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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. Thu . "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 = {Thu Aug 11 00:00:00 EDT 2016},
month = {Thu Aug 11 00:00:00 EDT 2016}
}

Journal Article:
Free Publicly Available Full Text
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  • 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
    Cited by 7
  • 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
    Cited by 7
  • New rudimentary (r) mutants have been isolated following mutagenesis with ethyl methanesulfonate (r/sup LE/), ICR-170 (r/sup LI/) and x rays (r/sup LX/). From wing phenotype measurements on homoallelic females, it has been shown that the r/sup LE/ mutant series includes several leaky alleles, as well as alleles that produce moderate and strong r phenotypes. All of the tested r/sup LI/ alleles yielded strong r phenotypes in homoallelic females, whereas the r/sup LX/ series was found to include both moderate and strong alleles. Based on allele complementation for the wing phenotype, it was found that all three mutant series include bothmore » complementing and noncomplementing alleles, but the relative frequencies of these two types of alleles differ considerably among the three series. Complementing alleles comprise most of the r/sup LE/ mutant series (19 of 25) and almost one-half of the r/sup LX/ series (five of 12), while only one of 16 r/sup LI/ mutants is a complementing allele. Data from enzyme assays of mutants mostly support the direct correlation of genetic complementation units with the activities of the first three enzymes in the de novo pyrimidine biosynthetic pathway. All of these findings are discussed in light of evidence that these three enzymes are contained within a trienzyme complex in animals. We conclude that the available genetic evidence supports the contention that the trienzyme complex is encoded by a single mRNA.« 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