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Small RNAs, big impact: small RNA pathways in transposon control and their effect on the host stress response

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Abstract

Transposons are mobile genetic elements that are a major constituent of most genomes. Organisms regulate transposable element expression, transposition, and insertion site preference, mitigating the genome instability caused by uncontrolled transposition. A recent burst of research has demonstrated the critical role of small non-coding RNAs in regulating transposition in fungi, plants, and animals. While mechanistically distinct, these pathways work through a conserved paradigm. The presence of a transposon is communicated by the presence of its RNA or by its integration into specific genomic loci. These signals are then translated into small non-coding RNAs that guide epigenetic modifications and gene silencing back to the transposon. In addition to being regulated by the host, transposable elements are themselves capable of influencing host gene expression. Transposon expression is responsive to environmental signals, and many transposons are activated by various cellular stresses. TEs can confer local gene regulation by acting as enhancers and can also confer global gene regulation through their non-coding RNAs. Thus, transposable elements can act as stress-responsive regulators that control host gene expression in cis and trans.

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Abbreviations

dsDNA:

Double-stranded DNA

dsRNA:

Double-stranded RNA

HDAC:

Histone deacetylase

HMT:

Histone methyltransferase

LINE:

Long interspersed element

LTR:

Long terminal repeat

ncRNA:

Non-coding RNA

ORF:

Open reading frame

piRNA:

PIWI-interacting RNA

Pol II, IV, V:

RNA polymerase II, IV, V

RdDM:

RNA-dependent DNA methylation

RDRC:

RNA-directed RNA polymerase complex

RITS:

RNA-induced transcriptional silencing

RNAi:

RNA interference

SC:

Sperm cells

SINE:

Short interspersed element

siRNA:

Short interfering RNA

TE:

Transposable element

TIR:

Terminal inverted repeat

VN:

Vegetative nucleus

References

  • Allen TA, Von Kaenel S, Goodrich JA, Kugel JF (2004) The SINE-encoded mouse B2 RNA represses mRNA transcription in response to heat shock. Nat Struct Mol Biol 11:816–821

    PubMed  CAS  Google Scholar 

  • Allshire RC, Javerzat JP, Redhead NJ, Cranston G (1994) Position effect variegation at fission yeast centromeres. Cell 76:157–169

    PubMed  CAS  Google Scholar 

  • Anderson HE, Wardle J, Korkut SV et al (2009) The fission yeast HIRA histone chaperone is required for promoter silencing and the suppression of cryptic antisense transcripts. Mol Cell Biol 29:5158–5167

    PubMed  CAS  Google Scholar 

  • Aravin AA, Sachidanandam R, Girard A et al (2007) Developmentally regulated piRNA clusters implicate MILI in transposon control. Science 316:744–747

    PubMed  CAS  Google Scholar 

  • Aravin AA, Sachidanandam R, Bourc'his D et al (2008) A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31:785–799

    PubMed  CAS  Google Scholar 

  • Ashe A, Sapetschnig A, Weick E-M et al (2012) piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell 150:88–99

    PubMed  CAS  Google Scholar 

  • Bagijn MP, Goldstein LD, Sapetschnig A et al (2012) Function, targets, and evolution of Caenorhabditis elegans piRNAs. Science 337:574–578

    PubMed  CAS  Google Scholar 

  • Bartels D, Salamini F (2001) Desiccation tolerance in the resurrection plant Craterostigma plantagineum. A contribution to the study of drought tolerance at the molecular level. Plant Physiol 127:1346–1353

    PubMed  CAS  Google Scholar 

  • Batista PJ, Ruby JG, Claycomb JM et al (2008) PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol Cell 31:67–78

    PubMed  CAS  Google Scholar 

  • Beck CR, Garcia-Perez JL, Badge RM, Moran JV (2011) LINE-1 elements in structural variation and disease. Annu Rev Genomics Hum Genet 12:187–215

    PubMed  CAS  Google Scholar 

  • Behrens R, Hayles J, Nurse P (2000) Fission yeast retrotransposon Tf1 integration is targeted to 5′ ends of open reading frames. Nucleic Acids Res 28:4709–4716

    PubMed  CAS  Google Scholar 

  • Bellen HJ, Levis RW, He Y et al (2011) The Drosophila gene disruption project: progress using transposons with distinctive site specificities. Genetics 188:731–743

    PubMed  CAS  Google Scholar 

  • Berretta J, Pinskaya M, Morillon A (2008) A cryptic unstable transcript mediates transcriptional trans-silencing of the Ty1 retrotransposon in S. cerevisiae. Genes Dev 22:615–626

    PubMed  CAS  Google Scholar 

  • Billi AC, Freeberg MA, Day AM et al (2013) A conserved upstream motif orchestrates autonomous, germline-enriched expression of Caenorhabditis elegans piRNAs. PLoS Genet 9:e1003392

    PubMed  CAS  Google Scholar 

  • Bourc'his D, Bestor TH (2004) Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431:96–99

    PubMed  Google Scholar 

  • Bowen NJ, Jordan IK, Epstein JA et al (2003) Retrotransposons and their recognition of pol II promoters: a comprehensive survey of the transposable elements from the complete genome sequence of Schizosaccharomyces pombe. Genome Res 13:1984–1997

    PubMed  CAS  Google Scholar 

  • Brennecke J, Aravin AA, Stark A et al (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128:1089–1103

    PubMed  CAS  Google Scholar 

  • Bühler M, Haas W, Gygi SP, Moazed D (2007) RNAi-dependent and -independent RNA turnover mechanisms contribute to heterochromatic gene silencing. Cell 129:707–721

    PubMed  Google Scholar 

  • Buker SM, Iida T, Bühler M et al (2007) Two different Argonaute complexes are required for siRNA generation and heterochromatin assembly in fission yeast. Nat Struct Mol Biol 14:200–207

    PubMed  CAS  Google Scholar 

  • Calarco JP, Borges F, Donoghue MTA et al (2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151:194–205

    PubMed  CAS  Google Scholar 

  • Cam HP, Noma K-I, Ebina H et al (2008) Host genome surveillance for retrotransposons by transposon-derived proteins. Nature 451:431–436

    PubMed  CAS  Google Scholar 

  • Capy P (1997) Evolution and impact of transposable elements. Springer, Berlin

  • Cecere G, Zheng GXY, Mansisidor AR et al (2012) Promoters recognized by forkhead proteins exist for individual 21U-RNAs. Mol Cell 47:734–745

    PubMed  CAS  Google Scholar 

  • Chan SW-L, Zilberman D, Xie Z et al (2004) RNA silencing genes control de novo DNA methylation. Science 303:1336

    PubMed  CAS  Google Scholar 

  • Chandler VL, Walbot V (1986) DNA modification of a maize transposable element correlates with loss of activity. Proc Natl Acad Sci U S A 83:1767–1771

    PubMed  CAS  Google Scholar 

  • Chatterjee AG, Leem Y-E, Kelly FD, Levin HL (2009) The chromodomain of Tf1 integrase promotes binding to cDNA and mediates target site selection. J Virol 83:2675–2685

    PubMed  CAS  Google Scholar 

  • Chen D, Toone WM, Mata J et al (2003) Global transcriptional responses of fission yeast to environmental stress. Mol Biol Cell 14:214–229

    PubMed  CAS  Google Scholar 

  • Chen ES, Zhang K, Nicolas E et al (2008) Cell cycle control of centromeric repeat transcription and heterochromatin assembly. Nature 451:734–737

    PubMed  CAS  Google Scholar 

  • Chikashige Y, Kinoshita N, Nakaseko Y et al (1989) Composite motifs and repeat symmetry in S. pombe centromeres: direct analysis by integration of NotI restriction sites. Cell 57:739–751

    PubMed  CAS  Google Scholar 

  • Chomet PS, Wessler S, Dellaporta SL (1987) Inactivation of the maize transposable element Activator (Ac) is associated with its DNA modification. EMBO J 6:295–302

    PubMed  CAS  Google Scholar 

  • Clarke L, Baum MP (1990) Functional analysis of a centromere from fission yeast: a role for centromere-specific repeated DNA sequences. Mol Cell Biol 10:1863–1872

    PubMed  CAS  Google Scholar 

  • Cokus SJ, Feng S, Zhang X et al (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–219

    PubMed  CAS  Google Scholar 

  • Dai J, Xie W, Brady TL et al (2007) Phosphorylation regulates integration of the yeast Ty5 retrotransposon into heterochromatin. Mol Cell 27:289–299

    PubMed  CAS  Google Scholar 

  • Das PP, Bagijn MP, Goldstein LD et al (2008) Piwi and piRNAs act upstream of an endogenous siRNA pathway to suppress Tc3 transposon mobility in the Caenorhabditis elegans germline. Mol Cell 31:79–90

    PubMed  CAS  Google Scholar 

  • Djupedal I, Portoso M, Spåhr H et al (2005) RNA Pol II subunit Rpb7 promotes centromeric transcription and RNAi-directed chromatin silencing. Genes Dev 19:2301–2306

    PubMed  CAS  Google Scholar 

  • Dowen RH, Pelizzola M, Schmitz RJ et al (2012) Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci U S A 109:E2183–E2191

    PubMed  CAS  Google Scholar 

  • Drinnenberg IA, Weinberg DE, Xie KT et al (2009) RNAi in budding yeast. Science 326:544–550

    PubMed  CAS  Google Scholar 

  • Durand-Dubief M, Sinha I, Fagerström-Billai F et al (2007) Specific functions for the fission yeast Sirtuins Hst2 and Hst4 in gene regulation and retrotransposon silencing. EMBO J 26:2477–2488

    PubMed  CAS  Google Scholar 

  • Eichten SR, Ellis NA, Makarevitch I et al (2012) Spreading of heterochromatin is limited to specific families of maize retrotransposons. PLoS Genet 8:e1003127

    PubMed  CAS  Google Scholar 

  • Espinoza CA, Goodrich JA, Kugel JF (2007) Characterization of the structure, function, and mechanism of B2 RNA, an ncRNA repressor of RNA polymerase II transcription. RNA 13:583–596

    PubMed  CAS  Google Scholar 

  • Feng G, Leem Y-E, Levin HL (2013) Transposon integration enhances expression of stress response genes. Nucleic Acids Res 41:775–789

    PubMed  CAS  Google Scholar 

  • Finnegan DJ (2012) Retrotransposons. Curr Biol 22:R432–R437

    PubMed  CAS  Google Scholar 

  • Fischer T, Cui B, Dhakshnamoorthy J et al (2009) Diverse roles of HP1 proteins in heterochromatin assembly and functions in fission yeast. Proc Natl Acad Sci U S A 106:8998–9003

    PubMed  CAS  Google Scholar 

  • Furini A, Koncz C, Salamini F, Bartels D (1997) High level transcription of a member of a repeated gene family confers dehydration tolerance to callus tissue of Craterostigma plantagineum. EMBO J 16:3599–3608

    PubMed  CAS  Google Scholar 

  • Gai X, Voytas DF (1998) A single amino acid change in the yeast retrotransposon Ty5 abolishes targeting to silent chromatin. Mol Cell 1:1051–1055

    PubMed  CAS  Google Scholar 

  • Gao Z, Liu H-L, Daxinger L et al (2010) An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 465:106–109

    PubMed  CAS  Google Scholar 

  • Gehring M, Bubb KL, Henikoff S (2009) Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324:1447–1451

    PubMed  CAS  Google Scholar 

  • Golden DE, Gerbasi VR, Sontheimer EJ (2008) An inside job for siRNAs. Mol Cell 31:309–312

    PubMed  CAS  Google Scholar 

  • Gowen JW, Gay EH (1933) Effect of temperature on eversporting eye color in Drosophila melanogaster. Science 77:312

    PubMed  CAS  Google Scholar 

  • Gullerova M, Proudfoot NJ (2008) Cohesin complex promotes transcriptional termination between convergent genes in S. pombe. Cell 132:983–995

    PubMed  CAS  Google Scholar 

  • Gullerova M, Proudfoot NJ (2012) Convergent transcription induces transcriptional gene silencing in fission yeast and mammalian cells. Nat Struct Mol Biol 19:1193–1201

    PubMed  CAS  Google Scholar 

  • Gunawardane LS, Saito K, Nishida KM et al (2007) A slicer-mediated mechanism for repeat-associated siRNA 5' end formation in Drosophila. Science 315:1587–1590

    PubMed  CAS  Google Scholar 

  • Guo Y, Levin HL (2010) High-throughput sequencing of retrotransposon integration provides a saturated profile of target activity in Schizosaccharomyces pombe. Genome Res 20:239–248

    PubMed  CAS  Google Scholar 

  • Haag JR, Ream TS, Marasco M et al (2012) In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing. Mol Cell 48:811–818

    PubMed  CAS  Google Scholar 

  • Hansen KR, Burns G, Mata J et al (2005) Global effects on gene expression in fission yeast by silencing and RNA interference machineries. Mol Cell Biol 25:590–601

    PubMed  CAS  Google Scholar 

  • Herr AJ, Jensen MB, Dalmay T, Baulcombe DC (2005) RNA polymerase IV directs silencing of endogenous DNA. Science 308:118–120

    PubMed  CAS  Google Scholar 

  • Hilbricht T, Varotto S, Sgaramella V et al (2008) Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection of the plant Craterostigma plantagineum. New Phytol 179:877–887

    PubMed  CAS  Google Scholar 

  • Hirochika H, Okamoto H, Kakutani T (2000) Silencing of retrotransposons in Arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12:357–369

    PubMed  CAS  Google Scholar 

  • Hoff EF, Levin HL, Boeke JD (1998) Schizosaccharomyces pombe retrotransposon Tf2 mobilizes primarily through homologous cDNA recombination. Mol Cell Biol 18:6839–6852

    PubMed  CAS  Google Scholar 

  • Hsieh T-F, Ibarra CA, Silva P et al (2009) Genome-wide demethylation of Arabidopsis endosperm. Science 324:1451–1454

    PubMed  CAS  Google Scholar 

  • Huang XA, Yin H, Sweeney S et al (2013) A major epigenetic programming mechanism guided by piRNAs. Dev Cell 24:502–516

    PubMed  CAS  Google Scholar 

  • Huettel B, Kanno T, Daxinger L et al (2006) Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J 25:2828–2836

    PubMed  CAS  Google Scholar 

  • Ibarra CA, Feng X, Schoft VK et al (2012) Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337:1360–1364

    PubMed  CAS  Google Scholar 

  • Ipsaro JJ, Haase AD, Knott SR et al (2012) The structural biochemistry of Zucchini implicates it as a nuclease in piRNA biogenesis. Nature 491:279–283

    PubMed  CAS  Google Scholar 

  • Ito H, Gaubert H, Bucher E et al (2011) An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472:115–119

    PubMed  CAS  Google Scholar 

  • Jeddeloh JA, Stokes TL, Richards EJ (1999) Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nat Genet 22:94–97

    PubMed  CAS  Google Scholar 

  • Jiang YW (2002) Transcriptional cosuppression of yeast Ty1 retrotransposons. Genes Dev 16:467–478

    PubMed  CAS  Google Scholar 

  • Kasschau KD, Fahlgren N, Chapman EJ et al (2007) Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol 5:e57

    PubMed  Google Scholar 

  • Kato M, Miura A, Bender J et al (2003) Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr Biol 13:421–426

    PubMed  CAS  Google Scholar 

  • Kato H, Goto DB, Martienssen RA et al (2005) RNA polymerase II is required for RNAi-dependent heterochromatin assembly. Science 309:467–469

    PubMed  CAS  Google Scholar 

  • Kato Y, Kaneda M, Hata K et al (2007) Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse. Hum Mol Genet 16:2272–2280

    PubMed  CAS  Google Scholar 

  • Khurana JS, Wang J, Xu J et al (2011) Adaptation to P element transposon invasion in Drosophila melanogaster. Cell 147:1551–1563

    PubMed  CAS  Google Scholar 

  • Kim JM, Vanguri S, Boeke JD et al (1998) Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res 8:464–478

    PubMed  CAS  Google Scholar 

  • Kloc A, Zaratiegui M, Nora E, Martienssen R (2008) RNA interference guides histone modification during the S phase of chromosomal replication. Curr Biol 18:490–495

    PubMed  CAS  Google Scholar 

  • Kuramochi-Miyagawa S, Watanabe T, Gotoh K et al (2008) DNA methylation of retrotransposon genes is regulated by Piwi family members MILI and MIWI2 in murine fetal testes. Genes Dev 22:908–917

    PubMed  CAS  Google Scholar 

  • Lander ES, Linton LM, Birren B et al (2001) Initial sequencing and analysis of the human genome. Nature 409:860–921

    PubMed  CAS  Google Scholar 

  • Law JA, Du J, Hale CJ et al (2013) Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498:385–389

    PubMed  CAS  Google Scholar 

  • Le Thomas A, Rogers AK, Webster A et al (2013) Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes Dev 27:390–399

    PubMed  Google Scholar 

  • Lee H-C, Gu W, Shirayama M et al (2012) C. elegans piRNAs mediate the genome-wide surveillance of germline transcripts. Cell 150:78–87

    PubMed  CAS  Google Scholar 

  • Lee NN, Chalamcharla VR, Reyes-Turcu F et al (2013) Mtr4-like Protein Coordinates Nuclear RNA Processing for Heterochromatin Assembly and for Telomere Maintenance. Cell 1–14. doi:10.1016/j.cell.2013.10.027

  • Levin HL, Moran JV (2011) Dynamic interactions between transposable elements and their hosts. Nat Rev Genet 12:615–627

    PubMed  CAS  Google Scholar 

  • Li T, Spearow J, Rubin CM, Schmid CW (1999) Physiological stresses increase mouse short interspersed element (SINE) RNA expression in vivo. Gene 239:367–372

    PubMed  CAS  Google Scholar 

  • Li C, Vagin VV, Lee S et al (2009) Collapse of germline piRNAs in the absence of Argonaute3 reveals somatic piRNAs in flies. Cell 137:509–521

    PubMed  CAS  Google Scholar 

  • Lister R, O'Malley RC, Tonti-Filippini J et al (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133:523–536

    PubMed  CAS  Google Scholar 

  • Liu WM, Chu WM, Choudary PV, Schmid CW (1995) Cell stress and translational inhibitors transiently increase the abundance of mammalian SINE transcripts. Nucleic Acids Res 23:1758–1765

    PubMed  CAS  Google Scholar 

  • Lorenz DR, Mikheyeva IV, Johansen P et al (2012) CENP-B cooperates with Set1 in bidirectional transcriptional silencing and genome organization of retrotransposons. Mol Cell Biol 32:4215–4225

    PubMed  CAS  Google Scholar 

  • Luan DD, Korman MH, Jakubczak JL, Eickbush TH (1993) Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72:595–605

    PubMed  CAS  Google Scholar 

  • Madrid M, Soto T, Franco A et al (2004) A cooperative role for Atf1 and Pap1 in the detoxification of the oxidative stress induced by glucose deprivation in Schizosaccharomyces pombe. J Biol Chem 279:41594–41602

    PubMed  CAS  Google Scholar 

  • Mariner PD, Walters RD, Espinoza CA et al (2008) Human Alu RNA is a modular transacting repressor of mRNA transcription during heat shock. Mol Cell 29:499–509

    PubMed  CAS  Google Scholar 

  • Matsuda E, Garfinkel DJ (2009) Posttranslational interference of Ty1 retrotransposition by antisense RNAs. Proc Natl Acad Sci U S A 106:15657–15662

    PubMed  CAS  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

    PubMed  CAS  Google Scholar 

  • McCue AD, Nuthikattu S, Reeder SH, Slotkin RK (2012) Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLoS Genet 8:e1002474

    PubMed  CAS  Google Scholar 

  • Mirouze M, Reinders J, Bucher E et al (2009) Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461:427–430

    PubMed  CAS  Google Scholar 

  • Miura A, Yonebayashi S, Watanabe K et al (2001) Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411:212–214

    PubMed  CAS  Google Scholar 

  • Miyao A, Tanaka K, Murata K, et al (2003) Target site specificity of the Tos17 Retrotransposon shows a preference for insertion within genes and against insertion in retrotransposon-rich regions of the genome. Plant Cell 15(8):1771–1780.

    Google Scholar 

  • Mosher RA, Melnyk CW, Kelly KA et al (2009) Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 460:283–286

    PubMed  CAS  Google Scholar 

  • Motamedi MR, Verdel A, Colmenares SU et al (2004) Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119:789–802

    PubMed  CAS  Google Scholar 

  • Mourier T, Willerslev E (2010) Large-scale transcriptome data reveals transcriptional activity of fission yeast LTR retrotransposons. BMC Genomics 11:167

    PubMed  Google Scholar 

  • Naito K, Zhang F, Tsukiyama T et al (2009) Unexpected consequences of a sudden and massive transposon amplification on rice gene expression. Nature 461:1130–1134. doi:10.1038/nature08479

    PubMed  CAS  Google Scholar 

  • Nishimasu H, Ishizu H, Saito K et al (2012) Structure and function of Zucchini endoribonuclease in piRNA biogenesis. Nature 491:284–287

    PubMed  CAS  Google Scholar 

  • Noma K-I, Sugiyama T, Cam H et al (2004) RITS acts in cis to promote RNA interference-mediated transcriptional and post-transcriptional silencing. Nat Genet 36:1174–1180

    PubMed  CAS  Google Scholar 

  • Qi Y, Denli AM, Hannon GJ (2005) Biochemical specialization within Arabidopsis RNA silencing pathways. Mol Cell 19:421–428

    PubMed  CAS  Google Scholar 

  • Qi Y, He X, Wang X-J et al (2006) Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443:1008–1012

    PubMed  Google Scholar 

  • Rebollo R, Karimi MM, Bilenky M et al (2011) Retrotransposon-induced heterochromatin spreading in the mouse revealed by insertional polymorphisms. PLoS Genet 7:e1002301

    PubMed  CAS  Google Scholar 

  • Reinhart BJ, Bartel DP (2002) Small RNAs correspond to centromere heterochromatic repeats. Science 297:1831

    PubMed  CAS  Google Scholar 

  • Rhind N, Chen Z, Yassour M et al (2011) Comparative functional genomics of the fission yeasts. Science 332:930–936

    PubMed  CAS  Google Scholar 

  • Rigal M, Mathieu O (2011) A “mille-feuille” of silencing: epigenetic control of transposable elements. Biochim Biophys Acta 1809:452–458

    PubMed  CAS  Google Scholar 

  • Sadaie M, Kawaguchi R, Ohtani Y et al (2008) Balance between distinct HP1 family proteins controls heterochromatin assembly in fission yeast. Mol Cell Biol 28:6973–6988

    PubMed  CAS  Google Scholar 

  • Schalch T, Job G, Noffsinger VJ et al (2009) High-affinity binding of Chp1 chromodomain to K9 methylated histone H3 is required to establish centromeric heterochromatin. Mol Cell 34:36–46

    PubMed  CAS  Google Scholar 

  • Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    PubMed  CAS  Google Scholar 

  • Sehgal A, Lee C-YS, Espenshade PJ (2007) SREBP controls oxygen-dependent mobilization of retrotransposons in fission yeast. PLoS Genet 3:e131

    PubMed  Google Scholar 

  • Shirayama M, Seth M, Lee H-C et al (2012) piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell 150:65–77

    PubMed  CAS  Google Scholar 

  • Sienski G, Dönertas D, Brennecke J (2012) Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell 151:964–980

    PubMed  CAS  Google Scholar 

  • Sigova A, Rhind N, Zamore PD (2004) A single Argonaute protein mediates both transcriptional and posttranscriptional silencing in Schizosaccharomyces pombe. Genes Dev 18:2359–2367

    PubMed  CAS  Google Scholar 

  • Singleton TL, Levin HL (2002) A long terminal repeat retrotransposon of fission yeast has strong preferences for specific sites of insertion. Eukaryot Cell 1:44–55

    PubMed  CAS  Google Scholar 

  • Slotkin RK, Vaughn M, Borges F et al (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472

    PubMed  CAS  Google Scholar 

  • Solyom S, Kazazian HH (2012) Mobile elements in the human genome: implications for disease. Genome Med 4:12

    PubMed  CAS  Google Scholar 

  • Spradling AC, Bellen HJ, Hoskins RA (2011) Drosophila P elements preferentially transpose to replication origins. Proc Natl Acad Sci U S A 108:15948–15953

    PubMed  CAS  Google Scholar 

  • Sugiyama T, Cam H, Verdel A et al (2005) RNA-dependent RNA polymerase is an essential component of a self-enforcing loop coupling heterochromatin assembly to siRNA production. Proc Natl Acad Sci U S A 102:152–157

    PubMed  CAS  Google Scholar 

  • Sugiyama T, Cam HP, Sugiyama R et al (2007) SHREC, an effector complex for heterochromatic transcriptional silencing. Cell 128:491–504

    PubMed  CAS  Google Scholar 

  • Tittel-Elmer M, Bucher E, Broger L et al (2010) Stress-induced activation of heterochromatic transcription. PLoS Genet 6:e1001175

    PubMed  Google Scholar 

  • Tsukahara S, Kobayashi A, Kawabe A et al (2009) Bursts of retrotransposition reproduced in Arabidopsis. Nature 461:423–426

    PubMed  CAS  Google Scholar 

  • Tudor M, Lobocka M, Goodell M et al (1992) The pogo transposable element family of Drosophila melanogaster. Mol Gen Genet 232:126–134

    PubMed  CAS  Google Scholar 

  • Vagin VV, Sigova A, Li C et al (2006) A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313:320–324

    PubMed  CAS  Google Scholar 

  • Van Ex F, Jacob Y, Martienssen RA (2011) Multiple roles for small RNAs during plant reproduction. Curr Opin Plant Biol 14:588–593

    PubMed  Google Scholar 

  • van Luenen HG, Plasterk RH (1994) Target site choice of the related transposable elements Tc1 and Tc3 of Caenorhabditis elegans. Nucleic Acids Res 22:262–269

    PubMed  Google Scholar 

  • Verdel A, Jia S, Gerber S et al (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303:672–676

    PubMed  CAS  Google Scholar 

  • Volpe TA, Kidner C, Hall IM et al (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833–1837

    PubMed  CAS  Google Scholar 

  • Vongs A, Kakutani T, Martienssen RA, Richards EJ (1993) Arabidopsis thaliana DNA methylation mutants. Science 260:1926–1928

    PubMed  CAS  Google Scholar 

  • Wheeler BS, Ruderman BT, Willard HF, Scott KC (2012) Uncoupling of genomic and epigenetic signals in the maintenance and inheritance of heterochromatin domains in fission yeast. Genetics 190:549–557

    PubMed  CAS  Google Scholar 

  • Wierzbicki AT, Haag JR, Pikaard CS (2008) Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135:635–648

    PubMed  CAS  Google Scholar 

  • Wierzbicki AT, Ream TS, Haag JR, Pikaard CS (2009) RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat Publ Group 41:630–634

    CAS  Google Scholar 

  • Wood V, Gwilliam R, Rajandream M-A et al (2002) The genome sequence of Schizosaccharomyces pombe. Nature 415:871–880

    PubMed  CAS  Google Scholar 

  • Woolcock KJ, Gaidatzis D, Punga T, Bühler M (2011) Dicer associates with chromatin to repress genome activity in Schizosaccharomyces pombe. Nat Struct Mol Biol 18:94–99

    PubMed  CAS  Google Scholar 

  • Xie W, Gai X, Zhu Y et al (2001) Targeting of the yeast Ty5 retrotransposon to silent chromatin is mediated by interactions between integrase and Sir4p. Mol Cell Biol 21:6606–6614

    PubMed  CAS  Google Scholar 

  • Xie Z, Johansen LK, Gustafson AM et al (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2:E104

    PubMed  Google Scholar 

  • Yamanaka S, Mehta S, Reyes-Turcu FE et al (2013) RNAi triggered by specialized machinery silences developmental genes and retrotransposons. Nature 493:557–560

    PubMed  CAS  Google Scholar 

  • Zaratiegui M, Vaughn MW, Irvine DV et al (2011) CENP-B preserves genome integrity at replication forks paused by retrotransposon LTR. Nature 469:112–115

    PubMed  CAS  Google Scholar 

  • Zeller G, Henz SR, Widmer CK et al (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58:1068–1082

    PubMed  CAS  Google Scholar 

  • Zhang X, Yazaki J, Sundaresan A et al (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201

    PubMed  CAS  Google Scholar 

  • Zhang X, Henderson IR, Lu C et al (2007) Role of RNA polymerase IV in plant small RNA metabolism. Proc Natl Acad Sci U S A 104:4536–4541

    PubMed  CAS  Google Scholar 

  • Zhang K, Mosch K, Fischle W, Grewal SIS (2008) Roles of the Clr4 methyltransferase complex in nucleation, spreading and maintenance of heterochromatin. Nat Struct Mol Biol 15:381–388

    PubMed  CAS  Google Scholar 

  • Zhang H, Ma Z-Y, Zeng L et al (2013) DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV. Proc Natl Acad Sci U S A 110:8290–8295

    PubMed  CAS  Google Scholar 

  • Zhong S-H, Liu J-Z, Jin H et al (2013) Warm temperatures induce transgenerational epigenetic release of RNA silencing by inhibiting siRNA biogenesis in Arabidopsis. Proc Natl Acad Sci U S A 110:9171–9176

    PubMed  CAS  Google Scholar 

  • Zhu Y, Dai J, Fuerst PG, Voytas DF (2003) Controlling integration specificity of a yeast retrotransposon. Proc Natl Acad Sci U S A 100:5891–5895

    PubMed  CAS  Google Scholar 

  • Zilberman D, Cao X, Jacobsen SE (2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299:716–719

    PubMed  CAS  Google Scholar 

  • Zou S, Voytas DF (1997) Silent chromatin determines target preference of the Saccharomyces retrotransposon Ty5. Proc Natl Acad Sci U S A 94:7412–7416

    PubMed  CAS  Google Scholar 

  • Zou S, Ke N, Kim JM, Voytas DF (1996) The Saccharomyces retrotransposon Ty5 integrates preferentially into regions of silent chromatin at the telomeres and mating loci. Genes Dev 10:634–645

    PubMed  CAS  Google Scholar 

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Acknowledgments

BSW is supported by the NIH Ruth L. Kirschstein National Research Service Award F32 GM100647-02 (NIGMS). Thanks to Teresa Lee for critical reading of the review.

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  1. Department of Molecular and Cell Biology, University of California at Berkeley, Berkeley, CA, 94720, USA

    Bayly S. Wheeler

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Correspondence to Bayly S. Wheeler.

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Responsible Editors: Brian P. Chadwick, Kristin C. Scott, and Beth A. Sullivan

Since this review was written, it has been shown that fission yeast heterochromatin formation at TEs in the absence of the exosome requires recruitment of RNA splicing factors. This work raises the intriguing possibility that heterochromatin formation at TEs in low glucose conditions could result from differential regulation of splicing in response to a changing environment (Lee et al. 2013)

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Wheeler, B.S. Small RNAs, big impact: small RNA pathways in transposon control and their effect on the host stress response. Chromosome Res 21, 587–600 (2013). https://doi.org/10.1007/s10577-013-9394-4

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