skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: The composition and organization of Drosophila heterochromatin are heterogeneous and dynamic

Abstract

Heterochromatin is enriched for specific epigenetic factors including Heterochromatin Protein 1a (HP1a), and is essential for many organismal functions. To elucidate heterochromatin organization and regulation, we purified Drosophila melanogaster HP1a interactors, and performed a genome-wide RNAi screen to identify genes that impact HP1a levels or localization. The majority of the over four hundred putative HP1a interactors and regulators identified were previously unknown. We found that 13 of 16 tested candidates (83%) are required for gene silencing, providing a substantial increase in the number of identified components that impact heterochromatin properties. Surprisingly, image analysis revealed that although some HP1a interactors and regulators are broadly distributed within the heterochromatin domain, most localize to discrete subdomains that display dynamic localization patterns during the cell cycle. We conclude that heterochromatin composition and architecture is more spatially complex and dynamic than previously suggested, and propose that a network of subdomains regulates diverse heterochromatin functions.

Authors:
 [1];  [1];  [2];  [1];  [2]
  1. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
National Institutes of Health (NIH); USDOE
OSTI Identifier:
1379562
Grant/Contract Number:
AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
eLife
Additional Journal Information:
Journal Volume: 5; Journal ID: ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Swenson, Joel M., Colmenares, Serafin U., Strom, Amy R., Costes, Sylvain V., and Karpen, Gary H. The composition and organization of Drosophila heterochromatin are heterogeneous and dynamic. United States: N. p., 2016. Web. doi:10.7554/eLife.16096.001.
Swenson, Joel M., Colmenares, Serafin U., Strom, Amy R., Costes, Sylvain V., & Karpen, Gary H. The composition and organization of Drosophila heterochromatin are heterogeneous and dynamic. United States. doi:10.7554/eLife.16096.001.
Swenson, Joel M., Colmenares, Serafin U., Strom, Amy R., Costes, Sylvain V., and Karpen, Gary H. 2016. "The composition and organization of Drosophila heterochromatin are heterogeneous and dynamic". United States. doi:10.7554/eLife.16096.001. https://www.osti.gov/servlets/purl/1379562.
@article{osti_1379562,
title = {The composition and organization of Drosophila heterochromatin are heterogeneous and dynamic},
author = {Swenson, Joel M. and Colmenares, Serafin U. and Strom, Amy R. and Costes, Sylvain V. and Karpen, Gary H.},
abstractNote = {Heterochromatin is enriched for specific epigenetic factors including Heterochromatin Protein 1a (HP1a), and is essential for many organismal functions. To elucidate heterochromatin organization and regulation, we purified Drosophila melanogaster HP1a interactors, and performed a genome-wide RNAi screen to identify genes that impact HP1a levels or localization. The majority of the over four hundred putative HP1a interactors and regulators identified were previously unknown. We found that 13 of 16 tested candidates (83%) are required for gene silencing, providing a substantial increase in the number of identified components that impact heterochromatin properties. Surprisingly, image analysis revealed that although some HP1a interactors and regulators are broadly distributed within the heterochromatin domain, most localize to discrete subdomains that display dynamic localization patterns during the cell cycle. We conclude that heterochromatin composition and architecture is more spatially complex and dynamic than previously suggested, and propose that a network of subdomains regulates diverse heterochromatin functions.},
doi = {10.7554/eLife.16096.001},
journal = {eLife},
number = ,
volume = 5,
place = {United States},
year = 2016,
month = 8
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Save / Share:
  • Heterochromatin is enriched for specific epigenetic factors including Heterochromatin Protein 1a (HP1a), and is essential for many organismal functions. To elucidate heterochromatin organization and regulation, we purified Drosophila melanogaster HP1a interactors, and performed a genome-wide RNAi screen to identify genes that impact HP1a levels or localization. The majority of the over four hundred putative HP1a interactors and regulators identified were previously unknown. We found that 13 of 16 tested candidates (83%) are required for gene silencing, providing a substantial increase in the number of identified components that impact heterochromatin properties. Surprisingly, image analysis revealed that although some HP1a interactors andmore » regulators are broadly distributed within the heterochromatin domain, most localize to discrete subdomains that display dynamic localization patterns during the cell cycle. We conclude that heterochromatin composition and architecture is more spatially complex and dynamic than previously suggested, and propose that a network of subdomains regulates diverse heterochromatin functions.« less
  • Heterochromatin is enriched for specific epigenetic factors including Heterochromatin Protein 1a (HP1a), and is essential for many organismal functions. To elucidate heterochromatin organization and regulation, we purified Drosophila melanogaster HP1a interactors, and performed a genome-wide RNAi screen to identify genes that impact HP1a levels or localization. The majority of the over four hundred putative HP1a interactors and regulators identified were previously unknown. We found that 13 of 16 tested candidates (83%) are required for gene silencing, providing a substantial increase in the number of identified components that impact heterochromatin properties. Surprisingly, image analysis revealed that although some HP1a interactors andmore » regulators are broadly distributed within the heterochromatin domain, most localize to discrete subdomains that display dynamic localization patterns during the cell cycle. We conclude that heterochromatin composition and architecture is more spatially complex and dynamic than previously suggested, and propose that a network of subdomains regulates diverse heterochromatin functions.« less
  • Heterochromatin is enriched for specific epigenetic factors including Heterochromatin Protein 1a (HP1a), and is essential for many organismal functions. To elucidate heterochromatin organization and regulation, we purified Drosophila melanogaster HP1a interactors, and performed a genome-wide RNAi screen to identify genes that impact HP1a levels or localization. The majority of the over four hundred putative HP1a interactors and regulators identified were previously unknown. We found that 13 of 16 tested candidates (83%) are required for gene silencing, providing a substantial increase in the number of identified components that impact heterochromatin properties. Surprisingly, image analysis revealed that although some HP1a interactors andmore » regulators are broadly distributed within the heterochromatin domain, most localize to discrete subdomains that display dynamic localization patterns during the cell cycle. We conclude that heterochromatin composition and architecture is more spatially complex and dynamic than previously suggested, and propose that a network of subdomains regulates diverse heterochromatin functions.« less
  • It is shown that, although no compaction of paracentromeric heterochromatin occurs during the first cleavage division in Drosophila melanogaster, the frequency of mitotic crossing-over in corresponding chromosome regions is increased, as compared to that in euchromatin. Because a similar situation is observed at later stages of Drosophila development, at which compact chromatin regions become well-manifested, it is concluded that the effect of heterochromatin on the frequency of crossing-over does not depend on its packing. A positive correlation between crossing-over events in paracentromeric heterochromatin and euchromatin was observed. This effect is probably due to the formation of a continuous region ofmore » somatic synapsis, which facilitates the process of mitotic crossing-over. On this basis, it is proposed that the effect of heterochromatin on mitotic crossing-over is associated with preferential chromosome pairing in the corresponding regions. 10 refs., 1 fig.« less
  • The classical phenomenon of position-effect variegation (PEV) is the mosaic expression that occurs when a chromosomal rearrangements moves a euchromatic gene near heterochromatin. A striking feature of this phenomenon is that genes far away from the junction with heterochromatin can be affected, as if the heterochromatic state {open_quotes}spreads.{close_quotes} We have investigated classical PEV of a Drosophila brown transgene affected by a heterochromatic junction {approximately} 60 kb away. PEV was enhanced when the transgene was locally duplicated using P transposase. Successive rounds of P transpose mutagenesis and phenotypic selection produced a series of PEV alleles with differences in phenotype that dependedmore » on transgene copy number and orientation. As for other examples of classical PEV, nearby heterochromatin was required for gene silencing. Modifications of classical PEV by alterations at a single site are unexpected, and these observations contradict models for spreading that invoke propagation of heterochromatin along the chromosome. Rather, our results support a model in which local alterations affect the affinity of a gene region for nearby heterochromatin via homology-based pairing, suggesting an alternative explanation for this 65-year-old phenomenon. 63 refs., 6 figs., 1 tab.« less