RNA silencing movement in plants

Journal of Integrative Plant Biology

Volumn 58, Issue 4, 2016, Pages 328-342

  Mermigka, Glykeria ^a   Verret, Frédéric ^b   Kalantidis, Kriton ^a,b  

^a UNIVERSITY OF CRETE   (Greece)

^b INSTITUTE OF MOLECULAR BIOLOGY AND BIOTECHNOLOGY   (Greece)

Author keywords

Cell non autonomous; Plant RNA silencing; Post transcriptional gene silencing; RNA interference; Short range silencing spread; Systemic silencing; Transcriptional gene silencing

Indexed keywords

CELL ORGANELLE; GENE EXPRESSION; GROWTH RESPONSE; MOLECULAR ANALYSIS; PLANT; RNA;

ANIMALIA; EMBRYOPHYTA;

ANIMAL; GENETICS; INSECT; METABOLISM; PHYSIOLOGY; PLANT; PLANT GENE; RNA INTERFERENCE; RNA TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; GENES, PLANT; INSECTS; PLANTS; RNA INTERFERENCE; RNA TRANSPORT; SIGNAL TRANSDUCTION;

EID: 84952836599     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/jipb.12423     Document Type: Article

References (159)

1. Adenot X, Elmayan T, Lauressergues D, Boutet S, Bouche N, Gasciolli V, Vaucheret H ( 2006) DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr Biol 16: 927-932
2. Alcazar RM, Lin R, Fire AZ ( 2008) Transmission dynamics of heritable silencing induced by double-stranded RNA in Caenorhabditis elegans. Genetics 180: 1275-1288
3. Allen E, Xie Z, Gustafson AM, Carrington JC ( 2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121: 207-221
4. Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, Mitchell PS, Bennett CF, Pogosova-Agadjanyan EL, Stirewalt DL, Tait JF, Tewari M ( 2011) Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA 108: 5003-5008
5. Ashe A, Belicard T, Le Pen J, Sarkies P, Frezal L, Lehrbach NJ, Felix MA, Miska EA ( 2013) A deletion polymorphism in the Caenorhabditis elegans RIG-I homolog disables viral RNA dicing and antiviral immunity. Elife 2:e00994
6. Ashe A, Sapetschnig A, Weick EM, Mitchell J, Bagijn MP, Cording AC, Doebley AL, Goldstein LD, Lehrbach NJ, Le Pen J, Pintacuda G, Sakaguchi A, Sarkies P, Ahmed S, Miska EA ( 2012) piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell 150: 88-99
7. Bai S, Kasai A, Yamada K, Li T, Harada T ( 2011) A mobile signal transported over a long distance induces systemic transcriptional gene silencing in a grafted partner. J Exp Bot 62: 4561-4570
8. Bartel DP ( 2004) MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297
9. Baulcombe D ( 1999) Viruses and gene silencing in plants. Arch Virol Suppl 15: 189-201
10. Baulcombe DC ( 2006) Short silencing RNA: The dark matter of genetics? Cold Spring Harb Symp Quant Biol 71: 13-20
11. Benkovics AH, Timmermans MC ( 2014) Developmental patterning by gradients of mobile small RNAs. Curr Opin Genet Dev 27C: 83-91
12. Bhogale S, Mahajan AS, Natarajan B, Rajabhoj M, Thulasiram HV, Banerjee AK ( 2014) MicroRN A156: A potential graft-transmissible microRNA that modulates plant architecture and tuberization in Solanum tuberosum ssp. andigena. Plant Physiol 164: 1011-1027
13. Bond DM, Baulcombe DC ( 2015) Epigenetic transitions leading to heritable, RNA-mediated de novo silencing in Arabidopsis thaliana. Proc Natl Acad Sci USA 112: 917-922
14. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O ( 2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320: 1185-1190
15. Brosnan CA, Mitter N, Christie M, Smith NA, Waterhouse PM, Carroll BJ ( 2007) Nuclear gene silencing directs reception of long-distance mRNA silencing in Arabidopsis. Proc Natl Acad Sci USA 104: 14741-14746
16. Brosnan CA, Voinnet O ( 2011) Cell-to-cell and long-distance siRNA movement in plants: Mechanisms and biological implications. Curr Opin Plant Biol 14: 580-587
17. Buckley BA, Burkhart KB, Gu SG, Spracklin G, Kershner A, Fritz H, Kimble J, Fire A, Kennedy S ( 2012) A nuclear Argonaute promotes multigenerational epigenetic inheritance and germline immortality. Nature 489: 447-451
18. Buhtz A, Pieritz J, Springer F, Kehr J ( 2010) Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10: 64
19. Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J ( 2008) Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53: 739-749
20. Calarco JP, Borges F, Donoghue MT, Van Ex F, Jullien PE, Lopes T, Gardner R, Berger F, Feijo JA, Becker JD, Martienssen RA ( 2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151: 194-205
21. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vaten A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN ( 2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465: 316-321
22. Chen X ( 2005) MicroRNA biogenesis and function in plants. FEBS Lett 579: 5923-5931
23. Chen X ( 2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25: 21-44
24. Chen X, Liang H, Zhang J, Zen K, Zhang CY ( 2012) Secreted microRNAs: A new form of intercellular communication. Trends Cell Biol 22: 125-132
25. Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC ( 2009) Pattern formation via small RNA mobility. Genes Dev 23: 549-554
26. Crete P, Leuenberger S, Iglesias VA, Suarez V, Schob H, Holtorf H, van Eeden S, Meins F ( 2001) Graft transmission of induced and spontaneous post-transcriptional silencing of chitinase genes. Plant J 28: 493-501
27. Dadami E, Moser M, Zwiebel M, Krczal G, Wassenegger M, Dalakouras A ( 2013) An endogene-resembling transgene delays the onset of silencing and limits siRNA accumulation. FEBS Lett 587: 706-710
28. Daxinger L, Kanno T, Bucher E, van der Winden J, Naumann U, Matzke AJ, Matzke M ( 2009) A stepwise pathway for biogenesis of 24-nt secondary siRNAs and spreading of DNA methylation. EMBO J 28: 48-57
29. de Felippes FF, Ott F, Weigel D ( 2011) Comparative analysis of non-autonomous effects of tasiRNAs and miRNAs in Arabidopsis thaliana. Nucleic Acids Res 39: 2880-2889
30. Dunoyer P, Brosnan CA, Schott G, Wang Y, Jay F, Alioua A, Himber C, Voinnet O ( 2010a) An endogenous, systemic RNAi pathway in plants. EMBO J 29: 1699-1712
31. Dunoyer P, Himber C, Ruiz-Ferrer V, Alioua A, Voinnet O ( 2007) Intra- and intercellular RNA interference in Arabidopsis thaliana requires components of the microRNA and heterochromatic silencing pathways. Nat Genet 39: 848-856
32. Dunoyer P, Himber C, 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
33. Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O ( 2010b) Small RNA duplexes function as mobile silencing signals between plant cells. Science 328: 912-916
34. Dunoyer P, Voinnet O ( 2009) Movement of RNA silencing between plant cells: Is the question now behind us? Trends Plant Sci 14: 643-644
35. Duxbury MS, Ashley SW, Whang EE ( 2005) RNA interference: A mammalian SID-1 homologue enhances siRNA uptake and gene silencing efficacy in human cells. Biochem Biophys Res Commun 331: 459-463
36. Dzitoyeva S, Dimitrijevic N, Manev H ( 2001) Intra-abdominal injection of double-stranded RNA into anesthetized adult Drosophila triggers RNA interference in the central nervous system. Mol Psychiatry 6: 665-670
37. Elhassan MO, Christie J, Duxbury MS ( 2012) Homo sapiens systemic RNA interference-defective-1 transmembrane family member 1 (SIDT1) protein mediates contact-dependent small RNA transfer and microRNA-21-driven chemoresistance. J Biol Chem 287: 5267-5277
38. Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, Lovat F, Fadda P, Mao C, Nuovo GJ, Zanesi N, Crawford M, Ozer GH, Wernicke D, Alder H, Caligiuri MA, Nana-Sinkam P, Perrotti D, Croce CM ( 2012) MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA 109: E2110-2116
39. Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC ( 2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16: 939-944
40. Felix MA, Ashe A, Piffaretti J, Wu G, Nuez I, Belicard T, Jiang Y, Zhao G, Franz CJ, Goldstein LD, Sanroman M, Miska EA, Wang D ( 2011) Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses. PLoS Biol 9: e1000586
41. Gasciolli V, Mallory AC, Bartel DP, 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
42. Gu SG, Pak J, Guang S, Maniar JM, Kennedy S, Fire A ( 2012) Amplification of siRNA in Caenorhabditis elegans generates a transgenerational sequence-targeted histone H3 lysine 9 methylation footprint. Nat Genet 44: 157-164
43. Guang S, Bochner AF, Burkhart KB, Burton N, Pavelec DM, Kennedy S ( 2010) Small regulatory RNAs inhibit RNA polymerase II during the elongation phase of transcription. Nature 465: 1097-1101
44. Guang S, Bochner AF, Pavelec DM, Burkhart KB, Harding S, Lachowiec J, Kennedy S ( 2008) An Argonaute transports siRNAs from the cytoplasm to the nucleus. Science 321: 537-541
45. Ha M, Kim VN ( 2014) Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 15: 509-524
46. Hamilton A, Voinnet O, Chappell L, Baulcombe D ( 2002) Two classes of short interfering RNA in RNA silencing. EMBO J 21: 4671-4679
47. Havecker ER, Wallbridge LM, Hardcastle TJ, Bush MS, Kelly KA, Dunn RM, Schwach F, Doonan JH, Baulcombe DC ( 2010) The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22: 321-334
48. He L, Hannon GJ ( 2004) MicroRNAs: Small RNAs with a big role in gene regulation. Nat Rev Genet 5: 522-531
49. Himber C, Dunoyer P, Moissiard G, Ritzenthaler C, Voinnet O ( 2003) Transitivity-dependent and -independent cell-to-cell movement of RNA silencing. EMBO J 22: 4523-4533
50. Hinas A, Wright AJ, Hunter CP ( 2012) SID-5 is an endosome-associated protein required for efficient systemic RNAi in C. elegans. Curr Biol 22: 1938-1943
51. Hunter CP, Winston WM, Molodowitch C, Feinberg EH, Shih J, Sutherlin M, Wright AJ, Fitzgerald MC ( 2006) Systemic RNAi in Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol 71: 95-100
52. Jones-Rhoades MW, Bartel DP, Bartel B ( 2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57: 19-53
53. Jones AL, Thomas CL, Maule AJ ( 1998) De novo methylation and co-suppression induced by a cytoplasmically replicating plant RNA virus. EMBO J 17: 6385-6393
54. Jose AM, Garcia GA, Hunter CP ( 2011) Two classes of silencing RNAs move between Caenorhabditis elegans tissues. Nat Struct Mol Biol 18: 1184-1188
55. Jose AM, Kim YA, Leal-Ekman S, Hunter CP ( 2012) Conserved tyrosine kinase promotes the import of silencing RNA into Caenorhabditis elegans cells. Proc Natl Acad Sci USA 109: 14520-14525
56. Jose AM, Smith JJ, Hunter CP ( 2009) Export of RNA silencing from C. elegans tissues does not require the RNA channel SID-1. Proc Natl Acad Sci USA 106: 2283-2288
57. Kalantidis K, Schumacher HT, Alexiadis T, Helm JM ( 2008) RNA silencing movement in plants. Biol Cell 100: 13-26
58. Kalantidis K, Tsagris M, Tabler M ( 2006) Spontaneous short-range silencing of a GFP transgene in Nicotiana benthamiana is possibly mediated by small quantities of siRNA that do not trigger systemic silencing. Plant J 45: 1006-1016
59. Kanazawa A, Inaba J, Shimura H, Otagaki S, Tsukahara S, Matsuzawa A, Kim BM, Goto K, Masuta C ( 2011) Virus-mediated efficient induction of epigenetic modifications of endogenous genes with phenotypic changes in plants. Plant J 65: 156-168
60. Kasai A, Kanehira A, Harada T ( 2010) miR172 Can Move Long Distances in Nicotiana benthamiana. Open Plant Sci J 4: 1-6
61. Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, Krizan KA, Carrington JC ( 2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction. Dev Cell 4: 205-217
62. Kehr J, Buhtz A ( 2008) Long distance transport and movement of RNA through the phloem. J Exp Bot 59: 85-92
63. Kim VN, Han J, Siomi MC ( 2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10: 126-139
64. Knauer S, Holt AL, Rubio-Somoza I, Tucker EJ, Hinze A, Pisch M, Javelle M, Timmermans MC, Tucker MR, Laux T ( 2013) A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Dev Cell 24: 125-132
65. Kobayashi K, Zambryski P ( 2007) RNA silencing and its cell-to-cell spread during Arabidopsis embryogenesis. Plant J 50: 597-604
66. Kotakis C, Vrettos N, Daskalaki MG, Kotzabasis K, Kalantidis K ( 2011) DCL3 and DCL4 are likely involved in the light intensity-RNA silencing cross talk in Nicotiana benthamiana. Plant Signal Behav 6: 1180-1182
67. Kotakis C, Vrettos N, Kotsis D, Tsagris M, Kotzabasis K, Kalantidis K ( 2010) Light intensity affects RNA silencing of a transgene in Nicotiana benthamiana plants. BMC Plant Biol 10: 220. doi: 10.1186/1471-2229-10-220
68. Lai EC ( 2005) miRNAs: Whys and wherefores of miRNA-mediated regulation. Curr Biol 15: R458-460
69. Le Masson I, Jauvion V, Bouteiller N, Rivard M, Elmayan T, Vaucheret H ( 2012) Mutations in the Arabidopsis H3K4me2/3 demethylase JMJ14 suppress posttranscriptional gene silencing by decreasing transgene transcription. Plant Cell 24: 3603-3612
70. Lehmann SM, Kruger C, Park B, Derkow K, Rosenberger K, Baumgart J, Trimbuch T, Eom G, Hinz M, Kaul D, Habbel P, Kalin R, Franzoni E, Rybak A, Nguyen D, Veh R, Ninnemann O, Peters O, Nitsch R, Heppner FL, Golenbock D, Schott E, Ploegh HL, Wulczyn FG, Lehnardt S ( 2012) An unconventional role for miRNA: Let-7 activates Toll-like receptor 7 and causes neurodegeneration. Nat Neurosci 15: 827-835
71. Liang D, White RG, Waterhouse PM ( 2012) Gene silencing in Arabidopsis spreads from the root to the shoot, through a gating barrier, by template-dependent, nonvascular, cell-to-cell movement. Plant Physiol 159: 984-1000
72. Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY, Wu PC, Chiou TJ ( 2008) Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147: 732-746
73. Llave C, Kasschau KD, Rector MA, Carrington JC ( 2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14: 1605-1619
74. Lu R, Maduro M, Li F, Li HW, Broitman-Maduro G, Li WX, Ding SW ( 2005) Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 436: 1040-1043
75. Lucas WJ, Ham BK, Kim JY ( 2009) Plasmodesmata - bridging the gap between neighboring plant cells. Trends Cell Biol 19: 495-503
76. Marin-Gonzalez E, Suarez-Lopez P ( 2012) " And yet it moves": Cell-to-cell and long-distance signaling by plant microRNAs. Plant Sci 196: 18-30
77. Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume L, Crespi MD, Maizel A ( 2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22: 1104-1117
78. Martin A, Adam H, Diaz-Mendoza M, Zurczak M, Gonzalez-Schain ND, Suarez-Lopez P ( 2009) Graft-transmissible induction of potato tuberization by the microRNA miR172. Development 136: 2873-2881
79. Matzke MA, Mosher RA ( 2014) RNA-directed DNA methylation: An epigenetic pathway of increasing complexity. Nat Rev Genet 15: 394-408
80. Maule AJ, Benitez-Alfonso Y, Faulkner C ( 2011) Plasmodesmata - membrane tunnels with attitude. Curr Opin Plant Biol 14, 683-690
81. McEwan DL, Weisman AS, Hunter CP ( 2012) Uptake of extracellular double-stranded RNA by SID-2. Mol Cell 47: 746-754
82. Megraw M, Baev V, Rusinov V, Jensen ST, Kalantidis K, Hatzigeorgiou AG ( 2006) MicroRNA promoter element discovery in Arabidopsis. RNA 12: 1612-1619
83. Meister G, Tuschl T ( 2004) Mechanisms of gene silencing by double-stranded RNA. Nature 431: 343-349
84. Mello CC, Conte D, Jr. ( 2004) Revealing the world of RNA interference. Nature 431: 338-342
85. Melnyk CW, Molnar A, Bassett A, Baulcombe DC ( 2011a) Mobile 24 nt small RNAs direct transcriptional gene silencing in the root meristems of Arabidopsis thaliana. Curr Biol 21: 1678-1683
86. Melnyk CW, Molnar A, Baulcombe DC ( 2011b) Intercellular and systemic movement of RNA silencing signals. EMBO J 30: 3553-3563
87. Mermigka G, Verret F, Kalantidis K ( 2015) RNA silencing movement in plants. Reviews in Cell Biology and Molecular Medicine. John Wiley & Sons, pp. 96-129
88. Mittelbrunn M, Gutierrez-Vazquez C, Villarroya-Beltri C, Gonzalez S, Sanchez-Cabo F, Gonzalez MA, Bernad A, Sanchez-Madrid F ( 2011) Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells. Nat Commun 2: 282
89. Mittelbrunn M, Sanchez-Madrid F ( 2012) Intercellular communication: Diverse structures for exchange of genetic information. Nat Rev Mol Cell Biol 13: 328-335
90. Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC ( 2010) Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328: 872-875
91. Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC ( 2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133: 128-141
92. Mosher RA, Schwach F, Studholme D, Baulcombe DC ( 2008) PolIVb influences RNA-directed DNA methylation independently of its role in siRNA biogenesis. Proc Natl Acad Sci USA 105: 3145-3150
93. Murchison EP, Hannon GJ ( 2004) miRNAs on the move: MiRNA biogenesis and the RNAi machinery. Curr Opin Cell Biol 16: 223-229
94. Ohshima K, Inoue K, Fujiwara A, Hatakeyama K, Kanto K, Watanabe Y, Muramatsu K, Fukuda Y, Ogura S, Yamaguchi K, Mochizuki T ( 2010) Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS ONE 5:e13247
95. Olmedo-Monfil V, Duran-Figueroa N, Arteaga-Vazquez M, Demesa-Arevalo E, Autran D, Grimanelli D, Slotkin RK, Martienssen RA, Vielle-Calzada JP ( 2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464: 628-632
96. Opalka N, Brugidou C, Bonneau C, Nicole M, Beachy RN, Yeager M, Fauquet C ( 1998) Movement of rice yellow mottle virus between xylem cells through pit membranes. Proc Natl Acad Sci USA 95: 3323-3328
97. Overhoff M, Sczakiel G ( 2005) Phosphorothioate-stimulated uptake of short interfering RNA by human cells. EMBO Rep 6: 1176-1181
98. Pak J, Fire A ( 2007) Distinct populations of primary and secondary effectors during RNAi in C. elegans. Science 315: 241-244
99. Palauqui JC, Balzergue S ( 1999) Activation of systemic acquired silencing by localised introduction of DNA. Curr Biol 9: 59-66
100. Palauqui JC, Elmayan T, Pollien JM, Vaucheret H ( 1997) Systemic acquired silencing: Transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J 16: 4738-4745
101. Pant BD, Buhtz A, Kehr J, Scheible WR ( 2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53: 731-738
102. Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR ( 2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150: 1541-1555
103. Parrish S, Fire A ( 2001) Distinct roles for RDE-1 and RDE-4 during RNA interference in Caenorhabditis elegans. RNA 7: 1397-1402
104. Patil BL, Fauquet CM ( 2015) Light intensity and temperature affect systemic spread of silencing signal in transient agroinfiltration studies. Mol Plant Pathol 16: 484-494
105. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans ES, Lindenberg JL, de Gruijl TD, Wurdinger T, Middeldorp JM ( 2010) Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA 107: 6328-6333
106. Peragine A, Yoshikawa M, Wu G, Albrecht HL, Poethig RS ( 2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18: 2368-2379
107. Pyott DE, Molnar A ( 2015) Going mobile: Non-cell-autonomous small RNAs shape the genetic landscape of plants. Plant Biotechnol J 13: 306-318
108. Qi Y, He X, Wang XJ, Kohany O, Jurka J, Hannon GJ ( 2006) Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443: 1008-1012
109. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP ( 2002) Prediction of plant microRNA targets. Cell 110: 513-520
110. Roberts AG, Cruz SS, Roberts IM, Prior D, Turgeon R, Oparka KJ ( 1997) Phloem unloading in sink leaves of Nicotiana benthamiana: Comparison of a fluorescent solute with a fluorescent virus. Plant Cell 9: 1381-1396
111. Rodriguez-Medina C, Atkins CA, Mann AJ, Jordan ME, Smith PM ( 2011) Macromolecular composition of phloem exudate from white lupin (Lupinus albus L.). BMC Plant Biol 11: 36
112. Roignant JY, Carre C, Mugat B, Szymczak D, Lepesant JA, Antoniewski C ( 2003) Absence of transitive and systemic pathways allows cell-specific and isoform-specific RNAi in Drosophila. RNA 9: 299-308
113. Saleh MC, van Rij RP, Hekele A, Gillis A, Foley E, O'Farrell PH, Andino R ( 2006) The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat Cell Biol 8: 793-802
114. Samuel CE ( 2001) Antiviral actions of interferons. Clin Microbiol Rev 14: 778-809
115. Sarkies P, Miska EA ( 2014) Small RNAs break out: The molecular cell biology of mobile small RNAs. Nat Rev Mol Cell Biol 15: 525-535
116. Schott DH, Cureton DK, Whelan SP, Hunter CP ( 2005) An antiviral role for the RNA interference machinery in Caenorhabditis elegans. Proc Natl Acad Sci USA 102: 18420-18424
117. Schwab R, Maizel A, Ruiz-Ferrer V, Garcia D, Bayer M, Crespi M, Voinnet O, Martienssen RA ( 2009) Endogenous TasiRNAs mediate non-cell autonomous effects on gene regulation in Arabidopsis thaliana. PLoS ONE 4:e5980
118. Schwach F, Vaistij FE, Jones L, Baulcombe DC ( 2005) An RNA-dependent RNA polymerase prevents meristem invasion by potato virus X and is required for the activity but not the production of a systemic silencing signal. Plant Physiol 138: 1842-1852
119. Searle IR, Pontes O, Melnyk CW, Smith LM, Baulcombe DC ( 2010) JMJ14, a JmjC domain protein, is required for RNA silencing and cell-to-cell movement of an RNA silencing signal in Arabidopsis. Genes Dev 24: 986-991
120. Sijen T, Fleenor J, Simmer F, Thijssen KL, Parrish S, Timmons L, Plasterk RH, Fire A ( 2001) On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107: 465-476
121. Sijen T, Steiner FA, Thijssen KL, Plasterk RH ( 2007) Secondary siRNAs result from unprimed RNA synthesis and form a distinct class. Science 315: 244-247
122. Siomi H, Siomi MC ( 2010) Posttranscriptional regulation of microRNA biogenesis in animals. Mol Cell 38: 323-332
123. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT, Jr., Carter BS, Krichevsky AM, Breakefield XO ( 2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10: 1470-1476
124. Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijo JA, Martienssen RA ( 2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136: 461-472
125. Smith LM, Pontes O, Searle I, Yelina N, Yousafzai FK, Herr AJ, Pikaard CS, Baulcombe DC ( 2007) An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 19: 1507-1521
126. Sohn SH, Frost J, Kim YH, Choi SK, Lee Y, Seo MS, Lim SH, Choi Y, Kim KH, Lomonossoff G ( 2014) Cell-autonomous-like silencing of GFP-partitioned transgenic Nicotiana benthamiana. J Exp Bot 65: 4271-4283
127. Szittya G, Silhavy D, Molnar A, Havelda Z, Lovas A, Lakatos L, Banfalvi Z, Burgyan J ( 2003) Low temperature inhibits RNA silencing-mediated defence by the control of siRNA generation. EMBO J 22: 633-640
128. Tabara H, Sarkissian M, Kelly WG, Fleenor J, Grishok A, Timmons L, Fire A, Mello CC ( 1999) The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99: 123-132
129. Tomoyasu Y, Denell RE ( 2004) Larval RNAi in Tribolium (Coleoptera) for analyzing adult development. Dev Genes Evol 214: 575-578
130. Tournier B, Tabler M, Kalantidis K ( 2006) Phloem flow strongly influences the systemic spread of silencing in GFP Nicotiana benthamiana plants. Plant J 47: 383-394
131. Turchinovich A, Burwinkel B ( 2012) Distinct AGO1 and AGO2 associated miRNA profiles in human cells and blood plasma. RNA Biol 9: 1066-1075
132. Turchinovich A, Samatov TR, Tonevitsky AG, Burwinkel B ( 2013) Circulating miRNAs: Cell-cell communication function? Front Genet 4:119
133. Turchinovich A, Weiz L, Langheinz A, Burwinkel B ( 2011) Characterization of extracellular circulating microRNA. Nucleic Acids Res 39: 7223-7233
134. Turnbull CG, Lopez-Cobollo RM ( 2013) Heavy traffic in the fast lane: Long-distance signalling by macromolecules. New Phytol 198: 33-51
135. Ulvila J, Parikka M, Kleino A, Sormunen R, Ezekowitz RA, Kocks C, Ramet M ( 2006) Double-stranded RNA is internalized by scavenger receptor-mediated endocytosis in Drosophila S2 cells. J Biol Chem 281: 14370-14375
136. Vaistij FE, Jones L, Baulcombe DC ( 2002) Spreading of RNA targeting and DNA methylation in RNA silencing requires transcription of the target gene and a putative RNA-dependent RNA polymerase. Plant Cell 14: 857-867
137. Valoczi A, Varallyay E, Kauppinen S, Burgyan J, Havelda Z ( 2006) Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. Plant J 47: 140-151
138. Varkonyi-Gasic E, Gould N, Sandanayaka M, Sutherland P, MacDiarmid RM ( 2010) Characterisation of microRNAs from apple (Malus domestica 'Royal Gala') vascular tissue and phloem sap. BMC Plant Biol 10: 159
139. Vasale JJ, Gu W, Thivierge C, Batista PJ, Claycomb JM, Youngman EM, Duchaine TF, Mello CC, Conte D, Jr. ( 2010) Sequential rounds of RNA-dependent RNA transcription drive endogenous small-RNA biogenesis in the ERGO-1/Argonaute pathway. Proc Natl Acad Sci USA 107: 3582-3587
140. Vazquez F, Vaucheret H, Rajagopalan R, Lepers C, Gasciolli V, Mallory AC, Hilbert JL, Bartel DP, Crete P ( 2004) Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16: 69-79
141. Verchot J, Driskel BA, Zhu Y, Hunger RM, Littlefield LJ ( 2001) Evidence that soilborne wheat mosaic virus moves long distance through the xylem in wheat. Protoplasma 218: 57-66
142. Voinnet O ( 2005) Non-cell autonomous RNA silencing. FEBS Lett 579: 5858-5871
143. Voinnet O, Baulcombe DC ( 1997) Systemic signalling in gene silencing. Nature 389:553
144. Voinnet O, Lederer C, Baulcombe DC ( 2000) A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103: 157-167
145. Voinnet O, Vain P, Angell S, Baulcombe DC ( 1998) Systemic spread of sequence-specific transgene RNA degradation in plants is initiated by localized introduction of ectopic promoterless DNA. Cell 95: 177-187
146. 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
147. Wierzbicki AT, Ream TS, Haag JR, Pikaard CS ( 2009) RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat Genet 41: 630-634
148. Wilkins C, Dishongh R, Moore SC, Whitt MA, Chow M, Machaca K ( 2005) RNA interference is an antiviral defence mechanism in Caenorhabditis elegans. Nature 436: 1044-1047
149. Wingard SA ( 1928) Hosts and symptoms of ring spot, a virus disease of plants. J Agric Res 37: 127-153
150. Winston WM, Sutherlin M, Wright AJ, Feinberg EH, Hunter CP ( 2007) Caenorhabditis elegans SID-2 is required for environmental RNA interference. Proc Natl Acad Sci USA 104: 10565-10570
151. Xie Z, Allen E, Fahlgren N, Calamar A, Givan SA, Carrington JC ( 2005a) Expression of Arabidopsis MIRNA genes. Plant Physiol 138: 2145-2154
152. Xie Z, Allen E, Wilken A, Carrington JC ( 2005b) DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc Natl Acad Sci USA 102: 12984-12989
153. Xin H, Li Y, Buller B, Katakowski M, Zhang Y, Wang X, Shang X, Zhang ZG, Chopp M ( 2012) Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells 30: 1556-1564
154. Yigit E, Batista PJ, Bei Y, Pang KM, Chen CC, Tolia NH, Joshua-Tor L, Mitani S, Simard MJ, Mello CC ( 2006) Analysis of the C. elegans Argonaute family reveals that distinct Argonautes act sequentially during RNAi. Cell 127: 747-757
155. Yoo BC, Kragler F, Varkonyi-Gasic E, Haywood V, Archer-Evans S, Lee YM, Lough TJ, Lucas WJ ( 2004) A systemic small RNA signaling system in plants. Plant Cell 16: 1979-2000
156. Yoshikawa M, Peragine A, Park MY, Poethig RS ( 2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19: 2164-2175
157. Zhang W, Kollwig G, Stecyk E, Apelt F, Dirks R, Kragler F ( 2014) Graft-transmissible movement of inverted-repeat-induced siRNA signals into flowers. Plant J 80: 106-121
158. Zheng X, Zhu J, Kapoor A, Zhu JK ( 2007) Role of Arabidopsis AGO6 in siRNA accumulation, DNA methylation and transcriptional gene silencing. EMBO J 26: 1691-1701
159. Zilberman D, Cao X, Jacobsen SE ( 2003) ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science 299: 716-719