DNA methylation influences the expression of DICER-LIKE4 isoforms, which encode proteins of alternative localization and function

Plant Cell

Volumn 28, Issue 11, 2016, Pages 2786-2804

  Pumplin, Nathan ^a   Sarazin, Alexis ^a   Jullien, Pauline E ^a,b   Bologna, Nicolas G ^a   Oberlin, Stefan ^a   Voinnet, Olivier ^a  

^a ETH ZURICH   (Switzerland)

^b INSTITUT DE RECHERCHE POUR LE DÉVELOPPEMENT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; DCL4 PROTEIN, ARABIDOPSIS; ISOPROTEIN; RIBONUCLEASE III; RNA DIRECTED RNA POLYMERASE; SMALL INTERFERING RNA; TRANSPOSON;

ARABIDOPSIS; DNA METHYLATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; TRANSPOSON;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; DNA METHYLATION; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION REGULATION, PLANT; PROTEIN ISOFORMS; RIBONUCLEASE III; RNA REPLICASE; RNA, SMALL INTERFERING;

EID: 85006298843     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.16.00554     Document Type: Article

References (89)

1. Adenot, X., Elmayan, T., Lauressergues, D., Boutet, S., Bouché, N., Gasciolli, V., and Vaucheret, H. (2006). DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr. Biol. 16: 927-932.
2. Aukerman, M.J., and Sakai, H. (2003). Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15: 2730-2741.
3. Baumberger, N., and Baulcombe, D.C. (2005). Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. USA 102: 11928-11933.
4. Belmonte, M.F., et al. (2013). Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc. Natl. Acad. Sci. USA 110: E435-E444.
5. Bemer, M., Heijmans, K., Airoldi, C., Davies, B., and Angenent, G.C. (2010). An atlas of type I MADS box gene expression during female gametophyte and seed development in Arabidopsis. Plant Physiol. 154: 287-300.
6. Bologna, N.G., and Voinnet, O. (2014). The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annu. Rev. Plant Biol. 65: 473-503.
7. Bond, D.M., and Baulcombe, D.C. (2015). Epigenetic transitions leading to heritable, RNA-mediated de novo silencing in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 112: 917-922.
8. Borges, F., and Martienssen, R.A. (2015). The expanding world of small RNAs in plants. Nat. Rev. Mol. Cell Biol. 16: 727-741.
9. Bouché, N., Lauressergues, D., Gasciolli, V., and Vaucheret, H. (2006). An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO J. 25: 3347-3356.
10. Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y.Y., Sieburth, L., and Voinnet, O. (2008). Widespread translational inhibition by plant miRNAs and siRNAs. Science 320: 1185-1190.
11. Burger, K., and Gullerova, M. (2015). Swiss army knives: noncanonical functions of nuclear Drosha and Dicer. Nat. Rev. Mol. Cell Biol. 16: 417-430.
12. Chen, X. (2004). A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303: 2022-2025.
13. Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
14. Connolly, D., Yang, Z., Castaldi, M., Simmons, N., Oktay, M.H., Coniglio, S., Fazzari, M.J., Verdier-Pinard, P., and Montagna, C. (2011). Septin 9 isoform expression, localization and epigenetic changes during human and mouse breast cancer progression. Breast Cancer Res. 13: R76.
15. Cook, A., Bono, F., Jinek, M., and Conti, E. (2007). Structural biology of nucleocytoplasmic transport. Annu. Rev. Biochem. 76: 647-671.
16. Creasey, K.M., Zhai, J., Borges, F., Van Ex, F., Regulski, M., Meyers, B.C., and Martienssen, R.A. (2014). miRNAs trigger widespread epigenetically activated siRNAs from transposons in Arabidopsis. Nature 508: 411-415.
17. de Felippes, F.F., and Weigel, D. (2010). Transient assays for the analysis of miRNA processing and function. Methods Mol. Biol. 592: 255-264.
18. Deleris, A., Gallego-Bartolome, J., Bao, J., Kasschau, K.D., Carrington, J.C., and Voinnet, O. (2006). Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313: 68-71.
19. Derrien, B., Baumberger, N., Schepetilnikov, M., Viotti, C., De Cillia, J., Ziegler-Graff, V., Isono, E., Schumacher, K., and Genschik, P. (2012). Degradation of the antiviral component ARGONAUTE1 by the autophagy pathway. Proc. Natl. Acad. Sci. USA 109: 15942-15946.
20. Dowen, R.H., Pelizzola, M., Schmitz, R.J., Lister, R., Dowen, J.M., Nery, J.R., Dixon, J.E., and Ecker, J.R. (2012). Widespread dynamic DNA methylation in response to biotic stress. Proc. Natl. Acad. Sci. USA 109: E2183-E2191.
21. Doyle, M., Badertscher, L., Jaskiewicz, L., Güttinger, S., Jurado, S., Hugenschmidt, T., Kutay, U., and Filipowicz, W. (2013). The double-stranded RNA binding domain of human Dicer functions as a nuclear localization signal. RNA 19: 1238-1252.
22. Drake, M., Furuta, T., Suen, K.M., Gonzalez, G., Liu, B., Kalia, A., Ladbury, J.E., Fire, A.Z., Skeath, J.B., and Arur, S. (2014). A requirement for ERK-dependent Dicer phosphorylation in coordinating oocyte-to-embryo transition in C. elegans. Dev. Cell 31: 614-628.
23. Du, M., Luo, M., Zhang, R., Finnegan, E.J., and Koltunow, A.M. (2014). Imprinting in rice: the role of DNA and histone methylation in modulating parent-of-origin specific expression and determining transcript start sites. Plant J. 79: 232-242.
24. Dunoyer, P., Himber, C., and Voinnet, O. (2005). DICER-LIKE 4 is required for RNA interference and produces the 21-nucleotide small interfering RNA component of the plant cell-to-cell silencing signal. Nat. Genet. 37: 1356-1360.
25. Emmerth, S., Schober, H., Gaidatzis, D., Roloff, T., Jacobeit, K., and Bühler, M. (2010). Nuclear retention of fission yeast dicer is a prerequisite for RNAi-mediated heterochromatin assembly. Dev. Cell 18: 102-113.
26. Fang, Y., and Spector, D.L. (2007). Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr. Biol. 17: 818-823.
27. Flemr, M., Malik, R., Franke, V., Nejepinska, J., Sedlacek, R., Vlahovicek, K., and Svoboda, P. (2013). A retrotransposon-driven dicer isoform directs endogenous small interfering RNA production in mouse oocytes. Cell 155: 807-816.
28. Garcia, D., Garcia, S., Pontier, D., Marchais, A., Renou, J.P., Lagrange, T., and Voinnet, O. (2012). Ago hook and RNA helicase motifs underpin dual roles for SDE3 in antiviral defense and silencing of nonconserved intergenic regions. Mol. Cell 48: 109-120.
29. Gasciolli, V., Mallory, A.C., Bartel, D.P., and Vaucheret, H. (2005). Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr. Biol. 15: 1494-1500.
30. Gehring, M., Bubb, K.L., and Henikoff, S. (2009). Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324: 1447-1451.
31. Gehring, M., Missirian, V., and Henikoff, S. (2011). Genomic analysis of parent-of-origin allelic expression in Arabidopsis thaliana seeds. PLoS One 6: e23687.
32. Gruntman, E., Qi, Y., Slotkin, R.K., Roeder, T., Martienssen, R.A., and Sachidanandam, R. (2008). Kismeth: analyzer of plant methylation states through bisulfite sequencing. BMC Bioinformatics 9: 371.
33. Haberle, V., et al. (2014). Two independent transcription initiation codes overlap on vertebrate core promoters. Nature 507: 381-385.
34. Henderson, I.R., Chan, S.R., Cao, X., Johnson, L., and Jacobsen, S.E. (2010). Accurate sodium bisulfite sequencing in plants. Epigenetics 5: 47-49.
35. Henderson, I.R., Zhang, X., Lu, C., Johnson, L., Meyers, B.C., Green, P.J., and Jacobsen, S.E. (2006). Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat. Genet. 38: 721-725.
36. Hiraguri, A., Itoh, R., Kondo, N., Nomura, Y., Aizawa, D., Murai, Y., Koiwa, H., Seki, M., Shinozaki, K., and Fukuhara, T. (2005). Specific interactions between Dicer-like proteins and HYL1/DRBfamily dsRNA-binding proteins in Arabidopsis thaliana. Plant Mol. Biol. 57: 173-188.
37. Hoffer, P., Ivashuta, S., Pontes, O., Vitins, A., Pikaard, C.,Mroczka, A., Wagner, N., and Voelker, T. (2011). Posttranscriptional gene silencing in nuclei. Proc. Natl. Acad. Sci. USA 108: 409-414.
38. Hoivik, E.A., Witsoe, S.L., Bergheim, I.R., Xu, Y., Jakobsson, I., Tengholm, A., Doskeland, S.O., and Bakke, M. (2013). DNA methylation of alternative promoters directs tissue specific expression of Epac2 isoforms. PLoS One 8: e67925.
39. Ibarra, C.A., et al. (2012). Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337: 1360-1364.
40. Jouannet, V., Moreno, A.B., Elmayan, T., Vaucheret, H., Crespi, M.D., and Maizel, A. (2012). Cytoplasmic Arabidopsis AGO7 accumulates in membrane-associated siRNA bodies and is required for ta-siRNA biogenesis. EMBO J. 31: 1704-1713.
41. Jullien, P.E., Susaki, D., Yelagandula, R., Higashiyama, T., and Berger, F. (2012). DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr. Biol. 22: 1825-1830.
42. Karimi, M., De Meyer, B., and Hilson, P. (2005). Modular cloning in plant cells. Trends Plant Sci. 10: 103-105.
43. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., and Salzberg, S.L. (2013). TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14: R36.
44. Klein-Cosson, C., Chambrier, P., Rogowsky, P.M., and Vernoud, V. (2015). Regulation of a maize HD-ZIP IV transcription factor by a non-conventional RDR2-dependent small RNA. Plant J. 81: 747-758.
45. Kosugi, S., Hasebe, M., Tomita, M., and Yanagawa, H. (2009). Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc. Natl. Acad. Sci. USA 106: 10171-10176.
46. Kumakura, N., Takeda, A., Fujioka, Y., Motose, H., Takano, R., and Watanabe, Y. (2009). SGS3 and RDR6 interact and colocalize in cytoplasmic SGS3/RDR6-bodies. FEBS Lett. 583: 1261-1266.
47. Kurtz, S., Phillippy, A., Delcher, A.L., Smoot, M., Shumway, M., Antonescu, C., and Salzberg, S.L. (2004). Versatile and open software for comparing large genomes. Genome Biol. 5: R12.
48. Laliberté, J.F., and Sanfaçon, H. (2010). Cellular remodeling during plant virus infection. Annu. Rev. Phytopathol. 48: 69-91.
49. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25.
50. Law, J.A., and Jacobsen, S.E. (2010). Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11: 204-220.
51. Lei, M., Zhang, H., Julian, R., Tang, K., Xie, S., and Zhu, J.K. (2015). Regulatory link between DNA methylation and active demethylation in Arabidopsis. Proc. Natl. Acad. Sci. USA 112: 3553-3557.
52. Love, M.I., Huber, W., and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15: 550.
53. Lu, J., Zhang, C., Baulcombe, D.C., and Chen, Z.J. (2012). Maternal siRNAs as regulators of parental genome imbalance and gene expression in endosperm of Arabidopsis seeds. Proc. Natl. Acad. Sci. USA 109: 5529-5534.
54. Ma, L., Hatlen, A., Kelly, L.J., Becher, H., Wang, W., Kovarik, A., Leitch, I.J., and Leitch, A.R. (2015). Angiosperms are unique among land plant lineages in the occurrence of key genes in the RNA-directed DNA methylation (RdDM) Pathway. Genome Biol. Evol. 7: 2648-2662.
55. Marí-Ordóñez, A., Marchais, A., Etcheverry, M., Martin, A., Colot, V., and Voinnet, O. (2013). Reconstructing de novo silencing of an active plant retrotransposon. Nat. Genet. 45: 1029-1039.
56. Martínez de Alba, A.E., Moreno, A.B., Gabriel, M., Mallory, A.C., Christ, A., Bounon, R., Balzergue, S., Aubourg, S., Gautheret, D., Crespi, M.D., Vaucheret, H., and Maizel, A. (2015). In plants, decapping prevents RDR6-dependent production of small interfering RNAs from endogenous mRNAs. Nucleic Acids Res. 43: 2902-2913.
57. McCue, A.D., Panda, K., Nuthikattu, S., Choudury, S.G., Thomas, E.N., and Slotkin, R.K. (2015). ARGONAUTE 6 bridges transposable element mRNA-derived siRNAs to the establishment of DNA methylation. EMBO J. 34: 20-35.
58. Mosher, R.A., Melnyk, C.W., Kelly, K.A., Dunn, R.M., Studholme, D.J., and Baulcombe, D.C. (2009). Uniparental expression of PolIV- dependent siRNAs in developing endosperm of Arabidopsis. Nature 460: 283-286.
59. Nuthikattu, S., McCue, A.D., Panda, K., Fultz, D., DeFraia, C., Thomas, E.N., and Slotkin, R.K. (2013). The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21-22 nucleotide small interfering RNAs. Plant Physiol. 162: 116-131.
60. Pall, G.S., and Hamilton, A.J. (2008). Improved northern blot method for enhanced detection of small RNA. Nat. Protoc. 3: 1077-1084.
61. Pélissier, T., Clavel, M., Chaparro, C., Pouch-Pélissier, M.N., Vaucheret, H., and Deragon, J.M. (2011). Double-stranded RNA binding proteins DRB2 and DRB4 have an antagonistic impact on polymerase IV-dependent siRNA levels in Arabidopsis. RNA 17: 1502-1510.
62. Pignatta, D., Erdmann, R.M., Scheer, E., Picard, C.L., Bell, G.W., and Gehring, M. (2014). Natural epigenetic polymorphisms lead to intraspecific variation in Arabidopsis gene imprinting. eLife 3: e03198.
63. Pontes, O., Li, C.F., Costa Nunes, P., Haag, J., Ream, T., Vitins, A., Jacobsen, S.E., and Pikaard, C.S. (2006). The Arabidopsis chromatinmodifying nuclear siRNA pathway involves a nucleolar RNA processing center. Cell 126: 79-92.
64. Pontier, D., et al. (2012). NERD, a plant-specific GW protein, defines an additional RNAi-dependent chromatin-based pathway in Arabidopsis. Mol. Cell 48: 121-132.
65. Pumplin, N., and Voinnet, O. (2013). RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counterdefence. Nat. Rev. Microbiol. 11: 745-760.
66. Qi, Y., Denli, A.M., and Hannon, G.J. (2005). Biochemical specialization within Arabidopsis RNA silencing pathways. Mol. Cell 19: 421-428.
67. Rajagopalan, R., Vaucheret, H., Trejo, J., and Bartel, D.P. (2006). A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 20: 3407-3425.
68. Reinders, J., Wulff, B.B., Mirouze, M., Marí-Ordóñez, A., Dapp, M., Rozhon, W., Bucher, E., Theiler, G., and Paszkowski, J. (2009). Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 23: 939-950.
69. Sarkies, P., et al. (2015). Ancient and novel small RNA pathways compensate for the loss of piRNAs in multiple independent nematode lineages. PLoS Biol. 13: e1002061.
70. Schindelin, J., et al. (2012). Fiji: an open-source platform for biologicalimage analysis. Nat. Methods 9: 676-682.
71. Schmid, M., Davison, T.S., Henz, S.R., Pape, U.J., Demar, M., Vingron, M., Schölkopf, B., Weigel, D., and Lohmann, J.U. (2005). A gene expression map of Arabidopsis thaliana development. Nat. Genet. 37: 501-506.
72. Scotto-Lavino, E., Du, G., and Frohman, M.A. (2006). 59 End cDNA amplification using classic RACE. Nat. Protoc. 1: 2555-2562.
73. Siomi, M.C., Sato, K., Pezic, D., and Aravin, A.A. (2011). PIWI-interacting small RNAs: the vanguard of genome defence. Nat. Rev. Mol. Cell Biol. 12: 246-258.
74. Slotkin, R.K., Vaughn, M., Borges, F., Tanurdzić, M., Becker, J.D., Feijó, J.A., and Martienssen, R.A. (2009). Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136: 461-472.
75. Song, L., Han, M.H., Lesicka, J., and Fedoroff, N. (2007). Arabidopsis primary microRNA processing proteins HYL1 and DCL1 define a nuclear body distinct from the Cajal body. Proc. Natl. Acad. Sci. USA 104: 5437-5442.
76. Song, X., et al. (2012). Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J. 69: 462-474.
77. Stroud, H., Do, T., Du, J., Zhong, X., Feng, S., Johnson, L., Patel, D.J., and Jacobsen, S.E. (2014). Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat. Struct. Mol. Biol. 21: 64-72.
78. Stroud, H., Greenberg, M.V., Feng, S., Bernatavichute, Y.V., and Jacobsen, S.E. (2013). Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152: 352-364.
79. Todesco, M., Rubio-Somoza, I., Paz-Ares, J., and Weigel, D. (2010). A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLoS Genet. 6: e1001031.
80. Vazquez, F., Vaucheret, H., Rajagopalan, R., Lepers, C., Gasciolli, V., Mallory, A.C., Hilbert, J.L., Bartel, D.P., and Crété, P. (2004). Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol. Cell 16: 69-79.
81. Wang, X.B., Jovel, J., Udomporn, P., Wang, Y., Wu, Q., Li, W.X., Gasciolli, V., Vaucheret, H., and Ding, S.W. (2011). 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 23: 1625-1638.
82. White, E., Schlackow, M., Kamieniarz-Gdula, K., Proudfoot, N.J., and Gullerova, M. (2014). Human nuclear Dicer restricts the deleterious accumulation of endogenous double-stranded RNA. Nat. Struct. Mol. Biol. 21: 552-559.
83. Williams, B.P., Pignatta, D., Henikoff, S., and Gehring, M. (2015). Methylation-sensitive expression of a DNA demethylase gene serves as an epigenetic rheostat. PLoS Genet. 11: e1005142.
84. Wu, L., Mao, L., and Qi, Y. (2012). Roles of dicer-like and argonaute proteins in TAS-derived small interfering RNA-triggered DNA methylation. Plant Physiol. 160: 990-999.
85. Xie, Z., Allen, E., Wilken, A., and Carrington, J.C. (2005). DICERLIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 102: 12984-12989.
86. Xie, Z., Johansen, L.K., Gustafson, A.M., Kasschau, K.D., Lellis, A.D., Zilberman, D., Jacobsen, S.E., and Carrington, J.C. (2004). Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2: E104.
87. Ye, R., Wang, W., Iki, T., Liu, C., Wu, Y., Ishikawa, M., Zhou, X., and Qi, Y. (2012). Cytoplasmic assembly and selective nuclear import of Arabidopsis Argonaute4/siRNA complexes. Mol. Cell 46: 859-870.
88. Yu, A., Lepère, G., Jay, F., Wang, J., Bapaume, L., Wang, Y., Abraham, A.L., Penterman, J., Fischer, R.L., Voinnet, O., and Navarro, L. (2013). Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc. Natl. Acad. Sci. USA 110: 2389-2394.
89. Zhu, S., Jeong, R.D., Lim, G.H., Yu, K., Wang, C., Chandra-Shekara, A.C., Navarre, D., Klessig, D.F., Kachroo, A., and Kachroo, P. (2013). Double-stranded RNA-binding protein 4 is required for resistance signaling against viral and bacterial pathogens. Cell Reports 4: 1168-1184.