Mapping Simple Repeated DNA Sequences in Heterochromatin of Drosophila melanogaster

INVESTIGATIONS

Mapping Simple Repeated DNA Sequences in Heterochromatin of Drosophila melanogaster

A. R. Lohe, A. J. Hilliker and P. A. Roberts
Department of Genetics, Washington University School of Medicine, St. Louis, Missouri 63110 Present address: Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge, Massachusetts 02138.

Heterochromatin in Drosophila has unusual genetic, cytological and molecular properties. Highly repeated DNA sequences (satellites) are the principal component of heterochromatin. Using probes from cloned satellites, we have constructed a chromosome map of 10 highly repeated, simple DNA sequences in heterochromatin of mitotic chromosomes of Drosophila melanogaster. Despite extensive sequence homology among some satellites, chromosomal locations could be distinguished by stringent in situ hybridizations for each satellite. Only two of the localizations previously determined using gradient-purified bulk satellite probes are correct. Eight new satellite localizations are presented, providing a megabase-level chromosome map of one-quarter of the genome. Five major satellites each exhibit a multichromosome distribution, and five minor satellites hybridize to single sites on the Y chromosome. Satellites closely related in sequence are often located near one another on the same chromosome. About 80% of Y chromosome DNA is composed of nine simple repeated sequences, in particular (AAGAC)(n) (8 Mb), (AAGAG)(n) (7 Mb) and (AATAT)(n) (6 Mb). Similarly, more than 70% of the DNA in chromosome 2 heterochromatin is composed of five simple repeated sequences. We have also generated a high resolution map of satellites in chromosome 2 heterochromatin, using a series of translocation chromosomes whose breakpoints in heterochromatin were ordered by N-banding. Finally, staining and banding patterns of heterochromatic regions are correlated with the locations of specific repeated DNA sequences. The basis for the cytochemical heterogeneity in banding appears to depend exclusively on the different satellite DNAs present in heterochromatin.

This article has been cited by other articles:

R. Piergentili and C. Mencarelli
Drosophila melanogaster kl-3 and kl-5 Y-loops harbor triple-stranded nucleic acids
J. Cell Sci., May 15, 2008; 121(10): 1605 - 1612.
[Abstract] [Full Text] [PDF]

A.-S. Fiston-Lavier, D. Anxolabehere, and H. Quesneville
A model of segmental duplication formation in Drosophila melanogaster
Genome Res., October 1, 2007; 17(10): 1458 - 1470.
[Abstract] [Full Text] [PDF]

E. N. Andreyeva, T. D. Kolesnikova, O. V. Demakova, M. Mendez-Lago, G. V. Pokholkova, E. S. Belyaeva, F. Rossi, P. Dimitri, A. Villasante, and I. F. Zhimulev
High-resolution analysis of Drosophila heterochromatin organization using SuUR Su(var)3-9 double mutants
PNAS, July 31, 2007; 104(31): 12819 - 12824.
[Abstract] [Full Text] [PDF]

L. Usakin, J. Abad, V. V. Vagin, B. de Pablos, A. Villasante, and V. A. Gvozdev
Transcription of the 1.688 Satellite DNA Family Is Under the Control of RNA Interference Machinery in Drosophila melanogaster Ovaries
Genetics, June 1, 2007; 176(2): 1343 - 1349.
[Abstract] [Full Text] [PDF]

Y. Xiang and R. S. Hawley
The Mechanism of Secondary Nondisjunction in Drosophila melanogaster Females
Genetics, September 1, 2006; 174(1): 67 - 78.
[Abstract] [Full Text] [PDF]

M. K. Gilbert, Y. Y. Tan, and C. M. Hart
The Drosophila Boundary Element-Associated Factors BEAF-32A and BEAF-32B Affect Chromatin Structure
Genetics, July 1, 2006; 173(3): 1365 - 1375.
[Abstract] [Full Text] [PDF]

D. J. Orengo, M. Papaceit, and E. Juan
A Minisatellite with Fold-Back Structure is Included in the 5'-Flanking Region of the Adh Gene of Scaptodrosophila lebanonensis
J. Hered., January 1, 2004; 95(1): 62 - 69.
[Abstract] [Full Text] [PDF]

B. T. Sage and A. K. Csink
Heterochromatic Self-Association, a Determinant of Nuclear Organization, Does Not Require Sequence Homology in Drosophila
Genetics, November 1, 2003; 165(3): 1183 - 1193.
[Abstract] [Full Text] [PDF]

P. Dimitri, N. Junakovic, and B. Arca
Colonization of Heterochromatic Genes by Transposable Elements in Drosophila
Mol. Biol. Evol., April 1, 2003; 20(4): 503 - 512.
[Abstract] [Full Text] [PDF]

D. E. Koryakov, E. V. Domanitskaya, S. N. Belyakin, and I. F. Zhimulev
Abnormal tissue-dependent polytenization of a block of chromosome 3 pericentric heterochromatin in Drosophila melanogaster
J. Cell Sci., March 15, 2003; 116(6): 1035 - 1044.
[Abstract] [Full Text] [PDF]

X. Sun, H. D. Le, J. M. Wahlstrom, and G. H. Karpen
Sequence Analysis of a Functional Drosophila Centromere
Genome Res., February 1, 2003; 13(2): 182 - 194.
[Abstract] [Full Text] [PDF]

C. M. Yan, K. W. Dobie, H. D. Le, A. Y. Konev, and G. H. Karpen
Efficient Recovery of Centric Heterochromatin P-Element Insertions in Drosophila melanogaster
Genetics, May 1, 2002; 161(1): 217 - 229.
[Abstract] [Full Text] [PDF]

N. Aulner, C. Monod, G. Mandicourt, D. Jullien, O. Cuvier, A. Sall, S. Janssen, U. K. Laemmli, and E. Kas
The AT-Hook Protein D1 Is Essential for Drosophila melanogaster Development and Is Implicated in Position-Effect Variegation
Mol. Cell. Biol., February 15, 2002; 22(4): 1218 - 1232.
[Abstract] [Full Text] [PDF]

D. E. Koryakov, I. F. Zhimulev, and P. Dimitri
Cytogenetic Analysis of the Third Chromosome Heterochromatin of Drosophila melanogaster
Genetics, February 1, 2002; 160(2): 509 - 517.
[Abstract] [Full Text] [PDF]

C. J. B. Rohr, H. Ranson, X. Wang, and N. J. Besansky
Structure and Evolution of mtanga, a Retrotransposon Actively Expressed on the Y Chromosome of the African Malaria Vector Anopheles gambiae
Mol. Biol. Evol., February 1, 2002; 19(2): 149 - 162.
[Abstract] [Full Text] [PDF]

K.-K. Hwang, J. C. Eissenberg, and H. J. Worman
Transcriptional repression of euchromatic genes by Drosophila heterochromatin protein 1 and histone modifiers
PNAS, September 13, 2001; (2001) 211303598.
[Abstract] [Full Text] [PDF]

H. S. Malik and S. Henikoff
Adaptive Evolution of Cid, a Centromere-Specific Histone in Drosophila
Genetics, March 1, 2001; 157(3): 1293 - 1298.
[Abstract] [Full Text]

A. B. Carvalho, B. P. Lazzaro, and A. G. Clark
Y chromosomal fertility factors kl-2 and kl-3 of Drosophila melanogaster encode dynein heavy chain polypeptides
PNAS, November 2, 2000; (2000) 230438397.
[Abstract] [Full Text]

T. Torok, M. Gorjanacz, P. J. Bryant, and I. Kiss
Prod is a novel DNA-binding protein that binds to the 1.686 g/cm3 10 bp satellite repeat of Drosophila melanogaster
Nucleic Acids Res., September 15, 2000; 28(18): 3551 - 3557.
[Abstract] [Full Text] [PDF]

J. Locke, L. Podemski, N. Aippersbach, H. Kemp, and R. Hodgetts
A Physical Map of the Polytenized Region (101EF-102F) of Chromosome 4 in Drosophila melanogaster
Genetics, July 1, 2000; 155(3): 1175 - 1183.
[Abstract] [Full Text]

A. Cortés and F. Azorín
DDP1, a Heterochromatin-Associated Multi-KH-Domain Protein of Drosophila melanogaster, Interacts Specifically with Centromeric Satellite DNA Sequences
Mol. Cell. Biol., June 1, 2000; 20(11): 3860 - 3869.
[Abstract] [Full Text]

B. Timakov and P. Zhang
Genetic Analysis of a Y-Chromosome Region That Induces Triplosterile Phenotypes and Is Essential for Spermatid Individualization in Drosophila melanogaster
Genetics, May 1, 2000; 155(1): 179 - 189.
[Abstract] [Full Text]

E. V. Tolchkov, V. I. Rasheva, S. Bonaccorsi, T. Westphal, and V. A. Gvozdev
The Size and Internal Structure of a Heterochromatic Block Determine Its Ability to Induce Position Effect Variegation in Drosophila melanogaster
Genetics, April 1, 2000; 154(4): 1611 - 1626.
[Abstract] [Full Text]

M. D. Adams, S. E. Celniker, R. A. Holt, C. A. Evans, J. D. Gocayne, P. G. Amanatides, S. E. Scherer, P. W. Li, R. A. Hoskins, R. F. Galle, et al.
The Genome Sequence of Drosophila melanogaster
Science, March 24, 2000; 287(5461): 2185 - 2195.
[Abstract] [Full Text]

J. Locke, L. Podemski, K. Roy, D. Pilgrim, and R. Hodgetts
Analysis of Two Cosmid Clones from Chromosome 4 of Drosophila melanogaster Reveals Two New Genes Amid an Unusual Arrangement of Repeated Sequences
Genome Res., February 1, 1999; 9(2): 137 - 149.
[Abstract] [Full Text]

K. Dej and A. Spradling
The endocycle controls nurse cell polytene chromosome structure during Drosophila oogenesis
Development, January 1, 1999; 126(2): 293 - 303.
[Abstract] [PDF]

Y. S. Rong and K. G. Golic
Dominant Defects in Drosophila Eye Pigmentation Resulting From a Euchromatin-Heterochromatin Fusion Gene
Genetics, December 1, 1998; 150(4): 1551 - 1566.
[Abstract] [Full Text]

A. K. Csink and S. Henikoff
Large-scale Chromosomal Movements During Interphase Progression in Drosophila
J. Cell Biol., October 5, 1998; 143(1): 13 - 22.
[Abstract] [Full Text] [PDF]

E. B. Cambareri, R. Aisner, and J. Carbon
Structure of the Chromosome VII Centromere Region in Neurospora crassa: Degenerate Transposons and Simple Repeats
Mol. Cell. Biol., September 1, 1998; 18(9): 5465 - 5477.
[Abstract] [Full Text]

E. V. Ananiev, R. L. Phillips, and H. W. Rines
Complex Structure of Knob DNA on Maize Chromosome 9: Retrotransposon Invasion into Heterochromatin
Genetics, August 1, 1998; 149(4): 2025 - 2037.
[Abstract] [Full Text] [PDF]

J. C. Fung, W. F. Marshall, A. Dernburg, D. A. Agard, and J. W. Sedat
Homologous Chromosome Pairing in Drosophila melanogaster Proceeds through Multiple Independent Initiations
J. Cell Biol., April 6, 1998; 141(1): 5 - 20.
[Abstract] [Full Text] [PDF]

J. Suso Platero, A. K. Csink, A. Quintanilla, and S. Henikoff
Changes in Chromosomal Localization of Heterochromatin-binding Proteins during the Cell Cycle in Drosophila
J. Cell Biol., March 23, 1998; 140(6): 1297 - 1306.
[Abstract] [Full Text] [PDF]

G. L. Sass and S. Henikoff
Comparative Analysis of Position–Effect Variegation Mutations in Drosophila melanogaster Delineates the Targets of Modifiers
Genetics, February 1, 1998; 148(2): 733 - 742.
[Abstract] [Full Text] [PDF]

T Torok, P D Harvie, M Buratovich, and P J Bryant
The product of proliferation disrupter is concentrated at centromeres and required for mitotic chromosome condensation and cell proliferation in Drosophila.
Genes & Dev., January 15, 1997; 11(2): 213 - 225.
[Abstract] [PDF]

M. Espinas, E. Jimenez-Garcia, A. Martinez-Balbas, and F. Azorin
Formation of Triple-stranded DNA at d(GA·TC)n Sequences Prevents Nucleosome Assembly and Is Hindered by Nucleosomes
J. Biol. Chem., December 13, 1996; 271(50): 31807 - 31812.
[Abstract] [Full Text] [PDF]

K. Bhat, G Farkas, F Karch, H Gyurkovics, J Gausz, and P Schedl
The GAGA factor is required in the early Drosophila embryo not only for transcriptional regulation but also for nuclear division
Development, January 4, 1996; 122(4): 1113 - 1124.
[Abstract] [PDF]

L L Wallrath and S C Elgin
Position effect variegation in Drosophila is associated with an altered chromatin structure.
Genes & Dev., May 15, 1995; 9(10): 1263 - 1277.
[Abstract] [PDF]

K.-K. Hwang, J. C. Eissenberg, and H. J. Worman
Transcriptional repression of euchromatic genes by Drosophila heterochromatin protein 1 and histone modifiers
PNAS, September 25, 2001; 98(20): 11423 - 11427.
[Abstract] [Full Text] [PDF]

A. B. Carvalho, B. P. Lazzaro, and A. G. Clark
Y chromosomal fertility factors kl-2 and kl-3 of Drosophila melanogaster encode dynein heavy chain polypeptides
PNAS, November 21, 2000; 97(24): 13239 - 13244.
[Abstract] [Full Text] [PDF]

				A.-S. Fiston-Lavier, D. Anxolabehere, and H. Quesneville A model of segmental duplication formation in Drosophila melanogaster Genome Res., October 1, 2007; 17(10): 1458 - 1470. [Abstract] [Full Text] [PDF]

				E. N. Andreyeva, T. D. Kolesnikova, O. V. Demakova, M. Mendez-Lago, G. V. Pokholkova, E. S. Belyaeva, F. Rossi, P. Dimitri, A. Villasante, and I. F. Zhimulev High-resolution analysis of Drosophila heterochromatin organization using SuUR Su(var)3-9 double mutants PNAS, July 31, 2007; 104(31): 12819 - 12824. [Abstract] [Full Text] [PDF]

				L. Usakin, J. Abad, V. V. Vagin, B. de Pablos, A. Villasante, and V. A. Gvozdev Transcription of the 1.688 Satellite DNA Family Is Under the Control of RNA Interference Machinery in Drosophila melanogaster Ovaries Genetics, June 1, 2007; 176(2): 1343 - 1349. [Abstract] [Full Text] [PDF]

				Y. Xiang and R. S. Hawley The Mechanism of Secondary Nondisjunction in Drosophila melanogaster Females Genetics, September 1, 2006; 174(1): 67 - 78. [Abstract] [Full Text] [PDF]

				M. K. Gilbert, Y. Y. Tan, and C. M. Hart The Drosophila Boundary Element-Associated Factors BEAF-32A and BEAF-32B Affect Chromatin Structure Genetics, July 1, 2006; 173(3): 1365 - 1375. [Abstract] [Full Text] [PDF]

				D. J. Orengo, M. Papaceit, and E. Juan A Minisatellite with Fold-Back Structure is Included in the 5'-Flanking Region of the Adh Gene of Scaptodrosophila lebanonensis J. Hered., January 1, 2004; 95(1): 62 - 69. [Abstract] [Full Text] [PDF]

				B. T. Sage and A. K. Csink Heterochromatic Self-Association, a Determinant of Nuclear Organization, Does Not Require Sequence Homology in Drosophila Genetics, November 1, 2003; 165(3): 1183 - 1193. [Abstract] [Full Text] [PDF]

				P. Dimitri, N. Junakovic, and B. Arca Colonization of Heterochromatic Genes by Transposable Elements in Drosophila Mol. Biol. Evol., April 1, 2003; 20(4): 503 - 512. [Abstract] [Full Text] [PDF]

				D. E. Koryakov, E. V. Domanitskaya, S. N. Belyakin, and I. F. Zhimulev Abnormal tissue-dependent polytenization of a block of chromosome 3 pericentric heterochromatin in Drosophila melanogaster J. Cell Sci., March 15, 2003; 116(6): 1035 - 1044. [Abstract] [Full Text] [PDF]

				X. Sun, H. D. Le, J. M. Wahlstrom, and G. H. Karpen Sequence Analysis of a Functional Drosophila Centromere Genome Res., February 1, 2003; 13(2): 182 - 194. [Abstract] [Full Text] [PDF]

				C. M. Yan, K. W. Dobie, H. D. Le, A. Y. Konev, and G. H. Karpen Efficient Recovery of Centric Heterochromatin P-Element Insertions in Drosophila melanogaster Genetics, May 1, 2002; 161(1): 217 - 229. [Abstract] [Full Text] [PDF]

				N. Aulner, C. Monod, G. Mandicourt, D. Jullien, O. Cuvier, A. Sall, S. Janssen, U. K. Laemmli, and E. Kas The AT-Hook Protein D1 Is Essential for Drosophila melanogaster Development and Is Implicated in Position-Effect Variegation Mol. Cell. Biol., February 15, 2002; 22(4): 1218 - 1232. [Abstract] [Full Text] [PDF]

				D. E. Koryakov, I. F. Zhimulev, and P. Dimitri Cytogenetic Analysis of the Third Chromosome Heterochromatin of Drosophila melanogaster Genetics, February 1, 2002; 160(2): 509 - 517. [Abstract] [Full Text] [PDF]

				C. J. B. Rohr, H. Ranson, X. Wang, and N. J. Besansky Structure and Evolution of mtanga, a Retrotransposon Actively Expressed on the Y Chromosome of the African Malaria Vector Anopheles gambiae Mol. Biol. Evol., February 1, 2002; 19(2): 149 - 162. [Abstract] [Full Text] [PDF]

				K.-K. Hwang, J. C. Eissenberg, and H. J. Worman Transcriptional repression of euchromatic genes by Drosophila heterochromatin protein 1 and histone modifiers PNAS, September 13, 2001; (2001) 211303598. [Abstract] [Full Text] [PDF]

				H. S. Malik and S. Henikoff Adaptive Evolution of Cid, a Centromere-Specific Histone in Drosophila Genetics, March 1, 2001; 157(3): 1293 - 1298. [Abstract] [Full Text]

				A. B. Carvalho, B. P. Lazzaro, and A. G. Clark Y chromosomal fertility factors kl-2 and kl-3 of Drosophila melanogaster encode dynein heavy chain polypeptides PNAS, November 2, 2000; (2000) 230438397. [Abstract] [Full Text]

				T. Torok, M. Gorjanacz, P. J. Bryant, and I. Kiss Prod is a novel DNA-binding protein that binds to the 1.686 g/cm3 10 bp satellite repeat of Drosophila melanogaster Nucleic Acids Res., September 15, 2000; 28(18): 3551 - 3557. [Abstract] [Full Text] [PDF]

				J. Locke, L. Podemski, N. Aippersbach, H. Kemp, and R. Hodgetts A Physical Map of the Polytenized Region (101EF-102F) of Chromosome 4 in Drosophila melanogaster Genetics, July 1, 2000; 155(3): 1175 - 1183. [Abstract] [Full Text]

				A. Cortés and F. Azorín DDP1, a Heterochromatin-Associated Multi-KH-Domain Protein of Drosophila melanogaster, Interacts Specifically with Centromeric Satellite DNA Sequences Mol. Cell. Biol., June 1, 2000; 20(11): 3860 - 3869. [Abstract] [Full Text]

				B. Timakov and P. Zhang Genetic Analysis of a Y-Chromosome Region That Induces Triplosterile Phenotypes and Is Essential for Spermatid Individualization in Drosophila melanogaster Genetics, May 1, 2000; 155(1): 179 - 189. [Abstract] [Full Text]

				E. V. Tolchkov, V. I. Rasheva, S. Bonaccorsi, T. Westphal, and V. A. Gvozdev The Size and Internal Structure of a Heterochromatic Block Determine Its Ability to Induce Position Effect Variegation in Drosophila melanogaster Genetics, April 1, 2000; 154(4): 1611 - 1626. [Abstract] [Full Text]

				M. D. Adams, S. E. Celniker, R. A. Holt, C. A. Evans, J. D. Gocayne, P. G. Amanatides, S. E. Scherer, P. W. Li, R. A. Hoskins, R. F. Galle, et al. The Genome Sequence of Drosophila melanogaster Science, March 24, 2000; 287(5461): 2185 - 2195. [Abstract] [Full Text]

				J. Locke, L. Podemski, K. Roy, D. Pilgrim, and R. Hodgetts Analysis of Two Cosmid Clones from Chromosome 4 of Drosophila melanogaster Reveals Two New Genes Amid an Unusual Arrangement of Repeated Sequences Genome Res., February 1, 1999; 9(2): 137 - 149. [Abstract] [Full Text]

				K. Dej and A. Spradling The endocycle controls nurse cell polytene chromosome structure during Drosophila oogenesis Development, January 1, 1999; 126(2): 293 - 303. [Abstract] [PDF]

				Y. S. Rong and K. G. Golic Dominant Defects in Drosophila Eye Pigmentation Resulting From a Euchromatin-Heterochromatin Fusion Gene Genetics, December 1, 1998; 150(4): 1551 - 1566. [Abstract] [Full Text]

				A. K. Csink and S. Henikoff Large-scale Chromosomal Movements During Interphase Progression in Drosophila J. Cell Biol., October 5, 1998; 143(1): 13 - 22. [Abstract] [Full Text] [PDF]

				E. B. Cambareri, R. Aisner, and J. Carbon Structure of the Chromosome VII Centromere Region in Neurospora crassa: Degenerate Transposons and Simple Repeats Mol. Cell. Biol., September 1, 1998; 18(9): 5465 - 5477. [Abstract] [Full Text]

				E. V. Ananiev, R. L. Phillips, and H. W. Rines Complex Structure of Knob DNA on Maize Chromosome 9: Retrotransposon Invasion into Heterochromatin Genetics, August 1, 1998; 149(4): 2025 - 2037. [Abstract] [Full Text] [PDF]

				J. C. Fung, W. F. Marshall, A. Dernburg, D. A. Agard, and J. W. Sedat Homologous Chromosome Pairing in Drosophila melanogaster Proceeds through Multiple Independent Initiations J. Cell Biol., April 6, 1998; 141(1): 5 - 20. [Abstract] [Full Text] [PDF]