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. 2002 Feb;160(2):609–621. doi: 10.1093/genetics/160.2.609

Recombinogenic effects of suppressors of position-effect variegation in Drosophila.

Thomas Westphal 1, Gunter Reuter 1
PMCID: PMC1461983  PMID: 11861565

Abstract

Compact chromatin structure, induction of gene silencing in position-effect variegation (PEV), and crossing-over suppression are typical features of heterochromatin. To identify genes affecting crossing-over suppression by heterochromatin we tested PEV suppressor mutations for their effects on crossing over in pericentromeric regions of Drosophila autosomes. From the 46 mutations (28 loci) studied, 16 Su(var) mutations of the nine genes Su(var)2-1, Su(var)2-2, Su(var)2-5, Su(var)2-10, Su(var)2-14, Su(var)2-15, Su(var)3-3, Su(var)3-7, and Su(var)3-9 significantly increase in heterozygotes or by additive effects in double and triple heterozygotes crossing over in the ri-p(p) region of chromosome 3. Su(var)2-2(01) and Su(var)2-14(01) display the strongest recombinogenic effects and were also shown to enhance recombination within the light-rolled heterochromatic region of chromosome 2. The dominant recombinogenic effects of Su(var) mutations are most pronounced in proximal euchromatin and are accompanied with significant reduction of meiotic nondisjunction. Our data suggest that crossing-over suppression by heterochromatin is controlled at chromatin structure as well as illustrate the possible effects of heterochromatin on total crossing-over frequencies in the genome.

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Selected References

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

  1. Anderson L. K., Reeves A., Webb L. M., Ashley T. Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics. 1999 Apr;151(4):1569–1579. doi: 10.1093/genetics/151.4.1569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker B. S., Carpenter A. T., Esposito M. S., Esposito R. E., Sandler L. The genetic control of meiosis. Annu Rev Genet. 1976;10:53–134. doi: 10.1146/annurev.ge.10.120176.000413. [DOI] [PubMed] [Google Scholar]
  3. Baker B. S., Carpenter A. T. Genetic analysis of sex chromosomal meiotic mutants in Drosophilia melanogaster. Genetics. 1972 Jun;71(2):255–286. doi: 10.1093/genetics/71.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Baksa K., Morawietz H., Dombrádi V., Axton M., Taubert H., Szabó G., Török I., Udvardy A., Gyurkovics H., Ször B. Mutations in the protein phosphatase 1 gene at 87B can differentially affect suppression of position-effect variegation and mitosis in Drosophila melanogaster. Genetics. 1993 Sep;135(1):117–125. doi: 10.1093/genetics/135.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beadle G. W. A Possible Influence of the Spindle Fibre on Crossing-Over in Drosophila. Proc Natl Acad Sci U S A. 1932 Feb;18(2):160–165. doi: 10.1073/pnas.18.2.160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Berghella L., Dimitri P. The heterochromatic rolled gene of Drosophila melanogaster is extensively polytenized and transcriptionally active in the salivary gland chromocenter. Genetics. 1996 Sep;144(1):117–125. doi: 10.1093/genetics/144.1.117. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bhat K. M., Farkas G., Karch F., Gyurkovics H., Gausz J., Schedl P. The GAGA factor is required in the early Drosophila embryo not only for transcriptional regulation but also for nuclear division. Development. 1996 Apr;122(4):1113–1124. doi: 10.1242/dev.122.4.1113. [DOI] [PubMed] [Google Scholar]
  8. Carpenter A. T., Baker B. S. On the Control of the Distribution of Meiotic Exchange in DROSOPHILA MELANOGASTER. Genetics. 1982 May;101(1):81–89. doi: 10.1093/genetics/101.1.81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cléard F., Delattre M., Spierer P. SU(VAR)3-7, a Drosophila heterochromatin-associated protein and companion of HP1 in the genomic silencing of position-effect variegation. EMBO J. 1997 Sep 1;16(17):5280–5288. doi: 10.1093/emboj/16.17.5280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Comings D. E. The structure and function of chromatin. Adv Hum Genet. 1972;3:237–431. doi: 10.1007/978-1-4757-4429-3_5. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Eissenberg J. C., James T. C., Foster-Hartnett D. M., Hartnett T., Ngan V., Elgin S. C. Mutation in a heterochromatin-specific chromosomal protein is associated with suppression of position-effect variegation in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1990 Dec;87(24):9923–9927. doi: 10.1073/pnas.87.24.9923. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Eissenberg J. C., Morris G. D., Reuter G., Hartnett T. The heterochromatin-associated protein HP-1 is an essential protein in Drosophila with dosage-dependent effects on position-effect variegation. Genetics. 1992 Jun;131(2):345–352. doi: 10.1093/genetics/131.2.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fanti L., Giovinazzo G., Berloco M., Pimpinelli S. The heterochromatin protein 1 prevents telomere fusions in Drosophila. Mol Cell. 1998 Nov;2(5):527–538. doi: 10.1016/s1097-2765(00)80152-5. [DOI] [PubMed] [Google Scholar]
  15. Gatti M., Baker B. S. Genes controlling essential cell-cycle functions in Drosophila melanogaster. Genes Dev. 1989 Apr;3(4):438–453. doi: 10.1101/gad.3.4.438. [DOI] [PubMed] [Google Scholar]
  16. Grigliatti T. Position-effect variegation--an assay for nonhistone chromosomal proteins and chromatin assembly and modifying factors. Methods Cell Biol. 1991;35:587–627. [PubMed] [Google Scholar]
  17. Hari K. L., Cook K. R., Karpen G. H. The Drosophila Su(var)2-10 locus regulates chromosome structure and function and encodes a member of the PIAS protein family. Genes Dev. 2001 Jun 1;15(11):1334–1348. doi: 10.1101/gad.877901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hawley R. S., Irick H., Zitron A. E., Haddox D. A., Lohe A., New C., Whitley M. D., Arbel T., Jang J., McKim K. There are two mechanisms of achiasmate segregation in Drosophila females, one of which requires heterochromatic homology. Dev Genet. 1992;13(6):440–467. doi: 10.1002/dvg.1020130608. [DOI] [PubMed] [Google Scholar]
  19. Hawley R. S. Meiosis as an "M" thing: twenty-five years of meiotic mutants in Drosophila. Genetics. 1993 Nov;135(3):613–618. doi: 10.1093/genetics/135.3.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ising G., Block K. Derivation-dependent distribution of insertion sites for a Drosophila transposon. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 2):527–544. doi: 10.1101/sqb.1981.045.01.069. [DOI] [PubMed] [Google Scholar]
  21. Karpen G. H., Le M. H., Le H. Centric heterochromatin and the efficiency of achiasmate disjunction in Drosophila female meiosis. Science. 1996 Jul 5;273(5271):118–122. doi: 10.1126/science.273.5271.118. [DOI] [PubMed] [Google Scholar]
  22. Kastenbaum M. A., Bowman K. O. Tables for determining the statistical significance of mutation frequencies. Mutat Res. 1970 May;9(5):527–549. doi: 10.1016/0027-5107(70)90038-2. [DOI] [PubMed] [Google Scholar]
  23. Koehler K. E., Boulton C. L., Collins H. E., French R. L., Herman K. C., Lacefield S. M., Madden L. D., Schuetz C. D., Hawley R. S. Spontaneous X chromosome MI and MII nondisjunction events in Drosophila melanogaster oocytes have different recombinational histories. Nat Genet. 1996 Dec;14(4):406–414. doi: 10.1038/ng1296-406. [DOI] [PubMed] [Google Scholar]
  24. Lamb N. E., Freeman S. B., Savage-Austin A., Pettay D., Taft L., Hersey J., Gu Y., Shen J., Saker D., May K. M. Susceptible chiasmate configurations of chromosome 21 predispose to non-disjunction in both maternal meiosis I and meiosis II. Nat Genet. 1996 Dec;14(4):400–405. doi: 10.1038/ng1296-400. [DOI] [PubMed] [Google Scholar]
  25. Lindsley D. L., Sandler L. The genetic analysis of meiosis in female Drosophila melanogaster. Philos Trans R Soc Lond B Biol Sci. 1977 Mar 21;277(955):295–312. doi: 10.1098/rstb.1977.0019. [DOI] [PubMed] [Google Scholar]
  26. Mather K. Crossing over and Heterochromatin in the X Chromosome of Drosophila Melanogaster. Genetics. 1939 Apr;24(3):413–435. doi: 10.1093/genetics/24.3.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. ROBERTS P. A. DIFFERENCE IN THE BEHAVIOR OF EU- AND HETERO-CHROMATIN: CROSSING-OVER. Nature. 1965 Feb 13;205:725–726. doi: 10.1038/205725b0. [DOI] [PubMed] [Google Scholar]
  28. Reuter G., Dorn R., Hoffmann H. J. Butyrate sensitive suppressor of position-effect variegation mutations in Drosophila melanogaster. Mol Gen Genet. 1982;188(3):480–485. doi: 10.1007/BF00330052. [DOI] [PubMed] [Google Scholar]
  29. Reuter G., Giarre M., Farah J., Gausz J., Spierer A., Spierer P. Dependence of position-effect variegation in Drosophila on dose of a gene encoding an unusual zinc-finger protein. Nature. 1990 Mar 15;344(6263):219–223. doi: 10.1038/344219a0. [DOI] [PubMed] [Google Scholar]
  30. Reuter G., Spierer P. Position effect variegation and chromatin proteins. Bioessays. 1992 Sep;14(9):605–612. doi: 10.1002/bies.950140907. [DOI] [PubMed] [Google Scholar]
  31. Reuter G., Wolff I. Isolation of dominant suppressor mutations for position-effect variegation in Drosophila melanogaster. Mol Gen Genet. 1981;182(3):516–519. doi: 10.1007/BF00293947. [DOI] [PubMed] [Google Scholar]
  32. Sandler L., Lindsley D. L., Nicoletti B., Trippa G. Mutants affecting meiosis in natural populations of Drosophila melanogaster. Genetics. 1968 Nov;60(3):525–558. doi: 10.1093/genetics/60.3.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Schotta G., Reuter G. Controlled expression of tagged proteins in Drosophila using a new modular P-element vector system. Mol Gen Genet. 2000 Jan;262(6):916–920. doi: 10.1007/pl00008659. [DOI] [PubMed] [Google Scholar]
  34. Sekelsky J. J., McKim K. S., Messina L., French R. L., Hurley W. D., Arbel T., Chin G. M., Deneen B., Force S. J., Hari K. L. Identification of novel Drosophila meiotic genes recovered in a P-element screen. Genetics. 1999 Jun;152(2):529–542. doi: 10.1093/genetics/152.2.529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sherman J. D., Stack S. M. Two-dimensional spreads of synaptonemal complexes from solanaceous plants. VI. High-resolution recombination nodule map for tomato (Lycopersicon esculentum). Genetics. 1995 Oct;141(2):683–708. doi: 10.1093/genetics/141.2.683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sinclair D. A. Crossing over between closely linked markers spanning the centromere of chromosome 3 in drosophila melanogaster. Genet Res. 1975 Oct;26(2):173–185. doi: 10.1017/s0016672300015974. [DOI] [PubMed] [Google Scholar]
  37. Sinclair D. A., Ruddell A. A., Brock J. K., Clegg N. J., Lloyd V. K., Grigliatti T. A. A cytogenetic and genetic characterization of a group of closely linked second chromosome mutations that suppress position-effect variegation in Drosophila melanogaster. Genetics. 1992 Feb;130(2):333–344. doi: 10.1093/genetics/130.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Stack S. M. Heterochromatin, the synaptonemal complex and crossing over. J Cell Sci. 1984 Oct;71:159–176. doi: 10.1242/jcs.71.1.159. [DOI] [PubMed] [Google Scholar]
  39. Tschiersch B., Hofmann A., Krauss V., Dorn R., Korge G., Reuter G. The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J. 1994 Aug 15;13(16):3822–3831. doi: 10.1002/j.1460-2075.1994.tb06693.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Vernì F., Gandhi R., Goldberg M. L., Gatti M. Genetic and molecular analysis of wings apart-like (wapl), a gene controlling heterochromatin organization in Drosophila melanogaster. Genetics. 2000 Apr;154(4):1693–1710. doi: 10.1093/genetics/154.4.1693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Weiler K. S., Wakimoto B. T. Heterochromatin and gene expression in Drosophila. Annu Rev Genet. 1995;29:577–605. doi: 10.1146/annurev.ge.29.120195.003045. [DOI] [PubMed] [Google Scholar]
  42. Wustmann G., Szidonya J., Taubert H., Reuter G. The genetics of position-effect variegation modifying loci in Drosophila melanogaster. Mol Gen Genet. 1989 Jun;217(2-3):520–527. doi: 10.1007/BF02464926. [DOI] [PubMed] [Google Scholar]
  43. Yamamoto M. T., Mitchelson A., Tudor M., O'Hare K., Davies J. A., Miklos G. L. Molecular and cytogenetic analysis of the heterochromatin-euchromatin junction region of the Drosophila melanogaster X chromosome using cloned DNA sequences. Genetics. 1990 Aug;125(4):821–832. doi: 10.1093/genetics/125.4.821. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Yamamoto M. Interchromosomal effects of heterochromatic deletions on recombination in Drosophila melanogaster. Genetics. 1979 Oct;93(2):437–448. doi: 10.1093/genetics/93.2.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Yamamoto M., Miklos G. L. Genetic studies on heterochromatin in Drosophila melanogaster and their implications for the functions of satellite DNA. Chromosoma. 1978 Mar 22;66(1):71–98. doi: 10.1007/BF00285817. [DOI] [PubMed] [Google Scholar]
  46. Zickler D., Kleckner N. Meiotic chromosomes: integrating structure and function. Annu Rev Genet. 1999;33:603–754. doi: 10.1146/annurev.genet.33.1.603. [DOI] [PubMed] [Google Scholar]

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