Small RNAs and heritable epigenetic variation in plants

Trends in Cell Biology

Volumn 24, Issue 2, 2014, Pages 100-107

  Bond, Donna M ^a   Baulcombe, David C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

DNA methylation; Epigenetics; Heritable variation; Small RNAs; Transgenerational inheritance

Indexed keywords

DNA METHYLTRANSFERASE; PLANT RNA; RNA; TRANSFER RNA;

CELL DIVISION; DNA METHYLATION; EMBRYO DEVELOPMENT; EPIGENETICS; GAMETOGENESIS; GENE EXPRESSION; GENE SILENCING; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; HERITABILITY; HYBRID; INHERITANCE; NONHUMAN; PHENOTYPE; PLANT CELL; PLANT GENETICS; PLANT GENOME; PLANT STRESS; PRIORITY JOURNAL; PROGENY; REVIEW; TRANSPOSON;

MAMMALIA;

DNA METHYLATION; EPIGENETICS; HERITABLE VARIATION; SMALL RNAS; TRANSGENERATIONAL INHERITANCE;

DNA METHYLATION; EPIGENESIS, GENETIC; GENES, PLANT; GENETIC VARIATION; PLANTS; RNA, SMALL NUCLEOLAR;

EID: 84892974070     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2013.08.001     Document Type: Review

References (77)

1. Jablonka E., Lamb M.J. Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life 2005, MIT Press.
2. Park S., Lehner B. Epigenetic epistatic interactions constrain the evolution of gene expression. Mol. Syst. Biol. 2013, 9:645-651.
3. Weigel D., Colot V. Epialleles in plant evolution. Genome Biol. 2012, 13:249-254.
4. Fedoroff N.V. Transposable elements, epigenetics, and genome evolution. Science 2012, 338:758-767.
5. Castel S.E., Martienssen R.A. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 2013, 14:100-112.
6. Baulcombe D. RNA silencing in plants. Nature 2004, 431:356-363.
7. Law J.A., Jacobsen S.E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 2010, 11:204-220.
8. Holeski L.M., et al. Transgenerational defense induction and epigenetic inheritance in plants. Trends Ecol. Evol. 2012, 27:618-626.
9. Bucher E., et al. Epigenetic control of transposon transcription and mobility in Arabidopsis. Curr. Opin. Plant Biol. 2012, 15:503-510.
10. Lisch D. Regulation of transposable elements in maize. Curr. Opin. Plant Biol. 2012, 15:511-516.
11. Haag J.R., Pikaard C.S. Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nat. Rev. Mol. Cell Biol. 2011, 12:483-492.
12. Law J.A., et al. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 2013, 10.1038/nature12178.
13. Smith L.M., et al. An SNF2 protein associated with nuclear RNA silencing and the spread of a silencing signal between cells in Arabidopsis. Plant Cell 2007, 19:1507-1521.
14. Zhang H., et al. DTF1 is a core component of RNA-directed DNA methylation and may assist in the recruitment of Pol IV. Proc. Natl. Acad. Sci. U.S.A. 2013, 10.1073/pnas.1300585110.
15. Law J.A., et al. SHH1, a homeodomain protein required for DNA methylation, as well as RDR2, RDM4, and chromatin remodeling factors, associate with RNA polymerase IV. PLoS Genet. 2011, 7:e1002195.
16. Haag J.R., et al. In vitro transcription activities of Pol IV, Pol V, and RDR2 reveal coupling of Pol IV and RDR2 for dsRNA synthesis in plant RNA silencing. Mol. Cell 2012, 48:811-818.
17. Xie Z., et al. Genetic and functional diversification of small RNA pathways in plants. PLoS Biol. 2004, 2:E104.
18. Havecker E.R., et al. The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 2010, 22:321-334.
19. Wierzbicki A.T., et al. Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 2008, 135:635-648.
20. Wierzbicki A.T., et al. RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat. Genet. 2009, 41:630-634.
21. Gao Z., et al. An RNA polymerase II- and AGO4-associated protein acts in RNA-directed DNA methylation. Nature 2010, 465:106-109.
22. Law J.A., et al. A protein complex required for polymerase V transcripts and RNA- directed DNA methylation in Arabidopsis. Curr. Biol. 2010, 20:951-956.
23. Wierzbicki A.T., et al. Spatial and functional relationships among Pol V-associated loci, Pol IV-dependent siRNAs, and cytosine methylation in the Arabidopsis epigenome. Genes Dev. 2012, 26:1825-1836.
24. Zhong X., et al. DDR complex facilitates global association of RNA polymerase V to promoters and evolutionarily young transposons. Nat. Struct. Mol. Biol. 2012, 19:870-875.
25. Pontes O., et al. RNA polymerase V functions in Arabidopsis interphase heterochromatin organization independently of the 24-nt siRNA-directed DNA methylation pathway. Mol. Plant 2009, 2:700-710.
26. Douet J., et al. A Pol V-mediated silencing, independent of RNA-directed DNA methylation, applies to 5S rDNA. PLoS Genet. 2009, 5:e1000690.
27. Nuthikattu S., et al. The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21-22 nucleotide small interfering RNAs. Plant Physiol. 2013, 162:116-131.
28. Zemach A., et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 2013, 153:193-205.
29. Zheng B., et al. Intergenic transcription by RNA polymerase II coordinates Pol IV and Pol V in siRNA-directed transcriptional gene silencing in Arabidopsis. Genes Dev. 2009, 23:2850-2860.
30. Jones L., et al. RNA-directed transcriptional gene silencing in plants can be inherited independently of the RNA trigger and requires Met1 for maintenance. Curr. Biol. 2001, 11:747-757.
31. Lu R., et al. Virus-induced gene silencing in plants. Methods 2003, 30:296-303.
32. Soppe W.J.J., et al. The late flowering phenotype of fwa mutants is caused by gain-of-function epigenetic alleles of a homeodomain gene. Mol. Cell 2000, 6:791-802.
33. Kinoshita Y., et al. Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J. 2007, 49:38-45.
34. Hollick J.B. Paramutation: a trans-homolog interaction affecting heritable gene regulation. Curr. Opin. Plant Biol. 2012, 15:536-543.
35. Alleman M., et al. An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 2006, 442:295-298.
36. Erhard K., et al. RNA polymerase IV functions in paramutation in Zea mays. Science 2009, 323:1201-1205.
37. Chan S.W-L., et al. Two-step recruitment of RNA-directed DNA methylation to tandem repeats. PLoS Biol. 2006, 4:e363.
38. Eamens A., et al. NRPD1a and NRPD1b are required to maintain post-transcriptional RNA silencing and RNA-directed DNA methylation in Arabidopsis. Plant J. 2008, 55:596-606.
39. Molnar A., et al. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 2010, 328:872-875.
40. Dunoyer P., et al. Small RNA duplexes function as mobile silencing signals between plant cells. Science 2010, 328:912-916.
41. Melnyk C.W., et al. Mobile 24 nt small RNAs direct transcriptional gene silencing in the root meristems of Arabidopsis thaliana. Curr. Biol. 2011, 21:1678-1683.
42. Dunoyer P., et al. An endogenous, systemic RNAi pathway in plants. EMBO J. 2010, 29:1699-1712.
43. Slotkin R.K., et al. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 2009, 136:461-472.
44. Zhu J-K. Active DNA demethylation mediated by DNA glycosylases. Annu. Rev. Genet. 2009, 43:143-166.
45. Schoft V.K., et al. Function of the DEMETER DNA glycosylase in the Arabidopsis thaliana male gametophyte. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:8042-8047.
46. Calarco J.P., et al. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 2012, 151:194-205.
47. Ibarra C.A., et al. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 2012, 337:1360-1364.
48. Mosher R.A., et al. Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 2009, 460:283-286.
49. Gehring M., et al. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 2009, 324:1447-1451.
50. Hsieh T-F., et al. Genome-wide demethylation of Arabidopsis endosperm. Science 2009, 324:1451-1454.
51. Mosher R.A., Melnyk C.W. siRNAs and DNA methylation: seedy epigenetics. Trends Plant Sci. 2010, 15:204-210.
52. Moritoh S., et al. Targeted disruption of an orthologue of DOMAINS REARRANGED METHYLASE 2, OsDRM2, impairs the growth of rice plants by abnormal DNA methylation. Plant J. 2012, 71:85-98.
53. International Rice Genome Sequencing Project The map-based sequence of the rice genome. Nature 2005, 436:793-800.
54. Schnable P.S., et al. The B73 maize genome: complexity, diversity, and dynamics. Science 2009, 326:1112-1115.
55. Buisine N., et al. Improved detection and annotation of transposable elements in sequenced genomes using multiple reference sequence sets. Genomics 2008, 91:467-475.
56. Lister R., et al. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 2008, 133:523-536.
57. Cokus S.J., et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 2008, 452:215-219.
58. Stroud H., et al. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 2013, 152:352-364.
59. Johannes F., et al. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 2009, 5:e1000530.
60. Reinders J., et al. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 2009, 23:939-950.
61. Roux F., et al. Genome-wide epigenetic perturbation jump-starts patterns of heritable variation found in nature. Genetics 2011, 188:1015-1017.
62. Johannes F., Colomé-Tatché M. Quantitative epigenetics through epigenomic perturbation of isogenic lines. Genetics 2011, 188:215-227.
63. Latzel V., et al. Epigenetic variation in plant responses to defence hormones. Ann. Bot. 2012, 110:1423-1428.
64. Teixeira F.K., et al. A role for RNAi in the selective correction of DNA methylation defects. Science 2009, 323:1600-1604.
65. Pavet V., et al. Arabidopsis displays centromeric DNA hypomethylation and cytological alterations of heterochromatin upon attack by Pseudomonas syringae. Mol. Plant Microbe Interact. 2006, 19:577-587.
66. Luna E., et al. Next-generation systemic acquired resistance. Plant Physiol. 2012, 158:844-853.
67. Dowen R.H., et al. Widespread dynamic DNA methylation in response to biotic stress. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:2183-2191.
68. Yu A., et al. Dynamics and biological relevance of DNA demethylation in Arabidopsis antibacterial defense. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:2389-2394.
69. Stroud H., et al. Plants regenerated from tissue culture contain stable epigenome changes in rice. eLife 2013, 2:e00354.
70. Navarro L., et al. Suppression of the microRNA pathway by bacterial effector proteins. Science 2008, 321:964-967.
71. Tian D., et al. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 2003, 423:74-77.
72. Dittrich-Reed D.R., Fitzpatrick B.M. Transgressive hybrids as hopeful monsters. Evol. Biol. 2013, 40:310-315.
73. Shivaprasad P.V., et al. Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J. 2012, 31:257-266.
74. Greaves I.K., et al. Trans chromosomal methylation in Arabidopsis hybrids. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:3570-3575.
75. McClintock B. The significance of responses of the genome to challenge. Science 1984, 226:792-801.
76. Roudier F., et al. Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J. 2011, 30:1928-1938.
77. Saze H., et al. DNA methylation in plants: relationship to small RNAs and histone modifications, and functions in transposon inactivation. Plant Cell Physiol. 2012, 53:766-784.