Silencing of active transposable elements in plants

Current Opinion in Plant Biology

Volumn 27, Issue , 2015, Pages 67-76

  Fultz, Dalen ^a   Choudury, Sarah G ^a   Slotkin, R Keith ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSPOSON;

BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; PLANT; PLANT GENOME; TRANSPOSON;

DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; GENOME, PLANT; MODELS, GENETIC; PLANTS;

EID: 84955512571     PISSN: 13695266     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbi.2015.05.027     Document Type: Review

References (89)

1. Lisch D. Epigenetic regulation of transposable elements in plants. Ann Rev Plant Biol 2009, 60:43-66.
2. Bucher E., Reinders J., Mirouze M. Epigenetic control of transposon transcription and mobility in Arabidopsis. Curr Opin Plant Biol 2012, 15:503-510.
3. Ito H., Kakutani T. Control of transposable elements in Arabidopsis thaliana. Chromosome Res 2014, 22:217-223.
4. Willing E.-M., Rawat V., Mandáková T., Maumus F., James G.V., Nordström K.J.V., Becker C., Warthmann N., Chica C., Szarzynska B., et al. Genome expansion of Arabis alpina linked with retrotransposition and reduced symmetric DNA methylation. Nat Plants 2015, 1:14023.
5. Matzke M.A., Mosher R.A. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 2014, 15:394-408.
6. Law J.A., Du J., Hale C.J., Feng S., Krajewski K., Palanca A.M.S., Strahl B.D., Patel D.J., Jacobsen S.E. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 2013, 498:385-389.
7. Nobuta K., Venu R.C., Lu C., Beló A., Vemaraju K., Kulkarni K., Wang W., Pillay M., Green P.J., Wang G.-L., et al. An expression atlas of rice mRNAs and small RNAs. Nat Biotechnol 2007, 25:473-477.
8. Cho S.H., Addo-Quaye C., Coruh C., Arif M.A., Ma Z., Frank W., Axtell M.J. Physcomitrella patens DCL3 is required for 22-24 nt siRNA accumulation, suppression of retrotransposon-derived transcripts, and normal development. PLoS Genet 2008, 4:e1000314.
9. Huang Y., Kendall T., Mosher R.A. Pol IV-dependent siRNA production is reduced in Brassica rapa. Biology (Basel) 2013, 2:1210-1223.
10. Wierzbicki A.T. The role of long non-coding RNA in transcriptional gene silencing. Curr Opin Plant Biol 2012, 15:517-522.
11. Teixeira F.K., Heredia F., Sarazin A., Roudier F., Boccara M., Ciaudo C., Cruaud C., Poulain J., Berdasco M., Fraga M.F., et al. A role for RNAi in the selective correction of DNA methylation defects. Science 2009, 323:1600-1604.
12. Ito H., Gaubert H., Bucher E., Mirouze M., Vaillant I., Paszkowski J. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 2011, 472:115-119.
13. Nuthikattu S., McCue A.D., Panda K., Fultz D., DeFraia C., Thomas E.N., Slotkin R.K. The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21-22 nucleotide small interfering RNAs. Plant Physiol 2013, 162:116-131.
14. Slotkin R.K., Freeling M., Lisch D. Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat Genet 2005, 37:641-644.
15. Lisch D., Bennetzen J.L. Transposable element origins of epigenetic gene regulation. Curr Opin Plant Biol 2011, 14:156-161.
16. El-Baidouri M., Carpentier M.-C., Cooke R., Gao D., Lasserre E., Llauro C., Mirouze M., Picault N., Jackson S.A., Panaud O. Widespread and frequent horizontal transfers of transposable elements in plants. Genome Res 2014, 24:831-838.
17. Diao X., Freeling M., Lisch D. Horizontal transfer of a plant transposon. PLoS Biol 2006, 4:e5.
18. Wei W., Ba Z., Gao M., Wu Y., Ma Y., Amiard S., White C.I., Rendtlew Danielsen J.M., Yang Y.-G., Qi Y. A role for small RNAs in DNA double-strand break repair. Cell 2012, 149:101-112.
19. Dunoyer P., Brosnan C.A., Schott G., Wang Y., Jay F., Alioua A., Himber C., Voinnet O. An endogenous, systemic RNAi pathway in plants. EMBO J 2010, 29:1699-1712.
20. McCue A.D., Nuthikattu S., Reeder S.H., Slotkin R.K. Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLoS Genet 2012, 8:e1002474.
21. Dowen R.H., Pelizzola M., Schmitz R.J., Lister R., Dowen J.M., Nery J.R., Dixon J.E., Ecker J.R. Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci U S A 2012, 109:E2183-E2191.
22. Sarkies P., Selkirk M.E., Jones J.T., Blok V., Boothby T., Goldstein B., Hanelt B., Ardila-Garcia A., Fast N.M., Schiffer P.M., et al. Ancient and novel small RNA pathways compensate for the loss of piRNAs in multiple independent nematode lineages. PLoS Biol 2015, 13:e1002061.
23. Cavrak V.V., Lettner N., Jamge S., Kosarewicz A., Bayer L.M., Scheid O.M. How a retrotransposon exploits the plant's heat stress response for its activation. PLoS Genet 2014, 10:e1004115.
24. Xie Z., Allen E., Wilken A., Carrington J.C. DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc Natl Acad Sci U S A 2005, 102:12984-12989.
25. Deleris A., Gallego-Bartolome J., Bao J., Kasschau K.D., Carrington J.C., Voinnet O. Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 2006, 313:68-71.
26. Cuperus J.T., Carbonell A., Fahlgren N., Garcia-Ruiz H., Burke R.T., Takeda A., Sullivan C.M., Gilbert S.D., Montgomery T.A., Carrington J.C. Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat Struct Mol Biol 2010, 17:997-1003.
27. Chen H.-M., Chen L.-T., Patel K., Li Y.-H., Baulcombe D.C., Wu S.-H. 22-Nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc Natl Acad Sci U S A 2010, 107:15269-15274.
28. Mlotshwa S., Pruss G.J., Peragine A., Endres M.W., Li J., Chen X., Poethig R.S., Bowman L.H., Vance V. DICER-LIKE2 plays a primary role in transitive silencing of transgenes in Arabidopsis. PLoS ONE 2008, 3:e1755.
29. Wang X.-B., Jovel J., Udomporn P., Wang Y., Wu Q., Li W.-X., Gasciolli V., Vaucheret H., Ding S.W. The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative argonautes in Arabidopsis thaliana. Plant Cell 2011, 23:1625-1638.
30. Zhang X., Zhu Y., Liu X., Hong X., Xu Y., Zhu P., Shen Y., Wu H., Ji Y., Wen X., et al. Suppression of endogenous gene silencing by bidirectional cytoplasmic RNA decay in Arabidopsis. Science 2015, 348:120-123.
31. Axtell M.J., Jan C., Rajagopalan R., Bartel D.P. A two-hit trigger for siRNA biogenesis in plants. Cell 2006, 127:565-577.
32. Pane A., Jiang P., Zhao D.Y., Singh M., Schüpbach T. The Cutoff protein regulates piRNA cluster expression and piRNA production in the Drosophila germline. EMBO J 2011, 30:4601-4615.
33. Dumesic P.A., Natarajan P., Chen C., Drinnenberg I.A., Schiller B.J., Thompson J., Moresco J.J., Yates J.R., Bartel D.P., Madhani H.D. Stalled spliceosomes are a signal for RNAi-mediated genome defense. Cell 2013, 152:957-968.
34. Goriaux C., Desset S., Renaud Y., Vaury C., Brasset E. Transcriptional properties and splicing of the flamenco piRNA cluster. EMBO Rep 2014, 15:411-418.
35. Malone C.D., Mestdagh C., Akhtar J., Kreim N., Deinhard P., Sachidanandam R., Treisman J., Roignant J.-Y. The exon junction complex controls transposable element activity by ensuring faithful splicing of the piwi transcript. Genes Dev 2014, 28:1786-1799.
36. Meyers B.C., Axtell M.J., Bartel B., Bartel D.P., Baulcombe D., Bowman J.L., Cao X., Carrington J.C., Chen X., Green P.J., et al. Criteria for annotation of plant MicroRNAs. Plant Cell 2008, 20:3186-3190.
37. Creasey K.M., Zhai J., Borges F., Van Ex F., Regulski M., Meyers B.C., Martienssen R.A. miRNAs trigger widespread epigenetically activated siRNAs from transposons in Arabidopsis. Nature 2014, 508:411-415.
38. Halic M., Moazed D. Dicer-independent primal RNAs trigger RNAi and heterochromatin formation. Cell 2010, 140:504-516.
39. Lee H.-C., Gu W., Shirayama M., Youngman E., Conte D., Mello C.C. C. elegans piRNAs mediate the genome-wide surveillance of germline transcripts. Cell 2012, 150:78-87.
40. Shirayama M., Seth M., Lee H.-C., Gu W., Ishidate T., Conte D., Mello C.C. piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell 2012, 150:65-77.
41. Marí-Ordóñez A., Marchais A., Etcheverry M., Martin A., Colot V., Voinnet O. Reconstructing de novo silencing of an active plant retrotransposon. Nat Genet 2013, 45:1029-1039.
42. Wu L., Mao L., Qi Y. Roles of DICER-LIKE and ARGONAUTE proteins in TAS-derived small interfering RNA-triggered DNA methylation. Plant Physiol 2012, 160:990-999.
43. Bond D.M., Baulcombe D.C. Epigenetic transitions leading to heritable RNA-mediated de novo silencing in Arabidopsis thaliana. Proc Natl Acad Sci U S A 2015, 112:917-922.
44. McCue A.D., Panda K., Nuthikattu S., Choudury S.G., Thomas E.N., Slotkin R.K. ARGONAUTE 6 bridges transposable element mRNA-derived siRNAs to the establishment of DNA methylation. EMBO J 2015, 34:20-35.
45. Sasaki T., Lee T.-F., Liao W.-W., Naumann U., Liao J.-L., Eun C., Huang Y.-Y., Fu J.L., Chen P.-Y., Meyers B.C., et al. Distinct and concurrent pathways of Pol II- and Pol IV-dependent siRNA biogenesis at a repetitive trans-silencer locus in Arabidopsis thaliana. Plant J 2014, 79:127-138.
46. Pontier D., Picart C., Roudier F., Garcia D., Lahmy S., Azevedo J., Alart E., Laudié M., Karlowski W.M., Cooke R., et al. NERD, a plant-specific GW protein, defines an additional RNAi-dependent chromatin-based pathway in Arabidopsis. Mol Cell 2012, 48:121-132.
47. Johnson L.M., Du J., Hale C.J., Bischof S., Feng S., Chodavarapu R.K., Zhong X., Marson G., Pellegrini M., Segal D.J., et al. SRA- and SET-domain-containing proteins link RNA polymerase V occupancy to DNA methylation. Nature 2014, 507:124-128.
48. Daxinger L., Kanno T., Bucher E., van der Winden J., Naumann U., Matzke A.J.M., Matzke M. A stepwise pathway for biogenesis of 24-nt secondary siRNAs and spreading of DNA methylation. EMBO J 2009, 28:48-57.
49. Zhang X., Germann S., Blus B.J., Khorasanizadeh S., Gaudin V., Jacobsen S.E. The Arabidopsis LHP1 protein colocalizes with histone H3 Lys27 trimethylation. Nat Struct Mol Biol 2007, 14:869-871.
50. Turck F., Roudier F., Farrona S., Martin-Magniette M.-L., Guillaume E., Buisine N., Gagnot S., Martienssen R.A., Coupland G., Colot V. Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 2007, 3:e86.
51. Zhong X., Hale C.J., Law J.A., Johnson L.M., Feng S., Tu A., Jacobsen S.E. DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nat Struct Mol Biol 2012, 19:870-875.
52. Zemach A., Kim M.Y., Hsieh P.-H., Coleman-Derr D., Eshed-Williams L., Thao K., Harmer S.L., Zilberman D. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 2013, 153:193-205.
53. Onodera Y., Haag J.R., Ream T., Costa-Nunes P., Pontes O., Pikaard C.S. Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 2005, 120:613-622.
54. Huettel B., Kanno T., Daxinger L., Aufsatz W., Matzke A.J.M., Matzke M. Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. EMBO J 2006, 25:2828-2836.
55. Erhard K.F., Parkinson S.E., Gross S.M., Barbour J-ER, Lim J.P., Hollick J.B. Maize RNA polymerase IV defines trans-generational epigenetic variation. Plant Cell 2013, 25:808-819.
56. Mathieu O., Reinders J., Caikovski M., Smathajitt C., Paszkowski J. Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 2007, 130:851-862.
57. Stroud H., Do T., Du J., Zhong X., Feng S., Johnson L., Patel D.J., Jacobsen S.E. Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol 2014, 21:64-72.
58. Lister R., O'Malley R.C., Tonti-Filippini J., Gregory B.D., Berry C.C., Millar A.H., Ecker J.R. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 2008, 133:523-536.
59. Li S., Vandivier L.E., Tu B., Gao L., Won S.Y., Li S., Zheng B., Gregory B.D., Chen X. Detection of Pol IV/RDR2-dependent transcripts at the genomic scale in Arabidopsis reveals features and regulation of siRNA biogenesis. Genome Res 2015, 25:235-245.
60. Gent J.I., Madzima T.F., Bader R., Kent M.R., Zhang X., Stam M., McGinnis K.M., Dawe R.K. Accessible DNA and relative depletion of H3K9me2 at maize loci undergoing RNA-directed DNA methylation. Plant Cell 2014, 26:4903-4917.
61. Blevins T., Pontvianne F., Cocklin R., Podicheti R., Chandrasekhara C., Yerneni S., Braun C., Lee B., Rusch D., Mockaitis K., et al. A two-step process for epigenetic inheritance in Arabidopsis. Mol Cell 2014, 54:30-42.
62. Saze H. Epigenetic memory transmission through mitosis and meiosis in plants. Semin Cell Dev Biol 2008, 19:527-536.
63. Becker C., Hagmann J., Müller J., Koenig D., Stegle O., Borgwardt K., Weigel D. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 2011, 480:245-249.
64. Daxinger L., Whitelaw E. Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat Rev Genet 2012, 13:153-162.
65. Baubec T., Finke A., Mittelsten Scheid O., Pecinka A. Meristem-specific expression of epigenetic regulators safeguards transposon silencing in Arabidopsis. EMBO Rep 2014, 15:446-452.
66. Martinez G., Slotkin R.K. Developmental relaxation of transposable element silencing in plants: functional or byproduct?. Curr Opin Plant Biol 2012, 15:496-502.
67. Schoft V.K., Chumak N., Mosiolek M., Slusarz L., Komnenovic V., Brownfield L., Twell D., Kakutani T., Tamaru H. Induction of RNA-directed DNA methylation upon decondensation of constitutive heterochromatin. EMBO Rep 2009, 10:1015-1021.
68. Slotkin R.K., Vaughn M., Borges F., Tanurdzic M., Becker J.D., Feijó J.A., Martienssen R.A. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 2009, 136:461-472.
69. Calarco J.P., Borges F., Donoghue M.T.A., Van Ex F., Jullien P.E., Lopes T., Gardner R., Berger F., Feijó J.A., Becker J.D., et al. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 2012, 151:194-205.
70. Pillot M., Baroux C., Vazquez M.A., Autran D., Leblanc O., Vielle-Calzada J.-P., Grossniklaus U., Grimanelli D. Embryo and endosperm inherit distinct chromatin and transcriptional states from the female gametes in Arabidopsis. Plant Cell 2010, 22:307-320.
71. Ibarra C.A., Feng X., Schoft V.K., Hsieh T.F., Uzawa R., Rodrigues J.A., Zemach A., Chumak N., Machlicova A., Nishimura T., et al. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 2012, 337:1360-1364.
72. Gehring M., Bubb K.L., Henikoff S. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 2009, 324:1447-1451.
73. Bourchis D., Voinnet O. A small-RNA perspective on gametogenesis fertilization, and early zygotic development. Science 2010, 330:617-622.
74. Brennecke J., Malone C.D., Aravin A.A., Sachidanandam R., Stark A., Hannon G.J. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 2008, 322:1387-1392.
75. Li H., Freeling M., Lisch D. Epigenetic reprogramming during vegetative phase change in maize. Proc Natl Acad Sci U S A 2010, 107:22184-22189.
76. Mirouze M., Reinders J., Bucher E., Nishimura T., Schneeberger K., Ossowski S., Cao J., Weigel D., Paszkowski J., Mathieu O. Selective epigenetic control of retrotransposition in Arabidopsis. Nature 2009, 461:427-430.
77. Rudenko G.N., Ono A., Walbot V. Initiation of silencing of maize MuDR/Mu transposable elements. Plant J 2003, 33:1013-1025.
78. Bennetzen J.L., Wang H. The contributions of transposable elements to the structure, function, and evolution of plant genomes. Annu Rev Plant Biol 2014, 65:505-530.
79. Fu Y., Kawabe A., Etcheverry M., Ito T., Toyoda A., Fujiyama A., Colot V., Tarutani Y., Kakutani T. Mobilization of a plant transposon by expression of the transposon-encoded anti-silencing factor. EMBO J 2013, 32:2407-2417.
80. Lisch D., Slotkin R.K. Strategies for silencing and escape: the ancient struggle between transposable elements and their hosts. Int Rev Cell Mol Biol 2011, 292:119-152.
81. Joly-Lopez Z., Bureau T.E. Diversity and evolution of transposable elements in Arabidopsis. Chromosome Res 2014, 22:203-216.
82. McCue A.D., Nuthikattu S., Slotkin R.K. Genome-wide identification of genes regulated in trans by transposable element small interfering RNAs. RNA Biol 2013, 10:1379-1395.
83. Liu J., He Y., Amasino R., Chen X. siRNAs targeting an intronic transposon in the regulation of natural flowering behavior in Arabidopsis. Genes Dev 2004, 18:2873-2878.
84. Singh J., Freeling M., Lisch D. A position effect on the heritability of epigenetic silencing. PLoS Genet 2008, 4:e1000216.
85. Kabelitz T., Kappel C., Henneberger K., Benke E., Nöh C., Bäurle I. eQTL mapping of transposon silencing reveals a position-dependent stable escape from epigenetic silencing and transposition of AtMu1 in the Arabidopsis lineage. Plant Cell 2014, 26:3261-3271.
86. Zhu J., Kapoor A., Sridhar V.V., Agius F., Zhu J.-K. The DNA glycosylase/lyase ROS1 functions in pruning DNA methylation patterns in Arabidopsis. Curr Biol 2007, 17:54-59.
87. Saze H., Shiraishi A., Miura A., Kakutani T. Control of genic DNA methylation by a jmjC domain-containing protein in Arabidopsis thaliana. Science 2008, 319:462-465.
88. Rigal M., Kevei Z., Pélissier T., Mathieu O. DNA methylation in an intron of the IBM1 histone demethylase gene stabilizes chromatin modification patterns. EMBO J 2012, 31:2981-2993.
89. Panda K., Slotkin R.K. Proposed mechanism for the initiation of transposable element silencing by the RDR6-directed DNA methylation pathway. Plant Signal Behav 2013, 8.