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Various modes of HP1a interactions with the euchromatic chromosome arms in Drosophila ovarian somatic cells

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Abstract

Heterochromatin protein 1a (HP1a) is a well-known component of pericentromeric and telomeric heterochromatin in Drosophila. However, its role and the mechanisms of its binding in the chromosome arms (ChAs) remain largely unclear. Here, we identified HP1a-interacting domains in the somatic cells of Drosophila ovaries using a DamID-seq approach and compared them with insertion sites of transposable elements (TEs) revealed by genome sequencing. Although HP1a domains cover only 13% of ChAs, they non-randomly associate with 42% of TE insertions. Furthermore, HP1a on average propagates at 2-kb distances from the TE insertions. These data confirm the role of TEs in formation of HP1a islands in ChAs. However, only 18% of HP1a domains have adjacent TEs, indicating the existence of other mechanisms of HP1a domain formation besides spreading from TEs. In particular, many TE-independent HP1a domains correspond to the regions attached to the nuclear pore complexes (NPCs) or contain active gene promoters. However, HP1a occupancy on the promoters does not significantly influence expression of corresponding genes. At the same time, the steady-state transcript level of many genes located outside of HP1a domains was altered upon HP1a knockdown in the somatic cells of ovaries, thus pointing to the strong indirect effect of HP1a depletion. Collectively, our results support an existence of at least three different mechanisms of HP1a domain emergence in ChAs: spreading from TE insertions, transient interactions with the chromatin located near NPCs, and targeting to the promoters of moderately expressed genes.

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Data availability

Raw and processed HP1a-DamID-seq data in ovaries and RNA-seq data in ovaries upon HP1a-SKD were deposited in the NCBI Gene Expression Omnibus (GEO) under the accession number GSE132756. Sequencing data for Drosophila genome were deposited in the NCBI SRA Database (SRR9305781). All other data generated during the current study are included in the article and its supplementary information files, or available from the corresponding authors on reasonable request.

Abbreviations

ChA:

Chromosome arm

H3K9me2/3:

Histone H3 di/tri methylated at lysine 9

HMM:

Hidden Markov model

HP1:

Heterochromatin protein 1

LTR:

Long terminal repeat

M-W:

Mann-Whitney

NPC:

Nuclear pore complex

OSCs:

Ovarian somatic cells

Pc:

Polycomb

Pol II:

RNA-polymerase II

PRE:

Polycomb response element

SKD:

Somatic knockdown

TE:

Transposable element

TSS:

Transcription start site

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Acknowledgments

We thank Maria Logacheva and Aleksey Penin (Lomonosov Moscow State University) for sequencing of Drosophila genome; the Center of Common Scientific Equipment of the Institute of Molecular Genetics, RAS, for providing access to the confocal microscope; Dr. Alexei V. Pindyurin (IMCB SB RAS), Prof. Fanglin Sun (Tsinghua University, School of Medicine), and the Bloomington Drosophila Stock Center for the fly stocks; Prof. Sarah Elgin (Washington University in St. Louis) for anti-HP1a antibodies and Prof. Paul Fisher (Stony Brook University School of Medicine) for anti-Lamin Dm0 antibodies.

Funding

This research was funded by Russian Foundation for Basic Research Grant No. 18-34-00140 to AAI. A part of the work related to the characteristic of somatic HP1a knockdown was funded by Russian Foundation for Basic Research Grant No. 19-04-01307 to MSK.

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  1. Department of Molecular Genetics of Cell, Institute of Molecular Genetics, Russian Academy of Sciences, Kurchatov Sq. 2, Moscow, Russia, 123182

    Artem A. Ilyin, Anastasia D. Stolyarenko, Mikhail S. Klenov & Yuri Y. Shevelyov

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  1. Artem A. Ilyin
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  2. Anastasia D. Stolyarenko
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  3. Mikhail S. Klenov
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  4. Yuri Y. Shevelyov
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MSK and YYS conceived and designed the experiments; AAI, ADS, and YYS performed the experiments; AAI with participation of MSK and YYS analyzed the data; MSK and YYS wrote the paper.

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Correspondence to Mikhail S. Klenov or Yuri Y. Shevelyov.

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Ilyin, A.A., Stolyarenko, A.D., Klenov, M.S. et al. Various modes of HP1a interactions with the euchromatic chromosome arms in Drosophila ovarian somatic cells. Chromosoma 129, 201–214 (2020). https://doi.org/10.1007/s00412-020-00738-5

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