A Reexamination of Spreading of Position-Effect Variegation in the white-roughest Region of Drosophila melanogaster

Corresponding author: Steven Henikoff, Fred Hutchinson Cancer Research Center and Howard Hughes Medical Institute, 1100 Fairview Ave. N, A1-162, Seattle, WA 98109-1024., steveh{at}fhcrc.org (E-mail)

Communicating editor: R. S. HAWLEY

In Drosophila, heterochromatin causes mosaic silencing of euchromatic genes brought next to it by chromosomal rearrangements. Silencing has been observed to "spread": genes closer to the heterochromatic rearrangement breakpoint are silenced more frequently than genes farther away. We have examined silencing of the white and roughest genes in the variegating rearrangements In(1)w^m4, In(1)w^mMc, and In(1)w^m51b. Eleven stocks bearing these chromosomes differ widely in the strength of silencing of white and roughest. Stock-specific differences in the relative frequencies of inactivation of white and roughest were found that map to the white-roughest region or the adjacent heterochromatin. Most stock-specific differences did not correlate with gross differences in the heterochromatic content of the rearranged chromosomes; however, two stocks, In(1)w^m51b and In(1)w^mMc, were found to have anomalous additional heterochromatin that may act in trans to suppress variegating alleles. In comparing different stocks, the frequency of silencing of the roughest gene, which is more distant from heterochromatin, does not correlate with the frequency of silencing of the more proximal white gene on the same chromosome, in contradiction to the expectation of models of continuous linear propagation of silencing. We frequently observed rough eye tissue that is pigmented, as though an active white gene is skipped.

This article has been cited by other articles:

				N. C. Riddle, W. Leung, K. A. Haynes, H. Granok, J. Wuller, and S. C. R. Elgin An Investigation of Heterochromatin Domains on the Fourth Chromosome of Drosophila melanogaster Genetics, March 1, 2008; 178(3): 1177 - 1191. [Abstract] [Full Text] [PDF]

				D. V. Irvine, M. Zaratiegui, N. H. Tolia, D. B. Goto, D. H. Chitwood, M. W. Vaughn, L. Joshua-Tor, and R. A. Martienssen Argonaute slicing is required for heterochromatic silencing and spreading. Science, August 25, 2006; 313(5790): 1134 - 1137. [Abstract] [Full Text] [PDF]

				M. Bulger Hyperacetylated Chromatin Domains: Lessons from Heterochromatin J. Biol. Chem., June 10, 2005; 280(23): 21689 - 21692. [Abstract] [Full Text] [PDF]

				B. T. Sage, J. L. Jones, A. L. Holmes, M. D. Wu, and A. K. Csink Sequence Elements in cis Influence Heterochromatic Silencing in trans Mol. Cell. Biol., January 1, 2005; 25(1): 377 - 388. [Abstract] [Full Text] [PDF]

				J. R. Danzer and L. L. Wallrath Mechanisms of HP1-mediated gene silencing in Drosophila Development, August 1, 2004; 131(15): 3571 - 3580. [Abstract] [Full Text] [PDF]

				F. Greil, I. van der Kraan, J. Delrow, J. F. Smothers, E. de Wit, H. J. Bussemaker, R. van Driel, S. Henikoff, and B. van Steensel Distinct HP1 and Su(var)3-9 complexes bind to sets of developmentally coexpressed genes depending on chromosomal location Genes & Dev., November 15, 2003; 17(22): 2825 - 2838. [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]

				E. S. Belyaeva, L. V. Boldyreva, E. I. Volkova, R. A. Nanayev, A. A. Alekseyenko, and I. F. Zhimulev Effect of the Suppressor of Underreplication (SuUR) Gene on Position-Effect Variegation Silencing in Drosophila melanogaster Genetics, November 1, 2003; 165(3): 1209 - 1220. [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]

				K. A. Maggert and G. H. Karpen The Activation of a Neocentromere in Drosophila Requires Proximity to an Endogenous Centromere Genetics, August 1, 2001; 158(4): 1615 - 1628. [Abstract] [Full Text] [PDF]

				E. Lebrun, E. Revardel, C. Boscheron, R. Li, E. Gilson, and G. Fourel Protosilencers in Saccharomyces cerevisiae Subtelomeric Regions Genetics, May 1, 2001; 158(1): 167 - 176. [Abstract] [Full Text]

				F.-L. Sun, M. H. Cuaycong, and S. C. R. Elgin Long-Range Nucleosome Ordering Is Associated with Gene Silencing in Drosophila melanogaster Pericentric Heterochromatin Mol. Cell. Biol., April 15, 2001; 21(8): 2867 - 2879. [Abstract] [Full Text]

				M Delattre, A Spierer, C. Tonka, and P Spierer The genomic silencing of position-effect variegation in Drosophila melanogaster: interaction between the heterochromatin-associated proteins Su(var)3-7 and HP1 J. Cell Sci., January 12, 2000; 113(23): 4253 - 4261. [Abstract] [PDF]

				O. L. Moritz, B. M. Tam, D. S. Papermaster, and T. Nakayama A Functional Rhodopsin-Green Fluorescent Protein Fusion Protein Localizes Correctly in Transgenic Xenopus laevis Retinal Rods and Is Expressed in a Time-dependent Pattern J. Biol. Chem., July 20, 2001; 276(30): 28242 - 28251. [Abstract] [Full Text] [PDF]