Abstract
A second chromosomal trans-acting modifier, Lightener of white (Low), modulates the phenotypic expression of various alleles of the white eye color gene. This modifier has an unusually broad spectrum of affected genes including white, brown, scarlet and the eye developmental genes, Bar and Lobe. In addition, Low weakly suppresses position effect variegation. Northern blot hybridization with different X and autosomal probes reveals that Low modulates genes of independent expression patterns. Interestingly, many of the modulations of gene expression are developmentally restricted and differ in intensity between the sexes. Low also elevates the expression of the histone tandem repeats in three distinct developmental stages. A deficiency encompassing the histone cluster reduces their transcript levels and significantly alters the expression of some of the tested genes. Thus, Low is a modifier that plays a role in modulating the expression of genes governing various processes including pigment deposition, eye development, chromosomal proteins and position effect variegation.
Full Text
The Full Text of this article is available as a PDF (6.8 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Baker B. S., Gorman M., Marín I. Dosage compensation in Drosophila. Annu Rev Genet. 1994;28:491–521. doi: 10.1146/annurev.ge.28.120194.002423. [DOI] [PubMed] [Google Scholar]
- 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]
- Belyaeva E. S., Zhimulev I. F. Cytogenetic and molecular aspects of position effect variegation in Drosophila. III. Continuous and discontinuous compaction of chromosomal material as a result of position effect variegation. Chromosoma. 1991 Aug;100(7):453–466. doi: 10.1007/BF00364556. [DOI] [PubMed] [Google Scholar]
- Bhadra U., Birchler J. A. Characterization of a sex-influenced modifier of gene expression and suppressor of position-effect variegation in Drosophila. Mol Gen Genet. 1996 Mar 20;250(5):601–613. doi: 10.1007/BF02174448. [DOI] [PubMed] [Google Scholar]
- Bier E., Vaessin H., Shepherd S., Lee K., McCall K., Barbel S., Ackerman L., Carretto R., Uemura T., Grell E. Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 1989 Sep;3(9):1273–1287. doi: 10.1101/gad.3.9.1273. [DOI] [PubMed] [Google Scholar]
- Bingham P. M., Chapman C. H. Evidence that white-blood is a novel type of temperature-sensitive mutation resulting from temperature-dependent effects of a transposon insertion on formation of white transcripts. EMBO J. 1986 Dec 1;5(12):3343–3351. doi: 10.1002/j.1460-2075.1986.tb04649.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bingham P. M., Judd B. H. A copy of the copia transposable element is very tightly linked to the Wa allele at the white locus of D. melanogaster. Cell. 1981 Sep;25(3):705–711. doi: 10.1016/0092-8674(81)90177-x. [DOI] [PubMed] [Google Scholar]
- Bingham P. M., Zachar Z. Evidence that two mutations, wDZL and z1, affecting synapsis-dependent genetic behavior of white are transcriptional regulatory mutations. Cell. 1985 Apr;40(4):819–825. doi: 10.1016/0092-8674(85)90341-1. [DOI] [PubMed] [Google Scholar]
- Birchler J. A. A study of enzyme activities in a dosage series of the long arm of chromosome one in maize. Genetics. 1979 Aug;92(4):1211–1229. doi: 10.1093/genetics/92.4.1211. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Birchler J. A., Hiebert J. C. Interaction of the Enhancer of white-apricot with transposable element alleles at the white locus in Drosophila melanogaster. Genetics. 1989 May;122(1):129–138. doi: 10.1093/genetics/122.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Birchler J. A., Hiebert J. C., Paigen K. Analysis of autosomal dosage compensation involving the alcohol dehydrogenase locus in Drosophila melanogaster. Genetics. 1990 Mar;124(3):679–686. [PMC free article] [PubMed] [Google Scholar]
- Birchler J. A., Newton K. J. Modulation of protein levels in chromosomal dosage series of maize: the biochemical basis of aneuploid syndromes. Genetics. 1981 Oct;99(2):247–266. doi: 10.1093/genetics/99.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Birchler J. A. The genetic basis of dosage compensation of alcohol dehydrogenase-1 in maize. Genetics. 1981 Mar;97(3-4):625–637. doi: 10.1093/genetics/97.3-4.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bouvet P., Dimitrov S., Wolffe A. P. Specific regulation of Xenopus chromosomal 5S rRNA gene transcription in vivo by histone H1. Genes Dev. 1994 May 15;8(10):1147–1159. doi: 10.1101/gad.8.10.1147. [DOI] [PubMed] [Google Scholar]
- Carbonare B. D., Gehring W. J. Excision of copia element in a revertant of the white-apricot mutation of Drosophila melanogaster leaves behind one long-terminal repeat. Mol Gen Genet. 1985;199(1):1–6. doi: 10.1007/BF00327501. [DOI] [PubMed] [Google Scholar]
- Chen J. D., Pirrotta V. Multimerization of the Drosophila zeste protein is required for efficient DNA binding. EMBO J. 1993 May;12(5):2075–2083. doi: 10.1002/j.1460-2075.1993.tb05856.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Csink A. K., Linsk R., Birchler J. A. Mosaic suppressor, a gene in Drosophila that modifies retrotransposon expression and interacts with zeste. Genetics. 1994 Feb;136(2):573–583. doi: 10.1093/genetics/136.2.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Csink A. K., Linsk R., Birchler J. A. The Lighten up (Lip) gene of Drosophila melanogaster, a modifier of retroelement expression, position effect variegation and white locus insertion alleles. Genetics. 1994 Sep;138(1):153–163. doi: 10.1093/genetics/138.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Davis P. S., Shen M. W., Judd B. H. Asymmetrical pairings of transposons in and proximal to the white locus of Drosophila account for four classes of regularly occurring exchange products. Proc Natl Acad Sci U S A. 1987 Jan;84(1):174–178. doi: 10.1073/pnas.84.1.174. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Davison D., Chapman C. H., Wedeen C., Bingham P. M. Genetic and physical studies of a portion of the white locus participating in transcriptional regulation and in synapsis-dependent interactions in Drosophila adult tissues. Genetics. 1985 Jul;110(3):479–494. doi: 10.1093/genetics/110.3.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Devlin R. H., Holm D. G., Grigliatti T. A. Autosomal dosage compensation Drosophila melanogaster strains trisomic for the left arm of chromosome 2. Proc Natl Acad Sci U S A. 1982 Feb;79(4):1200–1204. doi: 10.1073/pnas.79.4.1200. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Devlin R. H., Holm D. G., Grigliatti T. A. The influence of whole-arm trisomy on gene expression in Drosophila. Genetics. 1988 Jan;118(1):87–101. doi: 10.1093/genetics/118.1.87. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dorn R., Krauss V., Reuter G., Saumweber H. The enhancer of position-effect variegation of Drosophila, E(var)3-93D, codes for a chromatin protein containing a conserved domain common to several transcriptional regulators. Proc Natl Acad Sci U S A. 1993 Dec 1;90(23):11376–11380. doi: 10.1073/pnas.90.23.11376. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dreesen T. D., Johnson D. H., Henikoff S. The brown protein of Drosophila melanogaster is similar to the white protein and to components of active transport complexes. Mol Cell Biol. 1988 Dec;8(12):5206–5215. doi: 10.1128/mcb.8.12.5206. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eissenberg J. C. Position effect variegation in Drosophila: towards a genetics of chromatin assembly. Bioessays. 1989 Jul;11(1):14–17. doi: 10.1002/bies.950110105. [DOI] [PubMed] [Google Scholar]
- Farkas G., Gausz J., Galloni M., Reuter G., Gyurkovics H., Karch F. The Trithorax-like gene encodes the Drosophila GAGA factor. Nature. 1994 Oct 27;371(6500):806–808. doi: 10.1038/371806a0. [DOI] [PubMed] [Google Scholar]
- Fawcett D. H., Lister C. K., Kellett E., Finnegan D. J. Transposable elements controlling I-R hybrid dysgenesis in D. melanogaster are similar to mammalian LINEs. Cell. 1986 Dec 26;47(6):1007–1015. doi: 10.1016/0092-8674(86)90815-9. [DOI] [PubMed] [Google Scholar]
- Fisher-Adams G., Grunstein M. Yeast histone H4 and H3 N-termini have different effects on the chromatin structure of the GAL1 promoter. EMBO J. 1995 Apr 3;14(7):1468–1477. doi: 10.1002/j.1460-2075.1995.tb07133.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gehring W. J., Paro R. Isolation of a hybrid plasmid with homologous sequences to a transposing element of Drosophila melanogaster. Cell. 1980 Apr;19(4):897–904. doi: 10.1016/0092-8674(80)90081-1. [DOI] [PubMed] [Google Scholar]
- Goldberg M. L., Sheen J. Y., Gehring W. J., Green M. M. Unequal crossing-over associated with asymmetrical synapsis between nomadic elements in the Drosophila melanogaster genome. Proc Natl Acad Sci U S A. 1983 Aug;80(16):5017–5021. doi: 10.1073/pnas.80.16.5017. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Gunaratne P. H., Mansukhani A., Lipari S. E., Liou H. C., Martindale D. W., Goldberg M. L. Molecular cloning, germ-line transformation, and transcriptional analysis of the zeste locus of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1986 Feb;83(3):701–705. doi: 10.1073/pnas.83.3.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Guo M., Birchler J. A. Trans-acting dosage effects on the expression of model gene systems in maize aneuploids. Science. 1994 Dec 23;266(5193):1999–2002. doi: 10.1126/science.266.5193.1999. [DOI] [PubMed] [Google Scholar]
- Hayashi S., Ruddell A., Sinclair D., Grigliatti T. Chromosomal structure is altered by mutations that suppress or enhance position effect variegation. Chromosoma. 1990 Oct;99(6):391–400. doi: 10.1007/BF01726690. [DOI] [PubMed] [Google Scholar]
- Henikoff S. Dosage-dependent modification of position-effect variegation in Drosophila. Bioessays. 1996 May;18(5):401–409. doi: 10.1002/bies.950180510. [DOI] [PubMed] [Google Scholar]
- Hiebert J. C., Birchler J. A. Effects of the maleless mutation on X and autosomal gene expression in Drosophila melanogaster. Genetics. 1994 Mar;136(3):913–926. doi: 10.1093/genetics/136.3.913. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jack J. W., Judd B. H. Allelic pairing and gene regulation: A model for the zeste-white interaction in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1979 Mar;76(3):1368–1372. doi: 10.1073/pnas.76.3.1368. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kandolf H. The H1A histone variant is an in vivo repressor of oocyte-type 5S gene transcription in Xenopus laevis embryos. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7257–7261. doi: 10.1073/pnas.91.15.7257. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Karess R. E., Rubin G. M. A small tandem duplication is responsible for the unstable white-ivory mutation in Drosophila. Cell. 1982 Aug;30(1):63–69. doi: 10.1016/0092-8674(82)90012-5. [DOI] [PubMed] [Google Scholar]
- Karpen G. H., Spradling A. C. Reduced DNA polytenization of a minichromosome region undergoing position-effect variegation in Drosophila. Cell. 1990 Oct 5;63(1):97–107. doi: 10.1016/0092-8674(90)90291-l. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kelley R. L., Kuroda M. I. Equality for X chromosomes. Science. 1995 Dec 8;270(5242):1607–1610. doi: 10.1126/science.270.5242.1607. [DOI] [PubMed] [Google Scholar]
- Kim U. J., Han M., Kayne P., Grunstein M. Effects of histone H4 depletion on the cell cycle and transcription of Saccharomyces cerevisiae. EMBO J. 1988 Jul;7(7):2211–2219. doi: 10.1002/j.1460-2075.1988.tb03060.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Klose J., Putz B. Analysis of two-dimensional protein patterns from mouse embryos with different trisomies. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3753–3757. doi: 10.1073/pnas.80.12.3753. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kojima T., Ishimaru S., Higashijima S., Takayama E., Akimaru H., Sone M., Emori Y., Saigo K. Identification of a different-type homeobox gene, BarH1, possibly causing Bar (B) and Om(1D) mutations in Drosophila. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4343–4347. doi: 10.1073/pnas.88.10.4343. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Levis R., Hazelrigg T., Rubin G. M. Separable cis-acting control elements for expression of the white gene of Drosophila. EMBO J. 1985 Dec 16;4(13A):3489–3499. doi: 10.1002/j.1460-2075.1985.tb04108.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Locke J., Kotarski M. A., Tartof K. D. Dosage-dependent modifiers of position effect variegation in Drosophila and a mass action model that explains their effect. Genetics. 1988 Sep;120(1):181–198. doi: 10.1093/genetics/120.1.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lucchesi J. C., Skripsky T. The link between dosage compensation and sex differentiation in Drosophila melanogaster. Chromosoma. 1981;82(2):217–227. doi: 10.1007/BF00286106. [DOI] [PubMed] [Google Scholar]
- Moore G. D., Sinclair D. A., Grigliatti T. A. Histone Gene Multiplicity and Position Effect Variegation in DROSOPHILA MELANOGASTER. Genetics. 1983 Oct;105(2):327–344. doi: 10.1093/genetics/105.2.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mount S. M., Green M. M., Rubin G. M. Partial revertants of the transposable element-associated suppressible allele white-apricot in Drosophila melanogaster: structures and responsiveness to genetic modifiers. Genetics. 1988 Feb;118(2):221–234. doi: 10.1093/genetics/118.2.221. [DOI] [PMC free article] [PubMed] [Google Scholar]
- O'Brien S. J., Gethmann R. C. Segmental aneuploidy as a probe for structural genes in Drosophila: mitochondrial membrane enzymes. Genetics. 1973 Sep;75(1):155–167. doi: 10.1093/genetics/75.1.155. [DOI] [PMC free article] [PubMed] [Google Scholar]
- O'Hare K., Alley M. R., Cullingford T. E., Driver A., Sanderson M. J. DNA sequence of the Doc retroposon in the white-one mutant of Drosophila melanogaster and of secondary insertions in the phenotypically altered derivatives white-honey and white-eosin. Mol Gen Genet. 1991 Jan;225(1):17–24. doi: 10.1007/BF00282637. [DOI] [PubMed] [Google Scholar]
- Pirrotta V. Vectors for P-mediated transformation in Drosophila. Biotechnology. 1988;10:437–456. doi: 10.1016/b978-0-409-90042-2.50028-3. [DOI] [PubMed] [Google Scholar]
- Rabinow L., Nguyen-Huynh A. T., Birchler J. A. A trans-acting regulatory gene that inversely affects the expression of the white, brown and scarlet loci in Drosophila. Genetics. 1991 Oct;129(2):463–480. doi: 10.1093/genetics/129.2.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Raha S., Merante F., Proteau G., Reed J. K. Simultaneous isolation of total cellular RNA and DNA from tissue culture cells using phenol and lithium chloride. Genet Anal Tech Appl. 1990 Nov;7(7):173–177. doi: 10.1016/0735-0651(90)90022-8. [DOI] [PubMed] [Google Scholar]
- Reichert G. H. Two-dimensional gel analysis of proteins from mouse fetuses with trisomy 19 after DEAE-Sepharose chromatography. Genet Res. 1986 Jun;47(3):193–197. doi: 10.1017/s0016672300023120. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- 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]
- Sabl J. F., Birchler J. A. Dosage dependent modifiers of white alleles in Drosophila melanogaster. Genet Res. 1993 Aug;62(1):15–22. doi: 10.1017/s0016672300031517. [DOI] [PubMed] [Google Scholar]
- Seum C., Spierer A., Pauli D., Szidonya J., Reuter G., Spierer P. Position-effect variegation in Drosophila depends on dose of the gene encoding the E2F transcriptional activator and cell cycle regulator. Development. 1996 Jun;122(6):1949–1956. doi: 10.1242/dev.122.6.1949. [DOI] [PubMed] [Google Scholar]
- Shen X., Gorovsky M. A. Linker histone H1 regulates specific gene expression but not global transcription in vivo. Cell. 1996 Aug 9;86(3):475–483. doi: 10.1016/s0092-8674(00)80120-8. [DOI] [PubMed] [Google Scholar]
- Sinclair D. A., Lloyd V. K., Grigliatti T. A. Characterization of mutations that enhance position-effect variegation in Drosophila melanogaster. Mol Gen Genet. 1989 Apr;216(2-3):328–333. doi: 10.1007/BF00334372. [DOI] [PubMed] [Google Scholar]
- 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]
- Stewart B. R., Merriam J. R. Segmental aneuploidy and enzyme activity as a method for cytogenetic localization in drosophila melanogaster. Genetics. 1974 Feb;76(2):301–309. doi: 10.1093/genetics/76.2.301. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Talbert P. B., LeCiel C. D., Henikoff S. Modification of the Drosophila heterochromatic mutation brownDominant by linkage alterations. Genetics. 1994 Feb;136(2):559–571. doi: 10.1093/genetics/136.2.559. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tearle R. G., Belote J. M., McKeown M., Baker B. S., Howells A. J. Cloning and characterization of the scarlet gene of Drosophila melanogaster. Genetics. 1989 Jul;122(3):595–606. doi: 10.1093/genetics/122.3.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whatley S. A., Hall C., Davison A. N., Lim L. Alterations in the relative amounts of specific mRNA species in the developing human brain in Down's syndrome. Biochem J. 1984 May 15;220(1):179–187. doi: 10.1042/bj2200179. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Zachar Z., Bingham P. M. Regulation of white locus expression: the structure of mutant alleles at the white locus of Drosophila melanogaster. Cell. 1982 Sep;30(2):529–541. doi: 10.1016/0092-8674(82)90250-1. [DOI] [PubMed] [Google Scholar]
- Zlatanova J., Van Holde K. Histone H1 and transcription: still an enigma? J Cell Sci. 1992 Dec;103(Pt 4):889–895. doi: 10.1242/jcs.103.4.889. [DOI] [PubMed] [Google Scholar]