, Volume 127, Issue 1, pp 85–102 | Cite as

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

  • Daniil A. Maksimov
  • Petr P. Laktionov
  • Olga V. Posukh
  • Stepan N. Belyakin
  • Dmitry E. KoryakovEmail author
Original Article


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.


Drosophila SU(VAR)3-9 SETDB1 piRNA Transcription Spermatogenesis 



brain tissue of female larvae


brain tissue of male larvae


larval salivary glands (female)


larval salivary glands (male)


ovarian nurse cells


testes from aly mutants


testes from can mutants


testes from bam mutants


wild-type testes


transposable elements



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.


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).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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

Supplementary material

412_2017_647_Fig7_ESM.jpg (192 kb)
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)

412_2017_647_MOESM1_ESM.eps (3.8 mb)
High-resolution image (EPS 3917 kb)
412_2017_647_Fig8_ESM.jpg (187 kb)

(JPEG 186 kb)

412_2017_647_MOESM2_ESM.eps (4.7 mb)
High-resolution image (EPS 4762 kb)
412_2017_647_Fig9_ESM.jpg (160 kb)

(JPEG 159 kb)

412_2017_647_MOESM3_ESM.eps (4.6 mb)
High-resolution image (EPS 4686 kb)
412_2017_647_Fig10_ESM.jpg (162 kb)

(JPEG 162 kb)

412_2017_647_MOESM4_ESM.eps (4.5 mb)
High-resolution image (EPS 4639 kb)
412_2017_647_Fig11_ESM.jpg (175 kb)

(JPEG 174 kb)

412_2017_647_MOESM5_ESM.eps (2.9 mb)
High-resolution image (EPS 3006 kb)
412_2017_647_Fig12_ESM.jpg (203 kb)

(JPEG 202 kb)

412_2017_647_MOESM6_ESM.eps (3.7 mb)
High-resolution image (EPS 3756 kb)
412_2017_647_Fig13_ESM.jpg (108 kb)

(JPEG 107 kb)

412_2017_647_MOESM7_ESM.eps (1.5 mb)
High-resolution image (EPS 1577 kb)
412_2017_647_Fig14_ESM.jpg (29 kb)
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)

412_2017_647_MOESM8_ESM.eps (222 kb)
High-resolution image (EPS 221 kb)
412_2017_647_Fig15_ESM.jpg (90 kb)
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)

412_2017_647_MOESM9_ESM.eps (421 kb)
High-resolution image (EPS 420 kb)
412_2017_647_Fig16_ESM.jpg (77 kb)
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)

412_2017_647_MOESM10_ESM.eps (1018 kb)
High-resolution image (EPS 1018 kb)
412_2017_647_Fig17_ESM.jpg (60 kb)
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)

412_2017_647_MOESM11_ESM.eps (210 kb)
High-resolution image (EPS 210 kb)
412_2017_647_Fig18_ESM.jpg (58 kb)
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)

412_2017_647_MOESM12_ESM.eps (319 kb)
High-resolution image (EPS 318 kb)
412_2017_647_Fig19_ESM.jpg (300 kb)
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)

412_2017_647_MOESM13_ESM.eps (2 mb)
High-resolution image (EPS 2027 kb)
412_2017_647_Fig20_ESM.jpg (645 kb)
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)

412_2017_647_MOESM14_ESM.eps (19.2 mb)
High-resolution image (EPS 19688 kb)
412_2017_647_Fig21_ESM.jpg (130 kb)
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)

412_2017_647_MOESM15_ESM.eps (698 kb)
High-resolution image (EPS 698 kb)
412_2017_647_Fig22_ESM.jpg (40 kb)
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)

412_2017_647_MOESM16_ESM.eps (247 kb)
High-resolution image (EPS 247 kb)
412_2017_647_MOESM17_ESM.xls (268 kb)
ESM 1 (XLS 267 kb)


  1. Abad JP, de Pablos B, Osoegawa K, de Jong PJ, Martín-Gallardo A, Villasante A (2004) TAHRE, a novel telomeric retrotransposon from Drosophila melanogaster, reveals the origin of Drosophila telomeres. Mol Biol Evol 21:1620–1624CrossRefPubMedGoogle Scholar
  2. Andersson R, Enroth S, Rada-Iglesias A, Wadelius C, Komorowski J (2009) Nucleosomes are well positioned in exons and carry characteristic histone modifications. Genome Res 19:1732–1741CrossRefPubMedPubMedCentralGoogle Scholar
  3. Aravin AA, Naumova NM, Tulin AV, Vagin VV, Rozovsky YM, Gvozdev VA (2001) Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr Biol 11:1017–1027CrossRefPubMedGoogle Scholar
  4. Arbeitman MN, Furlong EEM, Imam F, Johnson E, Null BH, Baker BS, Krasnow MA, Scott MP, Davis RW, White KP (2002) Gene expression during the life cycle of Drosophila melanogaster. Science 297:2270–2275CrossRefPubMedGoogle Scholar
  5. Barski A, Cuddapah S, Cui K, Roh T-Y, Schones D, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129:823–837CrossRefPubMedGoogle Scholar
  6. Brennecke J, Aravin AA, Stark A, Dus M, Kellis M, Sachidanandam R, Hannon GJ (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128:1089–1103CrossRefPubMedGoogle Scholar
  7. Brinkman AB, Roelofsen T, Pennings SW, Martens JH, Jenuwein T, Stunnenberg HG (2006) Histone modification patterns associated with the human X chromosome. EMBO Rep 7:628–634PubMedPubMedCentralGoogle Scholar
  8. Brower-Toland B, Riddle NC, Jiang H, Huisinga KL, Elgin SCR (2009) Multiple SET methyltransferases are required to maintain normal heterochromatin domains in the genome of Drosophila melanogaster. Genetics 181:1303–1319CrossRefPubMedPubMedCentralGoogle Scholar
  9. Brown JB, Boley N, Eisman R et al (2014) Diversity and dynamics of the Drosophila transcriptome. Nature 512:393–399CrossRefPubMedPubMedCentralGoogle Scholar
  10. Clough E, Moon W, Wang S, Smith K, Hazelrigg T (2007) Histone methylation is required for oogenesis in Drosophila. Development 134:157–165CrossRefPubMedGoogle Scholar
  11. de Hoon MJL, Imoto S, Nolan J, Miyano S (2004) Open source clustering software. Bioinformatics 20:1453–1454CrossRefPubMedGoogle Scholar
  12. Doggett K, Jiang J, Aleti G, White-Cooper H (2011) Wake-up-call, a lin-52 paralogue, and Always early, a lin-9 homologue physically interact, but have opposing functions in regulating testis-specific gene expression. Dev Biol 355:381–393CrossRefPubMedPubMedCentralGoogle Scholar
  13. Figueiredo ML, Philip P, Stenberg P, Larsson J (2012) HP1a recruitment to promoters is independent of H3K9 methylation in Drosophila melanogaster. PLoS Genet 8:e1003061CrossRefPubMedPubMedCentralGoogle Scholar
  14. Filion GJ, van Bemmel JG, Braunschweig U et al (2010) Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143:212–224CrossRefPubMedPubMedCentralGoogle Scholar
  15. Firestein R, Cui X, Huie P, Cleary ML (2000) Set domain-dependent regulation of transcriptional silencing and growth control by SUV39H1, a mammalian ortholog of Drosophila Su(var)3-9. Mol Cell Biol 20:4900–4909CrossRefPubMedPubMedCentralGoogle Scholar
  16. Fritsch L, Robin P, Mathieu JR, Souidi M, Hinaux H, Rougeulle C, Harel-Bellan A, Ameyar-Zazoua M, Ait-Si-Ali S (2010) A subset of the histone H3 lysine 9 methyltransferases Suv39h1, G9a, GLP, and SETDB1 participate in a multimeric complex. Mol Cell 37:46–56CrossRefPubMedGoogle Scholar
  17. Glaser RL, Karpen GH, Spradling AC (1992) Replication forks are not found in a Drosophila minichromosome demonstrating a gradient of polytenization. Chromosoma 102:15–19CrossRefPubMedGoogle Scholar
  18. Graveley BR, Brooks AN, Carlson JW et al (2011) The developmental transcriptome of Drosophila melanogaster. Nature 471:473–479CrossRefPubMedGoogle Scholar
  19. Greil F, van der Kraan I, Delrow J, Smothers JF, de Wit E, Bussemaker HJ, van Driel R, Henikoff S, van Steensel B (2003) Distinct HP1 and Su(var)3-9 complexes bind to sets of developmentally coexpressed genes depending on chromosomal location. Genes Dev 17:2825–2838CrossRefPubMedPubMedCentralGoogle Scholar
  20. Haynes KA, Gracheva E, Elgin SCR (2007) A distinct type of heterochromatin within Drosophila melanogaster chromosome 4. Genetics 175:1539–1542CrossRefPubMedPubMedCentralGoogle Scholar
  21. Hon G, Wang W, Ren B (2009) Discovery and annotation of functional chromatin signatures in the human genome. PLoS Comput Biol 5:e1000566CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hsieh T, Brutlag D (1979) Sequence and sequence variation within the 1.688 g/cm3 satellite DNA of Drosophila melanogaster. J Mol Biol 135:465–481CrossRefPubMedGoogle Scholar
  23. Ivanova AV, Bonaduce MJ, Ivanov SV, Klar AJ (1998) The chromo and SET domains of the Clr4 protein are essential for silencing in fission yeast. Nat Genet 19:192–195CrossRefPubMedGoogle Scholar
  24. Kato Y, Kato M, Tachibana M, Shinkai Y, Yamaguchi M (2008) Characterization of Drosophila G9a in vivo and identification of genetic interactants. Genes Cells 13:703–722CrossRefPubMedGoogle Scholar
  25. Kharchenko PV, Alekseyenko AA, Schwartz YB et al (2011) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471:480–485CrossRefPubMedGoogle Scholar
  26. Kholodilov NG, Bolshakov VN, Blinov VM, Solovyov VV, Zhimulev IF (1988) Intercalary heterochromatin in Drosophila. III. Homology between DNA sequences from the Y chromosome, bases of polytene chromosome limbs, and chromosome 4 of D. melanogaster. Chromosoma 97:247–253CrossRefPubMedGoogle Scholar
  27. Klattenhoff C, Xi H, Li C et al (2009) The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 138:1137–1149CrossRefPubMedPubMedCentralGoogle Scholar
  28. Kolasinska-Zwierz P, Down T, Latorre I, Liu T, Liu XS, Ahringer J (2009) Differential chromatin marking of introns and expressed exons by H3K36me3. Nat Genet 41:376–381CrossRefPubMedPubMedCentralGoogle Scholar
  29. Koryakov DE, Domanitskaya EV, Belyakin SN, Zhimulev IF (2003) Abnormal tissue-dependent polytenization of a block of chromosome 3 pericentric heterochromatin in Drosophila melanogaster. J Cell Sci 116:1035–1044CrossRefPubMedGoogle Scholar
  30. Koryakov DE, Reuter G, Dimitri P, Zhimulev IF (2006) The SuUR gene influences the distribution of heterochromatic proteins HP1 and SU(VAR)3-9 on nurse cell polytene chromosomes of Drosophila melanogaster. Chromosoma 115:296–310CrossRefPubMedGoogle Scholar
  31. Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705CrossRefPubMedGoogle Scholar
  32. Krauss V (2008) Glimpses of evolution: heterochromatic histone H3K9 methyltransferases left its marks behind. Genetica 133:93–106CrossRefPubMedGoogle Scholar
  33. Laktionov PP, Maksimov DA, Andreeva EN, Shloma VV, Beliakin SN (2013) A genetic system for somatic and germinal lineage tracing in the Drosophila melanogaster gonads. Tsitologiia 55:185–189 (article in Russian)PubMedGoogle Scholar
  34. Laktionov PP, White-Cooper H, Maksimov DA, Beliakin SN (2014) Transcription factor comr acts as a direct activator in the genetic program controlling spermatogenesis in D. melanogaster. Mol Biol (Mosk) 48:153–165CrossRefGoogle Scholar
  35. Lee KS, Yoon J, Park JS, Kang YK (2010) Drosophila G9a is implicated in germ cell development. Insect Mol Biol 19:131–139CrossRefPubMedGoogle Scholar
  36. Luco RF, Allo M, Schor IE, Kornblihtt AR, Misteli T (2011) Epigenetics in alternative pre-mRNA splicing. Cell 144:16–26CrossRefPubMedPubMedCentralGoogle Scholar
  37. Lyko F, Maleszka R (2011) Insects as innovative models for functional studies of DNA methylation. Trends Genet 27:127–131CrossRefPubMedGoogle Scholar
  38. Maksimov DA, Koryakov DE, Belyakin SN (2014) Developmental variation of the SUUR protein binding correlates with gene regulation and specific chromatin types in D. melanogaster. Chromosoma 123:253–264CrossRefPubMedGoogle Scholar
  39. Maksimov DA, Laktionov PP, Belyakin SN (2016) Data analysis algorithm for DamID-seq profiling of chromatin proteins in Drosophila melanogaster. Chromosom Res 24:481–494CrossRefGoogle Scholar
  40. Mis J, Ner SS, Grigliatti TA (2006) Identification of three histone methyltransferases in Drosophila: dG9a is a suppressor of PEV and is required for gene silencing. Mol Gen Genom 275:513–526CrossRefGoogle Scholar
  41. Mohn F, Sienski G, Handler D, Brennecke J (2014) The Rhino-Deadlock-Cutoff complex licenses noncanonical transcription of dual-strand piRNA clusters in Drosophila. Cell 157:1364–1379CrossRefPubMedGoogle Scholar
  42. Mulder MP, van Duijn P, Gloor HJ (1968) The replicative organization of DNA in polytene chromosomes of Drosophila hydei. Genetica 39:385–428CrossRefPubMedGoogle Scholar
  43. Nieto Moreno N, Giono LE, Cambindo Botto AE, Muñoz MJ, Kornblihtt AR (2015) Chromatin, DNA structure and alternative splicing. FEBS Lett 589:3370–3378CrossRefPubMedGoogle Scholar
  44. Nishida KM, Saito K, Mori T, Kawamura Y, Nagami-Okada T, Inagaki S, Siomi H, Siomi MC (2007) Gene silencing mechanisms mediated by Aubergine-piRNA complexes in Drosophila male gonad. RNA 13:1911–1922CrossRefPubMedPubMedCentralGoogle Scholar
  45. Penke TJR, McKay DJ, Strah BD, Matera AG, Duronio RJ (2016) Direct interrogation of the role of H3K9 in metazoan heterochromatin function. Genes Dev 30:1866–1880CrossRefPubMedPubMedCentralGoogle Scholar
  46. Peters AH, O'Carroll D, Scherthan H et al (2001) Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability. Cell 107:323–337CrossRefPubMedGoogle Scholar
  47. Pindyurin AV, Pagie L, Kozhevnikova EN, van Arensbergen J, van Steensel B (2016) Inducible DamID systems for genomic mapping of chromatin proteins in Drosophila. Nucleic Acids Res 44:5646–5657CrossRefPubMedPubMedCentralGoogle Scholar
  48. Quénerch’du E, Anand A, Kai T (2016) The piRNA pathway is developmentally regulated during spermatogenesis in Drosophila. RNA 22:1044–1054CrossRefPubMedPubMedCentralGoogle Scholar
  49. Rangan P, Malone CD, Navarro C, Newbold SP, Hayes PS, Sachidanandam R, Hannon GJ, Lehmann R (2011) piRNA production requires heterochromatin formation in Drosophila. Curr Biol 21:1373–1379CrossRefPubMedPubMedCentralGoogle Scholar
  50. Riddle NC, Minoda A, Kharchenko PV et al (2011) Plasticity in patterns of histone modifications and chromosomal proteins in Drosophila heterochromatin. Genome Res 21:147–163CrossRefPubMedPubMedCentralGoogle Scholar
  51. Rougeulle C, Chaumeil J, Sarma K, Allis CD, Reinberg D, Avner P, Heard E (2004) Differential histone H3 Lys-9 and Lys-27 methylation profiles on the X chromosome. Mol Cell Biol 24:5475–5484CrossRefPubMedPubMedCentralGoogle Scholar
  52. Saint-André V, Batsché E, Rachez C, Muchardt C (2011) Histone H3 lysine 9 trimethylation and HP1γ favor inclusion of alternative exons. Nat Struct Mol Biol 18:337–344CrossRefPubMedGoogle Scholar
  53. Schotta G, Ebert A, Krauss V, Fischer A, Hoffmann J, Rea S, Jenuwein T, Dorn R, Reuter G (2002) Central role of Drosophila SU(VAR)3-9 in histone H3-K9 methylation and heterochromatic gene silencing. EMBO J 21:1121–1131CrossRefPubMedPubMedCentralGoogle Scholar
  54. Schotta G, Ebert A, Reuter G (2003) SU(VAR)3-9 is a conserved key function in heterochromatic gene silencing. Genetica 117:149–158CrossRefPubMedGoogle Scholar
  55. Seum C, Bontron S, Reo E, Delattre M, Spierer P (2007b) Drosophila G9a is a nonessential gene. Genetics 177:1955–1957CrossRefPubMedPubMedCentralGoogle Scholar
  56. Seum C, Reo E, Peng H, Rauscher FJ 3rd, Spierer P, Bontron S (2007a) Drosophila SETDB1 is required for chromosome 4 silencing. PLoS Genet 3:e76CrossRefPubMedPubMedCentralGoogle Scholar
  57. Sher N, Bell GW, Li S, Nordman J, Eng T, Eaton ML, Macalpine DM, Orr-Weaver TL (2012) Developmental control of gene copy number by repression of replication initiation and fork progression. Genome Res 22:64–75CrossRefPubMedPubMedCentralGoogle Scholar
  58. Sienski G, Batki J, Senti KA, Dönertas D, Tirian L, Meixner K, Brennecke J (2015) Silencio/CG9754 connects the Piwi-piRNA complex to the cellular heterochromatin machinery. Genes Dev 29:2258–2271CrossRefPubMedPubMedCentralGoogle Scholar
  59. Tóth KF, Pezic D, Stuwe E, Webster A (2016) The piRNA pathway guards the germline genome against transposable elements. Adv Exp Med Biol 886:51–77CrossRefPubMedPubMedCentralGoogle Scholar
  60. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515CrossRefPubMedPubMedCentralGoogle Scholar
  61. Tschiersch B, Hofmann A, Krauss V, Dorn R, Korge G, Reuter G (1994) The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J 13:3822–3831PubMedPubMedCentralGoogle Scholar
  62. Tzeng TY, Lee CH, Chan LW, Shen CK (2007) Epigenetic regulation of the Drosophila chromosome 4 by the histone H3K9 methyltransferase dSETDB1. Proc Natl Acad Sci U S A 104:12691–12696CrossRefPubMedPubMedCentralGoogle Scholar
  63. Vakoc CR, Mandat SA, Olenchock BA, Blobel GA (2005) Histone H3 lysine 9 methylation and HP1gamma are associated with transcription elongation through mammalian chromatin. Mol Cell 19:381–391CrossRefPubMedGoogle Scholar
  64. Wen K, Yang L, Xiong T et al (2016) Critical roles of long noncoding RNAs in Drosophila spermatogenesis. Genome Res 26:1233–1244CrossRefPubMedPubMedCentralGoogle Scholar
  65. Whitcomb SJ, Basu A, Allis CD, Bernstein E (2007) Polycomb group proteins: an evolutionary perspective. Trends Genet 23:494–502CrossRefPubMedGoogle Scholar
  66. White-Cooper H (2010) Molecular mechanisms of gene regulation during Drosophila spermatogenesis. Reproduction 139:11–21CrossRefPubMedGoogle Scholar
  67. Yarosh W, Spradling AC (2014) Incomplete replication generates somatic DNA alterations within Drosophila polytene salivary gland cells. Genes Dev 28:1840–1855CrossRefPubMedPubMedCentralGoogle Scholar
  68. Yoon J, Lee KS, Park JS, Yu K, Paik SG, Kang YK (2008) dSETDB1 and SU(VAR)3-9 sequentially function during germline-stem cell differentiation in Drosophila melanogaster. PLoS One 3:e2234CrossRefPubMedPubMedCentralGoogle Scholar
  69. Zhang G, Huang H, Liu D et al (2015b) N6-methyladenine DNA modification in Drosophila. Cell 161:893–906CrossRefPubMedGoogle Scholar
  70. Zhang T, Cooper S, Brockdorff N (2015a) The interplay of histone modifications—writers that read. EMBO Rep 16:1467–1481CrossRefPubMedPubMedCentralGoogle Scholar
  71. Zhu X, Ma H, Chen Z (2011) Phylogenetics and evolution of Su(var)3-9 SET genes in land plants: rapid diversification in structure and function. BMC Evol Biol 11:63CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Daniil A. Maksimov
    • 1
  • Petr P. Laktionov
    • 1
  • Olga V. Posukh
    • 1
  • Stepan N. Belyakin
    • 1
    • 2
  • Dmitry E. Koryakov
    • 1
    • 2
    Email author
  1. 1.Institute of Molecular and Cellular BiologyNovosibirskRussia
  2. 2.Novosibirsk State UniversityNovosibirskRussia

Personalised recommendations