Kelly L. E., Phillips A. M., Delbridge M., Stewart R. Identification of a gene family from Drosophila melanogaster encoding proteins with homology to invertebrate sarcoplasmic calcium-binding proteins (SCPS). Insect Biochem Mol Biol. 1997 Aug-Sep;27(8-9):783–792. doi: 10.1016/s0965-1748(97)00062-3. [DOI] [PubMed] [Google Scholar]
  22. Kozlova T., Zhimulev I. F., Kafatos F. C. Molecular organization of an individual Drosophila polytene chromomere: transcribed sequences in the 10A1-2 band. Mol Gen Genet. 1997 Dec;257(1):55–61. doi: 10.1007/s004380050623. [DOI] [PubMed] [Google Scholar]
  23. Kurek R., Reugels A. M., Lammermann U., Bünemann H. Molecular aspects of intron evolution in dynein encoding mega-genes on the heterochromatic Y chromosome of Drosophila sp. Genetica. 2000;109(1-2):113–123. doi: 10.1023/a:1026552604229. [DOI] [PubMed] [Google Scholar]
  24. Lohe A. R., Hilliker A. J., Roberts P. A. Mapping simple repeated DNA sequences in heterochromatin of Drosophila melanogaster. Genetics. 1993 Aug;134(4):1149–1174. doi: 10.1093/genetics/134.4.1149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Losada A., Agudo M., Abad J. P., Villasante A. HeT-A telomere-specific retrotransposons in the centric heterochromatin of Drosophila melanogaster chromosome 3. Mol Gen Genet. 1999 Dec;262(4-5):618–622. doi: 10.1007/s004380051124. [DOI] [PubMed] [Google Scholar]
  26. Marchant G. E., Holm D. G. Genetic analysis of the heterochromatin of chromosome 3 in Drosophila melanogaster. I. Products of compound-autosome detachment. Genetics. 1988 Oct;120(2):503–517. doi: 10.1093/genetics/120.2.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. McKee B., Lindsley D. L. Inseparability of X-Heterochromatic Functions Responsible for X:Y Pairing, Meiotic Drive, and Male Fertility in Drosophila melanogaster. Genetics. 1987 Jul;116(3):399–407. doi: 10.1093/genetics/116.3.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Nichols R., Schneuwly S. A., Dixon J. E. Identification and characterization of a Drosophila homologue to the vertebrate neuropeptide cholecystokinin. J Biol Chem. 1988 Sep 5;263(25):12167–12170. [PubMed] [Google Scholar]
  29. Nurminsky D. I., Shevelyov YYa, Nuzhdin S. V., Gvozdev V. A. Structure, molecular evolution and maintenance of copy number of extended repeated structures in the X-heterochromatin of Drosophila melanogaster. Chromosoma. 1994 Jul;103(4):277–285. doi: 10.1007/BF00352252. [DOI] [PubMed] [Google Scholar]
  30. Oda H., Uemura T., Shiomi K., Nagafuchi A., Tsukita S., Takeichi M. Identification of a Drosophila homologue of alpha-catenin and its association with the armadillo protein. J Cell Biol. 1993 Jun;121(5):1133–1140. doi: 10.1083/jcb.121.5.1133. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Palumbo G., Berloco M., Fanti L., Bozzetti M. P., Massari S., Caizzi R., Caggese C., Spinelli L., Pimpinelli S. Interaction systems between heterochromatin and euchromatin in Drosophila melanogaster. Genetica. 1994;94(2-3):267–274. doi: 10.1007/BF01443440. [DOI] [PubMed] [Google Scholar]
  32. Parks S., Wieschaus E. The Drosophila gastrulation gene concertina encodes a G alpha-like protein. Cell. 1991 Jan 25;64(2):447–458. doi: 10.1016/0092-8674(91)90652-f. [DOI] [PubMed] [Google Scholar]
  33. Pimpinelli S., Berloco M., Fanti L., Dimitri P., Bonaccorsi S., Marchetti E., Caizzi R., Caggese C., Gatti M. Transposable elements are stable structural components of Drosophila melanogaster heterochromatin. Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3804–3808. doi: 10.1073/pnas.92.9.3804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Pimpinelli S., Dimitri P. Cytogenetic analysis of segregation distortion in Drosophila melanogaster: the cytological organization of the Responder (Rsp) locus. Genetics. 1989 Apr;121(4):765–772. doi: 10.1093/genetics/121.4.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Pimpinelli S., Gatti M., De Marco A. Evidence for heterogeneity in heterochromatin of Drosophila melanogaster. Nature. 1975 Jul 24;256(5515):335–337. doi: 10.1038/256335a0. [DOI] [PubMed] [Google Scholar]
  36. 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. doi: 10.1093/genetics/109.4.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. RITOSSA F. M., SPIEGELMAN S. LOCALIZATION OF DNA COMPLEMENTARY TO RIBOSOMAL RNA IN THE NUCLEOLUS ORGANIZER REGION OF DROSOPHILA MELANOGASTER. Proc Natl Acad Sci U S A. 1965 Apr;53:737–745. doi: 10.1073/pnas.53.4.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Rasooly R. S., Robbins L. G. Rex and a suppressor of Rex are repeated neomorphic loci in the Drosophila melanogaster ribosomal DNA. Genetics. 1991 Sep;129(1):119–132. doi: 10.1093/genetics/129.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Rollins R. A., Morcillo P., Dorsett D. Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes. Genetics. 1999 Jun;152(2):577–593. doi: 10.1093/genetics/152.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Sawamura K., Yamamoto M. T. Cytogenetical localization of Zygotic hybrid rescue (Zhr), a Drosophila melanogaster gene that rescues interspecific hybrids from embryonic lethality. Mol Gen Genet. 1993 Jun;239(3):441–449. doi: 10.1007/BF00276943. [DOI] [PubMed] [Google Scholar]
  41. Schulze S., Sinclair D. A., Silva E., Fitzpatrick K. A., Singh M., Lloyd V. K., Morin K. A., Kim J., Holm D. G., Kennison J. A. Essential genes in proximal 3L heterochromatin of Drosophila melanogaster. Mol Gen Genet. 2001 Feb;264(6):782–789. doi: 10.1007/s004380000367. [DOI] [PubMed] [Google Scholar]
  42. Sinclair D. A., Suzuki D. T., Grigliatti T. A. Genetic and developmental analysis of a temperature-sensitive minute mutation of Drosophila melanogaster. Genetics. 1981 Mar-Apr;97(3-4):581–606. doi: 10.1093/genetics/97.3-4.581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Tulin A. V., Kogan G. L., Filipp D., Balakireva M. D., Gvozdev V. A. Heterochromatic Stellate gene cluster in Drosophila melanogaster: structure and molecular evolution. Genetics. 1997 May;146(1):253–262. doi: 10.1093/genetics/146.1.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wallrath L. L. Unfolding the mysteries of heterochromatin. Curr Opin Genet Dev. 1998 Apr;8(2):147–153. doi: 10.1016/s0959-437x(98)80135-4. [DOI] [PubMed] [Google Scholar]
  45. Zhimulev I. F. Polytene chromosomes, heterochromatin, and position effect variegation. Adv Genet. 1998;37:1–566. doi: 10.1016/s0065-2660(08)60341-7. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES