Transgenerational response to stress in plants and its application for breeding

Journal of Experimental Botany

Volumn 67, Issue 7, 2016, Pages 2081-2092

  Bilichak, Andriy ^a   Kovalchuk, Igor ^b  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

Chromatin modifications; DNA methylation; Epigenetic approach to plant engineering; Epigenetics; Plants; Small non coding rnas; Transgenerational inheritance

Indexed keywords

BREEDING; GENETIC EPIGENESIS; GENETICS; INHERITANCE; PHYSIOLOGICAL STRESS; PLANT; PLANT PHYSIOLOGY;

BREEDING; EPIGENESIS, GENETIC; INHERITANCE PATTERNS; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS; STRESS, PHYSIOLOGICAL;

EID: 84965002184     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erw066     Document Type: Review

References (115)

1. Abdelnoor RV, Yule R, Elo A, Christensen AC, Meyer-Gauen G, Mackenzie SA. 2003. Substoichiometric shifting in the plant mitochondrial genome is influenced by a gene homologous to MutS. Proceedings of the National Academy of Sciences, USA 100, 5968-5973.
2. Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796-815.
3. Ashe A, Sapetschnig A, Weick E-M, et al. 2012. piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell 150, 88-99.
4. Avramova Z. 2015. Transcriptional 'memory' of a stress: Transient chromatin and memory (epigenetic) marks at stress-response genes. The Plant Journal 83, 149-159.
5. Beaumont HJ, Gallie J, Kost C, Ferguson GC, Rainey PB. 2009. Experimental evolution of bet hedging. Nature 462, 90-93.
6. Bilichak A, Ilnystkyy Y, Hollunder J, Kovalchuk I. 2012. The progeny of Arabidopsis thaliana plants exposed to salt exhibit changes in DNA methylation, histone modifications and gene expression. PLoS One 7, e30515.
7. Bilichak A, Ilnytskyy Y, Woycicki R, Kepeshchuk N, Fogen D, Kovalchuk I. 2015. The elucidation of stress memory inheritance in Brassica rapa plants. Frontiers in Plant Science 6, 5.
8. Blodner C, Goebel C, Feussner I, Gatz C, Polle A. 2007. Warm and cold parental reproductive environments affect seed properties, fitness, and cold responsiveness in Arabidopsis thaliana progenies. Plant, Cell and Evironment 30, 165-175.
9. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C. 1998. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO Journal 17, 170-180.
10. Bologna NG, Voinnet O. 2014. The diversity, biogenesis, and activities of endogenous silencing small RNAs in Arabidopsis. Annual Review of Plant Biology 65, 473-503.
11. Bond DM, Baulcombe DC. 2014. Small RNAs and heritable epigenetic variation in plants. Trends in Cell Biology 24, 100-107.
12. Bond DM, Finnegan EJ. 2007. Passing the message on: inheritance of epigenetic traits. Trends in Plant Science 12, 211-216.
13. Boyko A, Blevins T, Yao Y, Golubov A, Bilichak A, Ilnytskyy Y, Hollunder J, Meins F Jr., Kovalchuk I. 2010b). Transgenerational adaptation of Arabidopsis to stress requires DNA methylation and the function of Dicer-like proteins. PLoS One 5, e9514.
14. Boyko A, Filkowski J, Kovalchuk I. 2005. Homologous recombination in plants is temperature and day-length dependent. Mutation Research 572, 73-83.
15. Boyko A, Golubov A, Bilichak A, Kovalchuk I. 2010a. Chlorine ions but not sodium ions alter genome stability of Arabidopsis thaliana. Plant and Cell Physiology 51, 1066-1078.
16. Boyko A, Kathiria P, Zemp FJ, Yao Y, Pogribny I, Kovalchuk I. 2007. Transgenerational changes in the genome stability and methylation in pathogen-infected plants: (virus-induced plant genome instability). Nucleic Acids Research 35, 1714-1725.
17. Boyko A, Kovalchuk I. 2011. Genome instability and epigenetic modification-heritable responses to environmental stress? Current Opinion in Plant Biology 14, 260-266.
18. 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.
19. Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J. 2008. Identification and characterization of small RNAs from the phloem of Brassica napus. The Plant Journal 53, 739-749.
20. Calarco JP, Borges F, Donoghue MT, et al. 2012. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151, 194-205.
21. Cortijo S, Wardenaar R, Colome-Tatche M, et al. 2014. Mapping the epigenetic basis of complex traits. Science 343, 1145-1148.
22. Crean AJ, Bonduriansky R. 2014. What is a paternal effect? Trends in Ecology and Evolution 29, 554-559.
23. de la Rosa Santamaria R, Shao MR, Wang G, Nino-Liu DO, Kundariya H, Wamboldt Y, Dweikat I, Mackenzie SA. 2014. MSH1- induced non-genetic variation provides a source of phenotypic diversity in Sorghum bicolor. PLoS One 9, e108407.
24. DeRose-Wilson L, Gaut BS. 2011. Mapping salinity tolerance during Arabidopsis thaliana germination and seedling growth. PLoS One 6, e22832.
25. Dickins TE, Rahman Q. 2012. The extended evolutionary synthesis and the role of soft inheritance in evolution. Proceedings of the Royal Society B: Biological Sciences 279, 2913-2921.
26. Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y. 2009. Differential expression of miRNAs in response to salt stress in maize roots. Annals of Botany 103, 29-38.
27. Donohue K. 2009. Completing the cycle: Maternal effects as the missing link in plant life histories. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 1059-1074.
28. Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, Voinnet O. 2010. Small RNA duplexes function as mobile silencing signals between plant cells. Science 328, 912-916.
29. Eichten SR, Briskine R, Song J, et al. 2013. Epigenetic and genetic influences on DNA methylation variation in maize populations. The Plant Cell 25, 2783-2797.
30. Galloway LF. 2001. The effect of maternal and paternal environments on seed characters in the herbaceous plant Campanula Americana (Campanulaceae). American Journal of Botany 88, 832-840.
31. Gao Z, Liu HL, Daxinger L, et al. 2010. An RNA polymerase II- And AGO4- Associated protein acts in RNA-directed DNA methylation. Nature 465, 106-109.
32. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. 2009. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nature Cell Biology 11, 1143-1149.
33. Gill SS, Anjum NA, Gill R, Jha M, Tuteja N. 2015. DNA damage and repair in plants under ultraviolet and ionizing radiations. Scientific World Journal 2015, 250158.
34. Graham JK, Smith ML, Simons AM. 2014. Experimental evolution of bet hedging under manipulated environmental uncertainty in Neurospora crassa. Proceedings of the Royal Society B: Biological Sciences 281, 20140706.
35. Haag JR, Pikaard CS. 2011. Multisubunit RNA polymerases IV and V: Purveyors of non-coding RNA for plant gene silencing. Nature Reviews Molecular Cell Biology 12, 483-492.
36. Hauben M, Haesendonckx B, Standaert E, et al. 2009. Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield. Proceedings of the National Academy of Sciences, USA 106, 20109-20114.
37. Hilton IB, D'Ippolito AM, Vockley CM, Thakore PI, Crawford GE, Reddy TE, Gersbach CA. 2015. Epigenome editing by a CRISPR-Cas9- based acetyltransferase activates genes from promoters and enhancers. Nature Biotechnology 33, 510-517.
38. Holliday R. 2006. Epigenetics: A historical overview. Epigenetics 1, 76-80.
39. Ingouff M, Rademacher S, Holec S, Soljic L, Xin N, Readshaw A, Foo SH, Lahouze B, Sprunck S, Berger F. 2010. Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Current Biology 20, 2137-2143.
40. Jablonka E, Lamb MJ. 2002. The changing concept of epigenetics. Annals of the New York Academy of Sciences 981, 82-96.
41. Jacobsen SE, Meyerowitz EM. 1997. Hypermethylated SUPERMAN epigenetic alleles in arabidopsis. Science 277, 1100-1103.
42. Jacobsen SE, Sakai H, Finnegan EJ, Cao X, Meyerowitz EM. 2000. Ectopic hypermethylation of flower-specific genes in Arabidopsis. Current Biology 10, 179-186.
43. Johannes F, Colomé-Tatché M. 2011. Quantitative epigenetics through epigenomic perturbation of isogenic lines. Genetics 188, 215-227.
44. Johannes F, Colot V, Jansen RC. 2008. Epigenome dynamics: A quantitative genetics perspective. Nature Reviews Genetics 9, 883-890.
45. Johannes F, Porcher E, Teixeira FK, et al. 2009. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genetics 5, e1000530.
46. Jullien PE, Berger F. 2010. DNA methylation reprogramming during plant sexual reproduction? Trends in Genetics 26, 394-399.
47. Kachroo A, Robin GP. 2013. Systemic signaling during plant defense. Current Opinion in Plant Biology 16, 527-533.
48. Kalisz S, Kramer EM. 2008. Variation and constraint in plant evolution and development. Heredity 100, 171-177.
49. Kawashima T, Berger F. 2014. Epigenetic reprogramming in plant sexual reproduction. Nature Reviews Genetics 15, 613-624.
50. Kidner CA, Martienssen RA. 2004. Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428, 81-84.
51. Kim J-M, Sasaki T, Ueda M, Sako K, Seki M. 2015. Chromatin changes in response to drought, salinity, heat, and cold stresses in plants. Frontiers in Plant Science 6, 114.
52. Kinoshita T, Miura A, Choi Y, Kinoshita Y, Cao X, Jacobsen SE, Fischer RL, Kakutani T. 2004. One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303, 521-523.
53. Kinoshita Y, Saze H, Kinoshita T, Miura A, Soppe WJ, Koornneef M, Kakutani T. 2007. Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. The Plant Journal 49, 38-45.
54. Lander ES, Linton LM, Birren B, et al. 2001. Initial sequencing and analysis of the human genome. Nature 409, 860-921.
55. Lee YS, Pressman S, Andress AP, et al. 2009. Silencing by small RNAs is linked to endosome trafficking. Nature Cell Biology 11, 1150-1156.
56. Li W-X, Oono Y, Zhu J, He X-J, Wu J-M, Iida K, Lu X-Y, Cui X, Jin H, Zhu J-K. 2008 The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. The Plant Cell 20, 2238-2251.
57. Lin S-I, Chiang S-F, Lin W-Y, Chen J-W, Tseng C-Y, Wu P-C, Chiou T-J. 2008. Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiology 147, 732-746.
58. Long L, Ou X, Liu J, Lin X, Sheng L, Liu B. 2009. The spaceflight environment can induce transpositional activation of multiple endogenous transposable elements in a genotype-dependent manner in rice. Journal of Plant Physiology 166, 2035-2045.
59. Long Y, Xia W, Li R, Wang J, Shao M, Feng J, King GJ, Meng J. 2011. Epigenetic QTL mapping in Brassica napus. Genetics 189, 1093-1102.
60. Luna E, Bruce TJ, Roberts MR, Flors V, Ton J. 2012. Next-generation systemic acquired resistance. Plant Physiology 158, 844-853.
61. Maeder ML, Angstman JF, Richardson ME, et al. 2013. Targeted DNA demethylation and endogenous gene activation using programmable TALE-TET1 fusions. Nature Biotechnology 31, 1137-1142.
62. Martienssen RA, Colot V. 2001. DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293, 1070-1074.
63. Martinez de Alba AE, Jauvion V, Mallory AC, Bouteiller N, Vaucheret H. 2011. The miRNA pathway limits AGO1 availability during siRNAmediated PTGS defense against exogenous RNA. Nucleic Acids Research 39, 9339-9344.
64. Melnyk CW, Molnar A, Baulcombe DC. 2011. Intercellular and systemic movement of RNA silencing signals. EMBO Journal 30, 3553-3563.
65. Mendenhall EM, Williamson KE, Reyon D, Zou JY, Ram O, Joung JK, Bernstein BE. 2013. Locus-specific editing of histone modifications at endogenous enhancers. Nature Biotechnology 31, 1133-1136.
66. Migicovsky Z, Kovalchuk I. 2013. Changes to DNA methylation and homologous recombination frequency in the progeny of stressed plants. Biochemistry and Cell Biology 91, 1-5.
67. Molinier J, Ries G, Zipfel C, Hohn B. 2006. Transgeneration memory of stress in plants. Nature 442, 1046-1049.
68. Morel JB, Godon C, Mourrain P, Beclin C, Boutet S, Feuerbach F, Proux F, Vaucheret H. 2002. Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post- Transcriptional gene silencing and virus resistance. The Plant Cell 14, 629-639.
69. Naydenov M, Baev V, Apostolova E, Gospodinova N, Sablok G, Gozmanova M, Yahubyan G. 2015. High- Temperature effect on genes engaged in DNA methylation and affected by DNA methylation in Arabidopsis. Plant Physiology and Biochemistry 87, 102-108.
70. Nuthikattu S, McCue AD, Panda K, Fultz D, DeFraia C, Thomas EN, Slotkin RK. 2013. The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21-22 nucleotide small interfering RNAs. Plant Physiology 162, 116-131.
71. Olofsson H, Ripa J, Jonzen N. 2009. Bet-hedging as an evolutionary game: The trade-off between egg size and number. Proceedings of the Royal Society B: Biological Sciences 276, 2963-2969.
72. Ossowski S, Schneeberger K, Lucas-Lledo JI, Warthmann N, Clark RM, Shaw RG, Weigel D, Lynch M. 2010. The rate and molecular spectrum of spontaneous mutations in Arabidopsis thaliana. Science 327, 92-94.
73. Ou X, Zhang Y, Xu C, Lin X, Zang Q, Zhuang T, Jiang L, von Wettstein D, Liu B. 2012. Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in rice (Oryza sativa L.). PLoS One 7, e41143.
74. Pant BD, Buhtz A, Kehr J, Scheible W-R. 2008. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. The Plant Journal 53, 731-738.
75. Pecinka A, Rosa M, Schikora A, Berlinger M, Hirt H, Luschnig C, Scheid OM 2009. Transgenerational stress memory is not a general response in Arabidopsis. PLoS One 4, e5202.
76. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. 2006. Membrane-derived microvesicles: important and underappreciated mediators of cell- To-cell communication. Leukemia 20, 1487-1495.
77. Reinders J, Wulff BB, Mirouze M, Mari-Ordonez A, Dapp M, Rozhon W, Bucher E, Theiler G, Paszkowski J. 2009. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes and Development 23, 939-950.
78. Richards EJ. 2009. Quantitative epigenetics: DNA sequence variation need not apply. Genes and Development 23, 1601-1605.
79. Sarkies P, Miska EA. 2014. Small RNAs break out: The molecular cell biology of mobile small RNAs. Nature Reviews Molecular Cell Biology 15, 525-535.
80. Saze H. 2008. Epigenetic memory transmission through mitosis and meiosis in plants. Seminars in Cell and Developmental Biology 19, 527-536.
81. Schmitz RJ, He Y, Valdes-Lopez O, et al. 2013a. Epigenome-wide inheritance of cytosine methylation variants in a recombinant inbred population. Genome Research 23, 1663-1674.
82. Schmitz RJ, Schultz MD, Urich MA, et al. 2013b. Patterns of population epigenomic diversity. Nature 495, 193-198.
83. Shedge V, Arrieta-Montiel M, Christensen AC, Mackenzie SA. 2007. Plant mitochondrial recombination surveillance requires unusual RecA and MutS homologs. The Plant Cell 19, 1251-1264.
84. Shedge V, Davila J, Arrieta-Montiel MP, Mohammed S, Mackenzie SA. 2010. Extensive rearrangement of the Arabidopsis mitochondrial genome elicits cellular conditions for thermotolerance. Plant Physiology 152, 1960-1970.
85. Shirayama M, Seth M, Lee H-C, Gu W, Ishidate T, Conte D Jr, Mello CC. 2012. piRNAs initiate an epigenetic memory of nonself RNA in the C. elegans germline. Cell 150, 65-77.
86. Stokes TL, Kunkel BN, Richards EJ. 2002. Epigenetic variation in Arabidopsis disease resistance. Genes and Development 16, 171-182.
87. Sunkar R, Li Y-F, Jagadeeswaran G. 2012. Functions of microRNAs in plant stress responses. Trends in Plant Science 17, 196-203.
88. Suter L, Widmer A. 2013a. Phenotypic effects of salt and heat stress over three generations in Arabidopsis thaliana. PLoS One 8, e80819.
89. Suter L, Widmer A. 2013b. Environmental heat and salt stress induce transgenerational phenotypic changes in Arabidopsis thaliana. PLoS One 8, e60364.
90. Svab Z, Maliga P. 2007. Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment. Proceedings of the National Academy of Sciences, USA 104, 7003-7008.
91. Takuno S, Gaut BS. 2013. Gene body methylation is conserved between plant orthologs and is of evolutionary consequence. Proceedings of the National Academy of Sciences, USA 110, 1797-1802.
92. Tenaillon MI, Hufford MB, Gaut BS, Ross-Ibarra J. 2011. Genome size and transposable element content as determined by high- Throughput sequencing in maize and Zea luxurians. Genome Biology and Evolution 3, 219-229.
93. Thieme CJ, Rojas-Triana M, Stecyk E, et al. 2015. Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nature Plants 1, 15025.
94. Tricker PJ. 2015. Transgenerational inheritance or resetting of stressinduced epigenetic modifications: Two sides of the same coin. Frontiers in Plant Science 6, 699.
95. Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T. 2009. Bursts of retrotransposition reproduced in Arabidopsis. Nature 461, 423-426.
96. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. 2007. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biology 9, 654-659.
97. van der Graaf A, Wardenaar R, Neumann DA, Taudt A, Shaw RG, Jansen RC, Schmitz RJ, Colome-Tatche M, Johannes F. 2015. Rate, spectrum, and evolutionary dynamics of spontaneous epimutations. Proceedings of the National Academy of Sciences, USA 112, 6676-6681.
98. Vaucheret H, Mallory AC, Bartel DP. 2006. AGO1 homeostasis entails coexpression of MIR168 and AGO1 and preferential stabilization of miR168 by AGO1. Molecular Cell 22, 129-136.
99. Vaucheret H, Vazquez F, Crete P, Bartel DP. 2004. The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes and Development 18, 1187-1197.
100. Vaughn MW, Tanurdzic M, Lippman Z, et al. 2007. Epigenetic natural variation in Arabidopsis thaliana. PLoS Biology 5, e174.
101. Verkest A, Byzova M, Martens C, et al. 2015. Selection for improved energy use efficiency and drought tolerance in canola results in distinct transcriptome and epigenome changes. Plant Physiology 168, 1338-1350.
102. Virdi KS, Laurie JD, Xu YZ, et al. 2015. Arabidopsis MSH1 mutation alters the epigenome and produces heritable changes in plant growth. Nature Communications 6, 6386.
103. Voinnet O, Baulcombe DC. 1997. Systemic signalling in gene silencing. Nature 389, 553.
104. 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.
105. Wierzbicki AT, Cocklin R, Mayampurath A, Lister R, Rowley MJ, Gregory BD, Ecker JR, Tang H, Pikaard CS. 2012. Spatial and functional relationships among Pol V- Associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes and Development 26, 1825-1836.
106. Wolf JB, Wade MJ. 2009. What are maternal effects (and what are they not)? Philosophical Transactions of the Royal Society B: Biological Sciences 364, 1107-1115.
107. Xu Y-Z, Arrieta-Montiel MP, Virdi KS, et al. 2011. MutS HOMOLOG1 is a nucleoid protein that alters mitochondrial and plastid properties and plant response to high light. The Plant Cell 23, 3428-3441.
108. Xu YZ, Santamaria Rde L, Virdi KS, et al. 2012. The chloroplast triggers developmental reprogramming when mutS HOMOLOG1 is suppressed in plants. Plant Physiology 159, 710-720.
109. Yang X, Kundariya H, Xu YZ, Sandhu A, Yu J, Hutton SF, Zhang M, Mackenzie SA 2015. MutS HOMOLOG1-derived epigenetic breeding potential in tomato. Plant Physiology 168, 222-232.
110. Yu A, Lepere G, Jay F, et al. 2013. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proceedings of the National Academy of Sciences, USA 110, 2389-2394.
111. Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, Harmer SL, Zilberman D 2013. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153, 193-205.
112. Zhai J, Liu J, Liu B, Li P, Meyers BC, Chen X, Cao X 2008. Small RNA-directed epigenetic natural variation in Arabidopsis thaliana. PLoS Genetics 4, e1000056.
113. Zheng B, Wang Z, Li S, Yu B, Liu JY, 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, 2850-2860.
114. Zheng X, Chen L, Li M, Lou Q, Xia H, Wang P, Li T, Liu H, Luo L 2013. Transgenerational variations in DNA methylation induced by drought stress in two rice varieties with distinguished difference to drought resistance. PLoS One 8, e80253.
115. Zhong SH, Liu JZ, Jin H, et al. 2013. Warm temperatures induce transgenerational epigenetic release of RNA silencing by inhibiting siRNA biogenesis in Arabidopsis. Proceedings of the National Academy of Sciences, USA 110, 9171-9176.