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Genome-wide analysis of SU(VAR)3-9 distribution in chromosomes of Drosophila melanogaster

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Abstract

Histone modifications represent one of the key factors contributing to proper genome regulation. One of histone modifications involved in gene silencing is methylation of H3K9 residue. Present in the chromosomes across different eukaryotes, this epigenetic mark is controlled by SU(VAR)3-9 and its orthologs. Despite SU(VAR)3-9 was discovered over two decades ago, little is known about the details of its chromosomal distribution pattern. To fill in this gap, we used DamID-seq approach and obtained high-resolution genome-wide profiles for SU(VAR)3-9 in two somatic (salivary glands and brain ganglia) and two germline (ovarian nurse cells and testes) tissues of Drosophila melanogaster. Analysis of tissue and developmental expression of SU(VAR)3-9-bound genes indicates that in the somatic tissues tested, as well as in the ovarian nurse cells, SU(VAR)3-9 tends to associate with transcriptionally silent genes. In contrast, in the testes, SU(VAR)3-9 shows preferential association with testis-specific genes, and its binding appears dynamic during spermatogenesis. In somatic cells, the mere presence/absence of SU(VAR)3-9 binding correlates with lower/higher expression. No such correlation is found in the male germline. Interestingly, transcription units in piRNA clusters (particularly flanks thereof) are frequently targeted by SU(VAR)3-9, and Su(var)3-9 mutation affects the expression of select piRNA species. Our analyses suggest a context-dependent role of SU(VAR)3-9. In euchromatin, SU(VAR)3-9 may serve to fine-tune the expression of individual genes, whereas in heterochromatin, chromosome 4, and piRNA clusters, it may act more broadly over large chromatin domains.

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Abbreviations

BR-F:

brain tissue of female larvae

BR-M:

brain tissue of male larvae

SG-F:

larval salivary glands (female)

SG-M:

larval salivary glands (male)

NC:

ovarian nurse cells

TS-aly:

testes from aly mutants

TS-can:

testes from can mutants

TS-bam:

testes from bam mutants

TS-WT:

wild-type testes

TE:

transposable elements

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Acknowledgements

The authors are grateful to Dr. A. Gorchakov for useful comments and translating manuscript. DNA sequencing was performed by the “Molecular and cellular biology” facility at IMCB SB RAS.

Funding

This work was supported by the grants from the Russian Foundation for Basic Research (12-04-00160 and 15-04-02264) and from the Russian Programme for Basic Research (0310-2016-0005). Bioinformatic analysis of the sequencing data of the testes samples was supported by the grant from the Russian Science Foundation (14-14-00641).

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  1. Daniil A. Maksimov and Petr P. Laktionov contributed equally to this work.

Authors and Affiliations

  1. Institute of Molecular and Cellular Biology, Novosibirsk, 630090, Russia

    Daniil A. Maksimov, Petr P. Laktionov, Olga V. Posukh, Stepan N. Belyakin & Dmitry E. Koryakov

  2. Novosibirsk State University, Novosibirsk, 630090, Russia

    Stepan N. Belyakin & Dmitry E. Koryakov

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  1. Daniil A. Maksimov
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  2. Petr P. Laktionov
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  3. Olga V. Posukh
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Correspondence to Dmitry E. Koryakov.

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This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Availability of data: Sequences of the DNA constructs are available under GenBank accession numbers JN993988, KY615608, KY615609, and KY615610. DamID-seq profiles have been deposited in the GEO under accession number GSE97351. RNA-seq data are available at the GEO database under accession number GSE97130.

Electronic supplementary material

Figure S1

General view of SU(VAR)3-9 binding profiles (colored, obtained in this study) in the chromosomes from all the samples, as well as SU(VAR)3-9 DamID-chip data (Kc cells) from Filion et al. (2010), SU(VAR)3-9 ChIP-seq data from modENCODE (L3 – third instar larvae, G. Karpen, ID5128), and H3K9me2 ChIP-chip data (salivary glands) from Figueiredo et al. (2012) (black). PH – pericentric heterochromatin; 31B-E, 39D-E, 42A-B – chromosome regions in salivary gland polytene chromosomes 2L and 2R. Significance of binding of SU(VAR)3-9-Dam (values above X axis) or Dam (values below X axis) in the range from 0 to 1017 is plotted on the Y axis (colored profiles). Y axis on the black profiles shows log2 (IP/input) values. Black horizontal lines denote threshold p-value corresponding to the FDR < 5%. Genomic coordinates on the X axis correspond to the BDGP Release 6. (JPEG 186 kb) (JPEG 191 kb)

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Figure S2

Binding of SU(VAR)3-9 to repetitive sequences. Fraction of reads corresponding to the 359-bp satellite, telomeric retrotransposons TART and TAHRE and TE 1360 (hoppel) among all the raw reads obtained for female larval brain ganglia. (JPEG 28 kb)

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Figure S3

Correlation between SU(VAR)3-9 binding and the presence of H3K9me2, H3K9me3, and H3K27me3 marks. Significance of binding (p) of SU(VAR)3-9-Dam (righthand) or Dam (lefthand) ranging from 0 to 1015 is plotted on the X axis. Y axis shows enrichment of the same region with methylated H3K9 or H3K27 mark, as inferred from the ChIP-chip data (Figueiredo et al. 2012; Sher et al. 2012). (JPEG 90 kb)

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Figure S4

Distribution of SU(VAR)3-9 in underrepresented regions of heterochromatin in polytene chromosomes. Pericentric heterochromatin in proximal-most region of 3R euchromatin in the chromosomes of nurse cells (NC), female larval brain ganglia (BR-F) and female larval salivary gland (SG-F). In salivary gland chromosomes, most of the peaks cluster in the distal heterochromatin, i.e. they are generally found in its polytenized part (Yarosh and Spradling 2014) (bottom image). In contrast, most of the DNA sequences mapping to the proximal heterochromatin are severely underreplicated in salivary glands and are therefore lost from analysis. Significance of SU(VAR)3-9 binding ranges from 0 to 1050 (Y axis). Bottom image shows replication profile, wherein 100% correspond to the genome-wide modal value of polytenization in salivary glands. Genomic coordinates indicated on the X axis correspond to the BDGP Release 6. (JPEG 76 kb)

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Figure S5

Fractions of TEs and genes among all SU(VAR)3-9-positive GATC-fragments in the heterochromatin (A-het) and euchromatin (A-eu) of autosomes. (JPEG 59 kb)

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Figure S6

Distribution of SU(VAR)3-9 within protein-coding genes and in genes of lncRNA. Significant (p < 0.01) enrichment or depletion of various portions of euchromatic genes and intergenic spacers with SU(VAR)3-9-bound GATC-fragments, compared to the genome average in the salivary glands (SG, male and female profiles combined), larval brain ganglia (BR, male and female profiles combined), testes (TS, wild-type and bam, aly, can mutant profiles combined) and nurse cells (NC). Bottom left of the image features enrichment of lncRNA targets in the Y-chromosome – in the testes (TS) and male larval brains (BR-M). Significance levels are shown near each bar, those below 0.01 are colored in red. (JPEG 57 kb)

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Figure S7

Distribution of SU(VAR)3-9-bound GATC-fragments within sls, Msp300, SK, and par-1 genes in different tissues. Significance of SU(VAR)3-9 binding is plotted on the Y axis and ranges from 0 to 1017. Coordinates shown on the X axis and positions of exons and introns correspond to the BDGP Release 6. (JPEG 299 kb)

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Figure S8

Expression clustering of SU(VAR)3-9-associated genes throughout fly development. E0-2 – E22-24 – embryos (hrs); L1 – L3 - larval stages; L3PS1-2 – L3PS7-9 – puff stages in the salivary glands of third instar larvae; WPP – white prepupae; P6 – P15 – pupal stages; Ad_F and Ad_M – adult females and males (days). modENCODE Temporal Expression Data (Graveley et al. 2011) and clustering software Gene Cluster 3.0 (de Hoon et al. 2004) were used for clustering analysis. Expression levels are shown as a log2 scale. Brackets denote gene clusters sharing testis-specific expression profile, asterisk denotes ovary-specific genes (Arbeitman et al. 2002). (JPEG 644 kb)

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Figure S9

Dynamic binding of SU(VAR)3-9 in testes. Binding of SU(VAR)3-9 with protein-coding (a, b) and lncRNA-coding (c, d) genes in the chromosomes from wild-type (WT) and mutant (bam, aly, and can) testes. Venn-diagrams (a, c) show the genes shared by different samples, and adjacent schemes (b, d) display changes in gene targets upon “transition” from one genotype to another. Shown are the numbers of genes that remain bound, lose or acquire SU(VAR)3-9 binding. (JPEG 129 kb)

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Figure S10

SU(VAR)3-9 peak densities in piRNA clusters. Average peak densities (peaks/Mb) in 84 piRNA clusters (Table S5) and in the the Su(Ste) locus (Y: 869892-1040412), measured in the larval brain ganglia and germline cells. (JPEG 40 kb)

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Maksimov, D.A., Laktionov, P.P., Posukh, O.V. et al. Genome-wide analysis of SU(VAR)3-9 distribution in chromosomes of Drosophila melanogaster . Chromosoma 127, 85–102 (2018). https://doi.org/10.1007/s00412-017-0647-4

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