Specific Tandem Repeats Are Sufficient for Paramutation-Induced Trans-Generational Silencing

English version České info

Paramutation is a well-studied epigenetic phenomenon in which trans communication between two different alleles leads to meiotically heritable transcriptional silencing of one of the alleles. Paramutation at the b1 locus involves RNA-mediated transcriptional silencing and requires specific tandem repeats that generate siRNAs. This study addressed three important questions: 1) are the tandem repeats sufficient for paramutation, 2) do they need to be in an allelic position to mediate paramutation, and 3) is there an association between the ability to mediate paramutation and repeat DNA methylation levels? Paramutation was achieved using multiple transgenes containing the b1 tandem repeats, including events with tandem repeats of only one half of the repeat unit (413 bp), demonstrating that these sequences are sufficient for paramutation and an allelic position is not required for the repeats to communicate. Furthermore, the transgenic tandem repeats increased the expression of a reporter gene in maize, demonstrating the repeats contain transcriptional regulatory sequences. Transgene-mediated paramutation required the mediator of paramutation1 gene, which is necessary for endogenous paramutation, suggesting endogenous and transgene-mediated paramutation both require an RNA-mediated transcriptional silencing pathway. While all tested repeat transgenes produced small interfering RNAs (siRNAs), not all transgenes induced paramutation suggesting that, as with endogenous alleles, siRNA production is not sufficient for paramutation. The repeat transgene-induced silencing was less efficiently transmitted than silencing induced by the repeats of endogenous b1 alleles, which is always 100% efficient. The variability in the strength of the repeat transgene-induced silencing enabled testing whether the extent of DNA methylation within the repeats correlated with differences in efficiency of paramutation. Transgene-induced paramutation does not require extensive DNA methylation within the transgene. However, increased DNA methylation within the endogenous b1 repeats after transgene-induced paramutation was associated with stronger silencing of the endogenous allele.

Vyšlo v časopise: Specific Tandem Repeats Are Sufficient for Paramutation-Induced Trans-Generational Silencing. PLoS Genet 9(10): e32767. doi:10.1371/journal.pgen.1003773
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003773

Souhrn

Zdroje

1. BrinkRA (1956) A genetic change associated with the R locus in maize which is directed and potentially reversible. Genetics 41 : 872–890.

2. CoeEH (1959) A Regular and Continuing Conversion-Type Phenomenon at the B Locus in Maize. Proc Natl Acad Sci U S A 45 : 828–832.

3. PattersonGI, ThorpeCJ, ChandlerVL (1993) Paramutation, an allelic interaction, is associated with a stable and heritable reduction of transcription of the maize b regulatory gene. Genetics 135 : 881–894.

4. HollickJB, PattersonGI, CoeEHJr, ConeKC, ChandlerVL (1995) Allelic interactions heritably alter the activity of a metastable maize pl allele. Genetics 141 : 709–719.

5. SidorenkoLV, PetersonT (2001) Transgene-induced silencing identifies sequences involved in the establishment of paramutation of the maize p1 gene. Plant Cell 13 : 319–335.

6. PiluR, PanzeriD, CassaniE, Cerino BadoneF, LandoniM, et al. (2009) A paramutation phenomenon is involved in the genetics of maize low phytic acid1-241 (lpa1-241) trait. Heredity 102 : 236–245.

7. HagemannR (1969) Somatic Conversion (Paramutation) at the Sulfurea Locus of Lycopersicon Esculentum Mill. III. Studies with Trisomics. Canadian Journal of Genetics and Cytology 11 : 346–358.

8. Mittelsten ScheidO, AfsarK, PaszkowskiJ (2003) Formation of stable epialleles and their paramutation-like interaction in tetraploid Arabidopsis thaliana. Nat Genet 34 : 450–454.

9. MeyerP, HeidmannI, NiedenhofI (1993) Differences in DNA-methylation are associated with a paramutation phenomenon in transgenic petunia. Plant J 4 : 89–100.

10. de VanssayA, BougeAL, BoivinA, HermantC, TeyssetL, et al. (2012) Paramutation in Drosophila linked to emergence of a piRNA-producing locus. Nature 490 : 112–115.

11. SuterCM, MartinDI (2010) Paramutation: the tip of an epigenetic iceberg? Trends Genet 26 : 9–14.

12. Arteaga-VazquezMA, ChandlerVL (2010) Paramutation in maize: RNA mediated trans-generational gene silencing. Curr Opin Genet Dev 20 : 156–163.

13. CoeEHJ (1966) The properties, origin and mechanism of conversion-type inheritance at the b locus in maize. Genetics 53 : 1035–1063.

14. ChandlerVL, EgglestonWB, DorweilerJE (2000) Paramutation in maize. Plant Mol Biol 43 : 121–145.

15. ErhardKFJr, HollickJB (2011) Paramutation: a process for acquiring trans-generational regulatory states. Curr Opin Plant Biol 14 : 210–216.

16. StamM (2009) Paramutation: a heritable change in gene expression by allelic interactions in trans. Mol Plant 2 : 578–588.

17. BarbourJE, LiaoIT, StonakerJL, LimJP, LeeCC, et al. (2012) required to maintain repression2 is a novel protein that facilitates locus-specific paramutation in maize. Plant Cell 24 : 1761–1775.

18. MatzkeM, KannoT, DaxingerL, HuettelB, MatzkeAJ (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21 : 367–376.

19. StamM, BeleleC, DorweilerJE, ChandlerVL (2002) Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes Dev 16 : 1906–1918.

20. StamM, BeleleC, RamakrishnaW, DorweilerJE, BennetzenJL, et al. (2002) The regulatory regions required for B' paramutation and expression are located far upstream of the maize b1 transcribed sequences. Genetics 162 : 917–930.

21. HaringM, BaderR, LouwersM, SchwabeA, van DrielR, et al. (2010) The role of DNA methylation, nucleosome occupancy and histone modifications in paramutation. Plant J 63 : 366–378.

22. LouwersM, BaderR, HaringM, van DrielR, de LaatW, et al. (2009) Tissue -⁠ and Expression Level-Specific Chromatin Looping at Maize b1 Epialleles. Plant Cell 21 : 832–842.

23. AllemanM, SidorenkoL, McGinnisK, SeshadriV, DorweilerJE, et al. (2006) An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442 : 295–298.

24. Arteaga-VazquezM, SidorenkoL, RabanalFA, ShrivistavaR, NobutaK, et al. (2010) RNA-mediated trans-communication can establish paramutation at the b1 locus in maize. Proc Natl Acad Sci U S A 107 : 12986–12991.

25. MetteMF, AufsatzW, van Der WindenJ, MatzkeMA, MatzkeAJ (2000) Transcriptional silencing and promoter methylation triggered by double -⁠ stranded RNA. Embo J 19 : 5194–5201.

26. StamM, BruinRd, KenterS, HoornRALvd, BloklandRv, et al. (1997) Post-transcriptional silencing of chalcone synthase in Petunia by inverted transgene repeats. Plant J 12 : 63–82.

27. XieZ, JohansenLK, GustafsonAM, KasschauKD, LellisAD, et al. (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2: E104.

28. BenfeyPN, RenL, ChuaN-H (1989) The CaMV 35S enhancer contains at least two domains which can confer different developmental and tissue-specific expression patterns. EMBO J 8 : 2195–2202.

29. JeffersonRA, KavanaghTA, BevanMW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. Embo J 6 : 3901–3907.

30. KilbyNJ, LeyserHMO, FurnerIJ (1992) Promoter methylation and progressive transgene inactivation in Arabidopsis. Plant Mol Biol 20 : 103–112.

31. HobbsSL, KpodarP, DeLongCM (1990) The effect of T-DNA copy number, position and methylation on reporter gene expression in tobacco transformants. Plant Mol Biol 15 : 851–864.

32. AssaadFF, TuckerKL, SignerER (1993) Epigenetic repeat-induced gene silencing (RIGS) in Arabidopsis. Plant Mol Biol 22 : 1067–1085.

33. ten LohuisM, GallianoH, HeidmannI, MeyerP (1995) Treatment with propionic and butyric acid enhances expression variegation and promoter methylation in plant transgenes. Biol Chem Hoppe Seyler 376 : 311–320.

34. CaoX, JacobsenSE (2002) Role of the arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12 : 1138–1144.

35. ChanSW, ZilbermanD, XieZ, JohansenLK, CarringtonJC, et al. (2004) RNA silencing genes control de novo DNA methylation. Science 303 : 1336.

36. ElmayanT, BalzergueS, BeonF, BourdonV, DaubremetJ, et al. (1998) Arabidopsis mutants impaired in cosuppression. Plant Cell 10 : 1747–1758.

37. KermicleJL, EgglestonWB, AllemanM (1995) Organization of paramutagenicity in R-stippled maize. Genetics 141 : 361–372.

38. PanavasT, WeirJ, WalkerEL (1999) The structure and paramutagenicity of the R-marbled haplotype of Zea mays. Genetics 153 : 979–991.

39. VillarCB, ErilovaA, MakarevichG, TroschR, KohlerC (2009) Control of PHERES1 imprinting in Arabidopsis by direct tandem repeats. Mol Plant 2 : 654–660.

40. ChanSW, ZhangX, BernatavichuteYV, JacobsenSE (2006) Two-step recruitment of RNA-directed DNA methylation to tandem repeats. PLoS Biol 4: e363.

41. LippmanZ, GendrelAV, BlackM, VaughnMW, DedhiaN, et al. (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430 : 471–476.

42. ChandlerVL (2010) Paramutation's properties and puzzles. Science 330 : 628–629.

43. MartienssenRA (2003) Maintenance of heterochromatin by RNA interference of tandem repeats. Nat Genet 35 : 213–214.

44. BrzeskaK, BrzeskiJ, SmithJ, ChandlerVL (2010) Transgenic Expression of CBBP, a CXC -Domain Protein, Establishes Paramutation in Maize. Proc Natl Acad Sci U S A 107 : 5561–5521.

45. SidorenkoL, DorweilerJE, CiganAM, Arteaga-VazquezM, VyasM, et al. (2009) A dominant mutation in mediator of paramutation2, one of three second-largest subunits of a plant-specific RNA polymerase, disrupts multiple siRNA silencing processes. PLoS Genet 5: e1000725.

46. PecinkaA, KatoN, MeisterA, ProbstAV, SchubertI, et al. (2005) Tandem repetitive transgenes and fluorescent chromatin tags alter local interphase chromosome arrangement in Arabidopsis thaliana. J Cell Sci 118 : 3751–3758.

47. RonshaugenM, LevineM (2004) Visualization of trans-homolog enhancer-promoter interactions at the Abd-B Hox locus in the Drosophila embryo. Dev Cell 7 : 925–932.

48. WatanabeK, PecinkaA, MeisterA, SchubertI, LamE (2005) DNA hypomethylation reduces homologous pairing of inserted tandem repeat arrays in somatic nuclei of Arabidopsis thaliana. Plant J 44 : 531–540.

49. BellO, TiwariVK, ThomaNH, SchubelerD (2011) Determinants and dynamics of genome accessibility. Nat Rev Genet 12 : 554–564.

50. HeintzmanND, StuartRK, HonG, FuY, ChingCW, et al. (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39 : 311–318.

51. SidorenkoL, LiX, TaglianiL, BowenB, PetersonT (1999) Characterization of the regulatory elements of the maize P-rr gene by transient expression assays. Plant Mol Biol 39 : 11–19.

52. SidorenkoLV, LiX, CoccioloneSM, ChopraS, TaglianiL, et al. (2000) Complex structure of a maize Myb gene promoter: functional analysis in transgenic plants. Plant J 22 : 471–482.

53. SidorenkoLV, ChandlerVL (2008) RNA Dependent RNA Polymerase is Required for Enhancer Mediated Transcriptional Silencing Associated with Paramutation at the Maize p1 Gene. Genetics 180 : 1983–1993.

54. ArmstrongCL, GreenCE (1985) Establishment and Maintenance of Friable, Embryogenic Maize Callus and the Involvement of L-Proline. Planta 164 : 207–214.

55. FrameBR, ZhangH, CoccioloneSM, SidorenkoLV, DietrichCR, et al. (2000) Production of transgenic maize from bombarded type II callus: effect of gold particle size and callus morphology on transformation efficiency. In Vitro and Developmental Biology-Plant 36 : 21–29.

56. StuitjeAR, VerbreeEC, van der LindenKH, MietkiewskaEM, NapJP, et al. (2003) Seed-expressed fluorescent proteins as versatile tools for easy (co)transformation and high-throughput functional genomics in Arabidopsis. Plant Biotechnol J 1 : 301–309.

57. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16 : 735–743.

58. Saghai-MaroofMA, SolimanKM, JorgensenRA, AllardRW (1984) Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci U S A 81 : 8014–8018.

59. Clarke JD (2002) Purifying DNA from Arabidopsis; Weigel D, Glazebrook J, editors. New York: Cold Spring Harbor Laboratory Press. 165–166 p.

60. AbràmoffMD, MagalhãesPJ, RamSJ (2004) Image Processing with ImageJ. Biophotonics International 11 : 36–42.

61. AnG, MitraA, ChoiHK, CostaMA, AnK, et al. (1989) Functional analysis of the 3′ control region of the potato wound-inducible proteinase inhibitor II gene. Plant Cell 1 : 115–122.

62. DorweilerJE, CareyCC, KuboKM, HollickJB, KermicleJL, et al. (2000) mediator of paramutation1 is required for establishment and maintenance of paramutation at multiple maize loci. Plant Cell 12 : 2101–2118.

63. BenfeyPN, RenL, ChuaNH (1989) The CaMV 35S enhancer contains at least two domains which can confer different developmental and tissue-specific expression patterns. EMBO J 8 : 2195–2202.