Abstract
RNA silencing refers to small RNA (sRNA)-directed, sequence-specific regulatory mechanisms operating in diverse eukaryotic organisms. Plants possess several genetically distinct sRNA-directed regulatory pathways that are known to operate either posttranscriptionally or transcriptionally. Over the years, the sRNA-directed posttranscriptional gene silencing (PTGS) and sRNA-directed DNA methylation (RdDM), which can lead to epigenetic transcriptional gene silencing (TGS), were considered distinct pathways with little or no interactions. Recent studies have uncovered an expression-dependent pathway termed RDR6-RdDM which involves the nuclear RNA polymerase II (Pol II), RNA-dependent RNA polymerase 6 (RDR6), and Pol V, but not Pol IV and RDR2, key components of the canonical Pol IV-, RDR2-, and DCL3-dependent RdDM (Pol IV-RdDM). The RDR6-RdDM pathway provides a mechanistic link between sRNA-directed PTGS and TGS, revealing previously unappreciated dynamic features of sRNA-directed regulation in plants. This 21- and 22-nucleotide (nt) sRNA-directed RdDM may represent a general transition step during de novo establishment of TGS through the canonical Pol IV-RdDM in plants.
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Arribas-Hernandez, L., Marchais, A., Poulsen, C., Haase, B., Hauptmann, J., Benes, V., et al. (2016). The slicer activity of ARGONAUTE1 is required specifically for the phasing, not production, of trans-acting short interfering RNAs in arabidopsis. The Plant Cell, 28(7), 1563–1580. https://doi.org/10.1105/tpc.16.00121.
Aukerman, M. J., & Sakai, H. (2003). Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. The Plant Cell, 15(11), 2730–2741. https://doi.org/10.1105/tpc.016238.
Axtell, M. J. (2013). Classification and comparison of small RNAs from plants. Annual Review of Plant Biology, 64, 137–159. https://doi.org/10.1146/annurev-arplant-050312-120043.
Axtell, M. J., Jan, C., Rajagopalan, R., & Bartel, D. P. (2006). A two-hit trigger for siRNA biogenesis in plants. Cell, 127(3), 565–577. https://doi.org/10.1016/j.cell.2006.09.032.
Bao, N., Lye, K. W., & Barton, M. K. (2004). MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome. Developmental Cell, 7(5), 653–662. https://doi.org/10.1016/j.devcel.2004.10.003.
Bologna, N. G., & Voinnet, O. (2014). The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annual Review of Plant Biology, 65, 473–503. https://doi.org/10.1146/annurev-arplant-050213-035728.
Bond, D. M., & Baulcombe, D. C. (2015). Epigenetic transitions leading to heritable, RNA-mediated de novo silencing in Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA, 112(3), 917–922. https://doi.org/10.1073/pnas.1413053112.
Bouche, N., Lauressergues, D., Gasciolli, V., & Vaucheret, H. (2006). An antagonistic function for Arabidopsis DCL2 in development and a new function for DCL4 in generating viral siRNAs. EMBO Journal, 25(14), 3347–3356. https://doi.org/10.1038/sj.emboj.7601217.
Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y. Y., Sieburth, L., et al. (2008). Widespread translational inhibition by plant miRNAs and siRNAs. Science, 320(5880), 1185–1190. https://doi.org/10.1126/science.1159151.
Chan, S. W., Zilberman, D., Xie, Z., Johansen, L. K., Carrington, J. C., & Jacobsen, S. E. (2004). RNA silencing genes control de novo DNA methylation. Science, 303(5662), 1336. https://doi.org/10.1126/science.1095989.
Chen, H. M., Chen, L. T., Patel, K., Li, Y. H., Baulcombe, D. C., & Wu, S. H. (2010). 22-Nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proceedings of the National Academy of Sciences USA, 107(34), 15269–15274. https://doi.org/10.1073/pnas.1001738107.
Chen, H. M., Li, Y. H., & Wu, S. H. (2007). Bioinformatic prediction and experimental validation of a microRNA-directed tandem trans-acting siRNA cascade in Arabidopsis. Proceedings of the National Academy of Sciences USA, 104(9), 3318–3323. https://doi.org/10.1073/pnas.0611119104.
Chen, X. M. (2004). A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science, 303(5666), 2022–2025. https://doi.org/10.1126/science.1088060.
Chitwood, D. H., Nogueira, F. T., Howell, M. D., Montgomery, T. A., Carrington, J. C., & Timmermans, M. C. (2009). Pattern formation via small RNA mobility. Genes and Development, 23(5), 549–554. https://doi.org/10.1101/gad.1770009.
Creasey, K. M., Zhai, J., Borges, F., Van Ex, F., Regulski, M., Meyers, B. C., et al. (2014). miRNAs trigger widespread epigenetically activated siRNAs from transposons in Arabidopsis. Nature, 508(7496), 411–415. https://doi.org/10.1038/nature13069.
Cuperus, J. T., Carbonell, A., Fahlgren, N., Garcia-Ruiz, H., Burke, R. T., Takeda, A., et al. (2010). Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nature Structural and Molecular Biology, 17(8), 997–1003. https://doi.org/10.1038/nsmb.1866.
Dalmay, T., Hamilton, A., Rudd, S., Angell, S., & Baulcombe, D. C. (2000). An RNA-Dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell, 101(5), 543–553. https://doi.org/10.1016/S0092-8674(00)80864-8.
de Felippes, F. F., Marchais, A., Sarazin, A., Oberlin, S., & Voinnet, O. (2017). A single miR390 targeting event is sufficient for triggering TAS3-tasiRNA biogenesis in Arabidopsis. Nucleic Acids Research, 45(9), 5539–5554. https://doi.org/10.1093/nar/gkx119.
Deleris, A., Gallego-Bartolome, J., Bao, J., Kasschau, K. D., Carrington, J. C., & Voinnet, O. (2006). Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science, 313(5783), 68–71. https://doi.org/10.1126/science.1128214.
Dukowic-Schulze, S., Sundararajan, A., Ramaraj, T., Kianian, S., Pawlowski, W. P., Mudge, J., et al. (2016). Novel meiotic miRNAs and indications for a role of phasiRNAs in meiosis. Front in Plant Sciences, 7, 762. https://doi.org/10.3389/fpls.2016.00762.
El-Shami, M., Pontier, D., Lahmy, S., Braun, L., Picart, C., Vega, D., et al. (2007). Reiterated WG/GW motifs form functionally and evolutionarily conserved ARGONAUTE-binding platforms in RNAi-related components. Genes and Development, 21(20), 2539–2544. https://doi.org/10.1101/gad.451207.
Eun, C., Lorkovic, Z. J., Naumann, U., Long, Q., Havecker, E. R., Simon, S. A., et al. (2011). AGO6 functions in RNA-mediated transcriptional gene silencing in shoot and root meristems in Arabidopsis thaliana. PLoS ONE, 6(10), e25730. https://doi.org/10.1371/journal.pone.0025730.
Fei, Q., Xia, R., & Meyers, B. C. (2013). Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. The Plant Cell, 25(7), 2400–2415. https://doi.org/10.1105/tpc.113.114652.
Fultz, D., & Slotkin, R. K. (2017). Exogenous transposable elements circumvent identity-based silencing, permitting the dissection of expression-dependent silencing. The Plant Cell, 29(2), 360–376. https://doi.org/10.1105/tpc.16.00718.
Gandikota, M., Birkenbihl, R. P., Hohmann, S., Cardon, G. H., Saedler, H., & Huijser, P. (2007). The miRNA156/157 recognition element in the 3′ UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. The Plant Journal, 49(4), 683–693. https://doi.org/10.1111/j.1365-313X.2006.02983.x.
Gasciolli, V., Mallory, A. C., Bartel, D. P., & Vaucheret, H. (2005). Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Current Biology, 15(16), 1494–1500. https://doi.org/10.1016/j.cub.2005.07.024.
Golden, T. A., Schauer, S. E., Lang, J. D., Pien, S., Mushegian, A. R., Grossniklaus, U., et al. (2002). SHORT INTEGUMENTS1/SUSPENSOR1/CARPEL FACTORY, a Dicer homolog, is a maternal effect gene required for embryo development in Arabidopsis. Plant Physiology, 130(2), 808–822. https://doi.org/10.1104/pp.003491.
Haag, J. R., & Pikaard, C. S. (2011). Multisubunit RNA polymerases IV and V: Purveyors of non-coding RNA for plant gene silencing. Nature Reviews Molecular Cell Biology, 12(8), 483–492. https://doi.org/10.1038/nrm3152.
Havecker, E. R., Wallbridge, L. M., Hardcastle, T. J., Bush, M. S., Kelly, K. A., Dunn, R. M., et al. (2010). The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. The Plant Cell, 22(2), 321–334. https://doi.org/10.1105/tpc.109.072199.
Henderson, I. R., Zhang, X., Lu, C., Johnson, L., Meyers, B. C., Green, P. J., et al. (2006). Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nature Genetics, 38(6), 721–725. https://doi.org/10.1038/ng1804.
Hou, C. Y., Lee, W. C., Chou, H. C., Chen, A. P., Chou, S. J., & Chen, H. M. (2016). Global analysis of truncated RNA ends reveals new insights into ribosome stalling in plants. The Plant Cell, 28(10), 2398–2416. https://doi.org/10.1105/tpc.16.00295.
Howell, M. D., Fahlgren, N., Chapman, E. J., Cumbie, J. S., Sullivan, C. M., Givan, S. A., et al. (2007). Genome-wide analysis of the RNA-DEPENDENT RNA POLYMERASE6/DICER-LIKE4 pathway in Arabidopsis reveals dependency on miRNA- and tasiRNA-directed targeting. The Plant Cell, 19(3), 926–942. https://doi.org/10.1105/tpc.107.050062.
Hsieh, L. C., Lin, S. I., Shih, A. C., Chen, J. W., Lin, W. Y., Tseng, C. Y., et al. (2009). Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiology, 151(4), 2120–2132. https://doi.org/10.1104/pp.109.147280.
Jauvion, V., Rivard, M., Bouteiller, N., Elmayan, T., & Vaucheret, H. (2012). RDR2 partially antagonizes the production of RDR6-dependent siRNA in sense transgene-mediated PTGS. PLoS ONE, 7(1), e29785. https://doi.org/10.1371/journal.pone.0029785.
Jones-Rhoades, M. W., Bartel, D. P., & Bartel, B. (2006). MicroRNAs and their regulatory roles in plants. Annual Review of Plant Biology, 57, 19–53. https://doi.org/10.1146/annurev.arplant.57.032905.105218.
Jouannet, V., Moreno, A. B., Elmayan, T., Vaucheret, H., Crespi, M. D., & Maizel, A. (2012). Cytoplasmic Arabidopsis AGO7 accumulates in membrane-associated siRNA bodies and is required for ta-siRNA biogenesis. EMBO Journal, 31(7), 1704–1713. https://doi.org/10.1038/emboj.2012.20.
Kanno, T., Yoshikawa, M., & Habu, Y. (2013). Locus-Specific Requirements of DDR Complexes for Gene-Body Methylation of TAS Genes in Arabidopsis thaliana. Plant Molecular Biology Reporter, 31(4), 1048–1052. https://doi.org/10.1007/s11105-012-0554-z.
Kant, S., Peng, M., & Rothstein, S. J. (2011). Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in arabidopsis. PLoS Genetics, 7(3), e1002021. https://doi.org/10.1371/journal.pgen.1002021.
Kasschau, K. D., Xie, Z., Allen, E., Llave, C., Chapman, E. J., Krizan, K. A., et al. (2003). P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA Function. Developmental Cell, 4(2), 205–217.
Kidner, C. A., & Martienssen, R. A. (2005). The role of ARGONAUTE1 (AGO1) in meristem formation and identity. Development Biology, 280(2), 504–517. https://doi.org/10.1016/j.ydbio.2005.01.031.
Lanet, E., Delannoy, E., Sormani, R., Floris, M., Brodersen, P., Crete, P., et al. (2009). Biochemical evidence for translational repression by Arabidopsis microRNAs. The Plant Cell, 21(6), 1762–1768. https://doi.org/10.1105/tpc.108.063412.
Laubinger, S., Zeller, G., Henz, S. R., Buechel, S., Sachsenberg, T., Wang, J. W., et al. (2010). Global effects of the small RNA biogenesis machinery on the Arabidopsis thaliana transcriptome. Proceedings of the National Academy of Sciences USA, 107(41), 17466–17473. https://doi.org/10.1073/pnas.1012891107.
Law, J. A., & Jacobsen, S. E. (2010). Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Reviews Genetics, 11(3), 204–220. https://doi.org/10.1038/nrg2719.
Li, S., Le, B., Ma, X., Li, S., You, C., Yu, Y., et al. (2016). Biogenesis of phased siRNAs on membrane-bound polysomes in Arabidopsis. Elife, 5, e22750. https://doi.org/10.7554/eLife.22750.
Li, S., Liu, L., Zhuang, X., Yu, Y., Liu, X., Cui, X., et al. (2013). MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell, 153(3), 562–574. https://doi.org/10.1016/j.cell.2013.04.005.
Li, S. F., Vandivier, L. E., Tu, B., Gao, L., Won, S. Y., Li, S. B., et al. (2015). Detection of Pol IV/RDR2-dependent transcripts at the genomic scale in Arabidopsis reveals features and regulation of siRNA biogenesis. Genome Research, 25(2), 235–245. https://doi.org/10.1101/gr.182238.114.
Lin, S. I., Santi, C., Jobet, E., Lacut, E., El Kholti, N., Karlowski, W. M., et al. (2010). Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant and Cell Physiology, 51(12), 2119–2131. https://doi.org/10.1093/pcp/pcq170.
Lin, W. Y., Huang, T. K., & Chiou, T. J. (2013). Nitrogen limitation adaptation, a target of microRNA827, mediates degradation of plasma membrane-localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis. The Plant Cell, 25(10), 4061–4074. https://doi.org/10.1105/tpc.113.116012.
Llave, C., Xie, Z., Kasschau, K. D., & Carrington, J. C. (2002). Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science, 297(5589), 2053–2056. https://doi.org/10.1126/science.1076311.
Luo, Z., & Chen, Z. (2007). Improperly terminated, unpolyadenylated mRNA of sense transgenes is targeted by RDR6-mediated RNA silencing in Arabidopsis. The Plant Cell, 19(3), 943–958. https://doi.org/10.1105/tpc.106.045724.
Lynn, K., Fernandez, A., Aida, M., Sedbrook, J., Tasaka, M., Masson, P., et al. (1999). The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development, 126(3), 469–481.
Mallory, A., & Vaucheret, H. (2010). Form, function, and regulation of ARGONAUTE proteins. The Plant Cell, 22(12), 3879–3889. https://doi.org/10.1105/tpc.110.080671.
Mari-Ordonez, A., Marchais, A., Etcheverry, M., Martin, A., Colot, V., & Voinnet, O. (2013). Reconstructing de novo silencing of an active plant retrotransposon. Nature Genetics, 45(9), 1029–1041. https://doi.org/10.1038/ng.2703.
Martinez de Alba, A. E., Moreno, A. B., Gabriel, M., Mallory, A. C., Christ, A., Bounon, R., et al. (2015). In plants, decapping prevents RDR6-dependent production of small interfering RNAs from endogenous mRNAs. Nucleic Acids Research, 43(5), 2902–2913. https://doi.org/10.1093/nar/gkv119.
Matzke, M. A., Kanno, T., & Matzke, A. J. M. (2015). RNA-directed DNA methylation: The evolution of a complex epigenetic pathway in flowering plants. Annual Review of Plant Biology, 66(66), 243–267. https://doi.org/10.1146/annurev-arplant-043014-114633.
Maumus, F., & Quesneville, H. (2014). Ancestral repeats have shaped epigenome and genome composition for millions of years in Arabidopsis thaliana. Nature Communications, 5, 4104. https://doi.org/10.1038/ncomms5104.
McCue, A. D., Panda, K., Nuthikattu, S., Choudury, S. G., Thomas, E. N., & Slotkin, R. K. (2015). ARGONAUTE 6 bridges transposable element mRNA-derived siRNAs to the establishment of DNA methylation. EMBO Journal, 34(1), 20–35. https://doi.org/10.15252/embj.201489499.
Melnyk, C. W., Molnar, A., & Baulcombe, D. C. (2011). Intercellular and systemic movement of RNA silencing signals. EMBO Journal, 30(17), 3553–3563. https://doi.org/10.1038/emboj.2011.274.
Mi, S. J., Cai, T., Hu, Y. G., Chen, Y., Hodges, E., Ni, F. R., et al. (2008). Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5’ terminal nucleotide. Cell, 133(1), 116–127. https://doi.org/10.1016/j.cell.2008.02.034.
Montgomery, T. A., Howell, M. D., Cuperus, J. T., Li, D. W., Hansen, J. E., Alexander, A. L., et al. (2008). Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell, 133(1), 128–141. https://doi.org/10.1016/j.cell.2008.02.033.
Mourrain, P., Beclin, C., Elmayan, T., Feuerbach, F., Godon, C., Morel, J. B., et al. (2000). Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell, 101(5), 533–542.
Nuthikattu, S., McCue, A. D., Panda, K., Fultz, D., DeFraia, C., Thomas, E. N., et al. (2013). The Initiation of Epigenetic silencing of active transposable elements is triggered by RDR6 and 21-22 nucleotide small interfering RNAs. Plant Physiology, 162(1), 116–131. https://doi.org/10.1104/pp.113.216481.
Panda, K., Ji, L., Neumann, D. A., Daron, J., Schmitz, R. J., & Slotkin, R. K. (2016). Full-length autonomous transposable elements are preferentially targeted by expression-dependent forms of RNA-directed DNA methylation. Genome Biology, 17(1), 170. https://doi.org/10.1186/s13059-016-1032-y.
Park, B. S., Seo, J. S., & Chua, N. H. (2014). NITROGEN LIMITATION ADAPTATION recruits PHOSPHATE2 to target the phosphate transporter PT2 for degradation during the regulation of Arabidopsis phosphate homeostasis. The Plant Cell, 26(1), 454–464. https://doi.org/10.1105/tpc.113.120311.
Peragine, A., Yoshikawa, M., Wu, G., Albrecht, H. L., & Poethig, R. S. (2004). SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes and Development, 18(19), 2368–2379. https://doi.org/10.1101/gad.1231804.
Pontier, D., Picart, C., Roudier, F., Garcia, D., Lahmy, S., Azevedo, J., et al. (2012). NERD, a plant-specific GW protein, defines an additional RNAi-dependent chromatin-based pathway in Arabidopsis. Molecular Cell, 48(1), 121–132. https://doi.org/10.1016/j.molcel.2012.07.027.
Poulsen, C., Vaucheret, H., & Brodersen, P. (2013). Lessons on RNA silencing mechanisms in plants from eukaryotic argonaute structures. The Plant Cell, 25(1), 22–37. https://doi.org/10.1105/tpc.112.105643.
Pyott, D. E., & Molnar, A. (2015). Going mobile: non-cell-autonomous small RNAs shape the genetic landscape of plants. Plant Biotechnology Journal, 13(3), 306–318. https://doi.org/10.1111/pbi.12353.
Qi, Y., He, X., Wang, X. J., Kohany, O., Jurka, J., & Hannon, G. J. (2006). Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature, 443(7114), 1008–1012. https://doi.org/10.1038/nature05198.
Schauer, S. E., Jacobsen, S. E., Meinke, D. W., & Ray, A. (2002). DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends in Plant Science, 7(11), 487–491.
Slotkin, R. K., Vaughn, M., Borges, F., Tanurdzic, M., Becker, J. D., Feijo, J. A., et al. (2009). Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell, 136(3), 461–472. https://doi.org/10.1016/j.cell.2008.12.038.
Soppe, W. J. J., Jacobsen, S. E., Alonso-Blanco, C., Jackson, J. P., Kakutani, T., Koornneef, M., et al. (2000). The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Molecular Cell, 6(4), 791–802. https://doi.org/10.1016/S1097-2765(05)00090-0.
Stroud, H., Do, T., Du, J., Zhong, X., Feng, S., Johnson, L., et al. (2014). Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nature Structural and Molecular Biology, 21(1), 64–72. https://doi.org/10.1038/nsmb.2735.
Sunkar, R., Chinnusamy, V., Zhu, J. H., & Zhu, J. K. (2007). Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. Trends in Plant Science, 12(7), 301–309. https://doi.org/10.1016/j.tplants.2007.05.001.
Takeda, A., Iwasaki, S., Watanabe, T., Utsumi, M., & Watanabe, Y. (2008). The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant and Cell Physiology, 49(4), 493–500. https://doi.org/10.1093/pcp/pcn043.
Teixeira, F. K., Heredia, F., Sarazin, A., Roudier, F., Boccara, M., Ciaudo, C., et al. (2009). A role for RNAi in the selective correction of DNA methylation defects. Science, 323(5921), 1600–1604. https://doi.org/10.1126/science.1165313.
Vaucheret, H. (2008). Plant ARGONAUTES. Trends in Plant Science, 13(7), 350–358. https://doi.org/10.1016/j.tplants.2008.04.007.
Vazquez, F., Vaucheret, H., Rajagopalan, R., Lepers, C., Gasciolli, V., Mallory, A. C., et al. (2004). Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Molecular Cell, 16(1), 69–79. https://doi.org/10.1016/j.molcel.2004.09.028.
Vidal, E. A., Araus, V., Lu, C., Parry, G., Green, P. J., Coruzzi, G. M., et al. (2010). Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA, 107(9), 4477–4482. https://doi.org/10.1073/pnas.0909571107.
Voinnet, O. (2009). Origin, biogenesis, and activity of plant microRNAs. Cell, 136(4), 669–687. https://doi.org/10.1016/j.cell.2009.01.046.
Vongs, A., Kakutani, T., Martienssen, R. A., & Richards, E. J. (1993). Arabidopsis thaliana DNA methylation mutants. Science, 260(5116), 1926–1928.
Wang, F., & Axtell, M. J. (2017). AGO4 is specifically required for heterochromatic siRNA accumulation at Pol V-dependent loci in Arabidopsis thaliana. The Plant Journal, 90(1), 37–47. https://doi.org/10.1111/tpj.13463.
Wendte, J. M., Haag, J. R., Singh, J., McKinlay, A., Pontes, O. M., & Pikaard, C. S. (2017). Functional dissection of the Pol V largest subunit CTD in RNA-directed DNA methylation. Cell Reports, 19(13), 2796–2808. https://doi.org/10.1016/j.celrep.2017.05.091.
Wu, L., Mao, L., & Qi, Y. (2012). Roles of dicer-like and argonaute proteins in TAS-derived small interfering RNA-triggered DNA methylation. Plant Physiology, 160(2), 990–999. https://doi.org/10.1104/pp.112.200279.
Xie, Z., Allen, E., Fahlgren, N., Calamar, A., Givan, S. A., & Carrington, J. C. (2005). Expression of Arabidopsis MIRNA genes. Plant Physiology, 138(4), 2145–2154. https://doi.org/10.1104/pp.105.062943.
Xie, Z., Jia, G., & Ghosh, A. (2012). Small RNAs in Plants. In R. Sunkar (ed.), MicroRNAs in plant development and stress responses. Signaling and communication in plants (vol. 15, pp. 1–28). https://doi.org/10.1007/978-3-642-27384-1_1.
Xie, Z., Johansen, L. K., Gustafson, A. M., Kasschau, K. D., Lellis, A. D., Zilberman, D., et al. (2004). Genetic and functional diversification of small RNA pathways in plants. PLoS Biology, 2(5), E104. https://doi.org/10.1371/journal.pbio.0020104.
Yamasaki, H., Abdel-Ghany, S. E., Cohu, C. M., Kobayashi, Y., Shikanai, T., & Pilon, M. (2007). Regulation of copper homeostasis by micro-RNA in Arabidopsis. Journal of Biological Chemistry, 282(22), 16369–16378. https://doi.org/10.1074/jbc.M700138200.
Yang, Z. Y., Ebright, Y. W., Yu, B., & Chen, X. M. (2006). HEN1 recognizes 21-24 nt small RNA duplexes and deposits a methyl group onto the 2 ‘ OH of the 3 ‘ terminal nucleotide. Nucleic Acids Research, 34(2), 667–675. https://doi.org/10.1093/nar/gkj474.
Ye, R., Wang, W., Iki, T., Liu, C., Wu, Y., Ishikawa, M., et al. (2012). Cytoplasmic assembly and selective nuclear import of Arabidopsis Argonaute4/siRNA complexes. Molecular Cell, 46(6), 859–870. https://doi.org/10.1016/j.molcel.2012.04.013.
Yoshikawa, M., Iki, T., Numa, H., Miyashita, K., Meshi, T., & Ishikawa, M. (2016). A short open reading frame encompassing the MicroRNA173 Target site plays a role in trans-acting small interfering RNA biogenesis. Plant Physiology, 171(1), 359–368. https://doi.org/10.1104/pp.16.00148.
Yoshikawa, M., Peragine, A., Park, M. Y., & Poethig, R. S. (2005). A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes and Development, 19(18), 2164–2175. https://doi.org/10.1101/gad.1352605.
Yu, B., Bi, L., Zhai, J., Agarwal, M., Li, S., Wu, Q., et al. (2010). siRNAs compete with miRNAs for methylation by HEN1 in Arabidopsis. Nucleic Acids Research, 38(17), 5844–5850. https://doi.org/10.1093/nar/gkq348.
Yu, B., Yang, Z. Y., Li, J. J., Minakhina, S., Yang, M. C., Padgett, R. W., et al. (2005). Methylation as a crucial step in plant microRNA biogenesis. Science, 307(5711), 932–935. https://doi.org/10.1126/science.1107130.
Zemach, A., Kim, M. Y., Hsieh, P. H., Coleman-Derr, D., Eshed-Williams, L., Thao, K., et al. (2013). The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell, 153(1), 193–205. https://doi.org/10.1016/j.cell.2013.02.033.
Zhai, J., Bischof, S., Wang, H., Feng, S., Lee, T. F., Teng, C., et al. (2015). A one precursor one siRNA Model for Pol IV-dependent siRNA biogenesis. Cell, 163(2), 445–455. https://doi.org/10.1016/j.cell.2015.09.032.
Zhang, C., Ng, D. W., Lu, J., & Chen, Z. J. (2012). Roles of target site location and sequence complementarity in trans-acting siRNA formation in Arabidopsis. The Plant Journal, 69(2), 217–226. https://doi.org/10.1111/j.1365-313X.2011.04783.x.
Zheng, B., Wang, Z., Li, S., Yu, B., Liu, J. Y., & Chen, X. (2009). Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes and Development, 23(24), 2850–2860. https://doi.org/10.1101/gad.1868009.
Zheng, X., Zhu, J., Kapoor, A., & Zhu, J. K. (2007). Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO Journal, 26(6), 1691–1701. https://doi.org/10.1038/sj.emboj.7601603.
Zhong, X., Hale, C. J., Law, J. A., Johnson, L. M., Feng, S., Tu, A., et al. (2012). DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nature Structural and Molecular Biology, 19(9), 870–875. https://doi.org/10.1038/nsmb.2354.
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We thank Chris Rock for critically reading the manuscript. We apologize to colleagues whose relevant work could not be covered due to space limitations.
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Xie, Z., Cheng, H. Interplay and transition between small RNA-directed posttranscriptional and transcriptional gene silencing in plants. Ind J Plant Physiol. 22, 371–381 (2017). https://doi.org/10.1007/s40502-017-0337-5
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DOI: https://doi.org/10.1007/s40502-017-0337-5