Heat-Induced Release of Epigenetic Silencing Reveals the Concealed Role of an Imprinted Plant Gene

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In plants, expression of certain imprinted genes is restricted to embryo nourishing tissue, the endosperm. Since these genes are silenced by epigenetic mechanisms during vegetative growth, it has been assumed that they have no role in this phase of the plant life cycle. Here, we report on heat-mediated release of epigenetic silencing and ectopic activation of the Arabidopsis thaliana endosperm-imprinted gene SDC. The stress induced activation of SDC involves epigenetic regulation but not the canonical heat-shock perception and signaling, and it seems to be required for efficient growth recovery after the stress. Our results exemplify a potential concealed role of an imprinted gene in plant responses to environmental challenges.

Vyšlo v časopise: Heat-Induced Release of Epigenetic Silencing Reveals the Concealed Role of an Imprinted Plant Gene. PLoS Genet 10(11): e32767. doi:10.1371/journal.pgen.1004806
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004806

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Zdroje

1. VongsA, KakutaniT, MartienssenRA, RichardsEJ (1993) Arabidopsis thaliana DNA methylation mutants. Science 260: 1926–1928.

2. MorelJB, MourrainP, BeclinC, VaucheretH (2000) DNA methylation and chromatin structure affect transcriptional and post-transcriptional transgene silencing in Arabidopsis. Curr Biol 10: 1591–1594.

3. CaoX, AufsatzW, ZilbermanD, MetteMF, HuangMS, et al. (2003) Role of the DRM and CMT3 methyltransferases in RNA-directed DNA methylation. Curr Biol 13: 2212–2217.

4. MathieuO, ReindersJ, CaikovskiM, SmathajittC, PaszkowskiJ (2007) Transgenerational stability of the Arabidopsis epigenome is coordinated by CG methylation. Cell 130: 851–862.

5. ZemachA, KimMY, HsiehPH, Coleman-DerrD, Eshed-WilliamsL, et al. (2013) The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153: 193–205.

6. CaoX, JacobsenSE (2002) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. PNAS 99: 16491–16498.

7. PikaardCS, HaagJR, ReamT, WierzbickiAT (2008) Roles of RNA polymerase IV in gene silencing. Trends Plant Sci 13: 390–397.

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

9. LischD (2009) Epigenetic regulation of transposable elements in plants. Ann Rev Plant Biol 60: 43–66.

10. RajaP, SanvilleBC, BuchmannRC, BisaroDM (2008) Viral genome methylation as an epigenetic defense against geminiviruses. J Virology 82: 8997–9007.

11. KohlerC, WolffP, SpillaneC (2012) Epigenetic mechanisms underlying genomic imprinting in plants. Ann Rev Plant Biol 63: 331–352.

12. RaissigMT, BarouxC, GrossniklausU (2011) Regulation and flexibility of genomic imprinting during seed development. Plant Cell 23: 16–26.

13. HendersonIR, JacobsenSE (2008) Tandem repeats upstream of the Arabidopsis endogene SDC recruit non-CG DNA methylation and initiate siRNA spreading. Genes & Dev 22: 1597–1606.

14. PecinkaA, DinhHQ, BaubecT, RosaM, LettnerN, et al. (2010) Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell 22: 3118–3129.

15. Lang-MladekC, PopovaO, KiokK, BerlingerM, RakicB, et al. (2010) Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in Arabidopsis. Mol Plant 3: 594–602.

16. Tittel-ElmerM, BucherE, BrogerL, MathieuO, PaszkowskiJ, et al. (2010) Stress-induced activation of heterochromatic transcription. PLoS Genet 6: e1001175.

17. WangLC, WuJR, ChangWL, YehCH, KeYT, et al. (2013) Arabidopsis HIT4 encodes a novel chromocentre-localized protein involved in the heat reactivation of transcriptionally silent loci and is essential for heat tolerance in plants. J Exp Bot 64: 1689–1701.

18. HabuY, MathieuO, TariqM, ProbstAV, SmathajittC, et al. (2006) Epigenetic regulation of transcription in intermediate heterochromatin. EMBO Rep 7: 1279–1284.

19. ListerR, O'MalleyRC, Tonti-FilippiniJ, GregoryBD, BerryCC, et al. (2008) Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell 133: 523–536.

20. YokthongwattanaC, BucherE, CaikovskiM, VaillantI, NicoletJ, et al. (2010) MOM1 and Pol-IV/V interactions regulate the intensity and specificity of transcriptional gene silencing. EMBO J 29: 340–351.

21. HongSW, VierlingE (2001) Hsp101 is necessary for heat tolerance but dispensable for development and germination in the absence of stress. Plant J 27: 25–35.

22. OhnoY, NarangajavanaJ, YamamotoA, HattoriT, KagayaY, et al. (2011) Ectopic gene expression and organogenesis in Arabidopsis mutants missing BRU1 required for genome maintenance. Genetics 189: 83–95.

23. StroudH, GreenbergMV, FengS, BernatavichuteYV, JacobsenSE (2013) Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152: 352–364.

24. HsiehTF, ShinJ, UzawaR, SilvaP, CohenS, et al. (2011) Regulation of imprinted gene expression in Arabidopsis endosperm. PNAS 108: 1755–1762.

25. VuTM, NakamuraM, CalarcoJP, SusakiD, LimPQ, et al. (2013) RNA-directed DNA methylation regulates parental genomic imprinting at several loci in Arabidopsis. Development 140: 2953–2960.

26. KilianJ, WhiteheadD, HorakJ, WankeD, WeinlS, et al. (2007) The AtGenExpress global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J 50: 347–363.

27. YehCH, KaplinskyNJ, HuC, CharngYY (2012) Some like it hot, some like it warm: phenotyping to explore thermotolerance diversity. Plant Sci 195: 10–23.

28. Van LeeneJ, WittersE, InzeD, De JaegerG (2008) Boosting tandem affinity purification of plant protein complexes. Trends Plant Sci 13: 517–520.

29. GutzatR, Mittelsten ScheidO (2012) Epigenetic responses to stress: triple defense? Curr Op Plant Biol 15: 568–573.

30. PopovaOV, DinhHQ, AufsatzW, JonakC (2013) The RdDM pathway is required for basal heat tolerance in Arabidopsis. Mol Plant 6: 396–410.

31. HuY, ZhangL, HeS, HuangM, TanJ, et al. (2012) Cold stress selectively unsilences tandem repeats in heterochromatin associated with accumulation of H3K9ac. Plant Cell Environ 35: 2130–2142.

32. DowenRH, PelizzolaM, SchmitzRJ, ListerR, DowenJM, et al. (2012) Widespread dynamic DNA methylation in response to biotic stress. PNAS 109: E2183–2191.

33. CortijoS, WardenaarR, Colomé-TatchéM, GillyA, EtcheverryM, et al. (2014) Mapping the Epigenetic Basis of Complex Traits. Science 343: 1145–1148.

34. McClungCR, DavisSJ (2010) Ambient thermometers in plants: from physiological outputs towards mechanisms of thermal sensing. Current Biol CB 20: R1086–1092.

35. SanchezDH, LippoldF, RedestigH, HannahMA, ErbanA, et al. (2008) Integrative functional genomics of salt acclimatization in the model legume Lotus japonicus. Plant J 53: 973–987.

36. DingY, FrommM, AvramovaZ (2012) Multiple exposures to drought 'train' transcriptional responses in Arabidopsis. Nat Comm 3: 740.

37. SaniE, HerzykP, PerrellaG, ColotV, AmtmannA (2013) Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biol 14: R59.

38. IwasakiM, PaszkowskiJ (2014) Identification of genes preventing transgenerational transmission of stress-induced epigenetic states. PNAS 111: 8547–8552.

39. ChodavarapuRK, FengS, BernatavichuteYV, ChenPY, StroudH, et al. (2010) Relationship between nucleosome positioning and DNA methylation. Nature 466: 388–392.

40. HuaZ, PoolJE, SchmitzRJ, SchultzMD, ShiuSH, et al. (2013) Epigenomic programming contributes to the genomic drift evolution of the F-Box protein superfamily in Arabidopsis. PNAS 110: 16927–16932.

41. JeongCW, RohH, DangTV, ChoiYD, FischerRL, et al. (2011) An E3 ligase complex regulates SET-domain polycomb group protein activity in Arabidopsis thaliana. PNAS 108: 8036–8041.

42. BemerM, GrossniklausU (2012) Dynamic regulation of Polycomb group activity during plant development. Curr Op Plant Biol 15: 523–529.

43. KankelMW, RamseyDE, StokesTL, FlowersSK, HaagJR, et al. (2003) Arabidopsis MET1 cytosine methyltransferase mutants. Genetics 163: 1109–1122.

44. OnoderaY, HaagJR, ReamT, Costa NunesP, PontesO, et al. (2005) Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120: 613–622.

45. PontierD, YahubyanG, VegaD, BulskiA, Saez-VasquezJ, et al. (2005) Reinforcement of silencing at transposons and highly repeated sequences requires the concerted action of two distinct RNA polymerases IV in Arabidopsis. Genes & Dev 19: 2030–2040.

46. NaumannK, FischerA, HofmannI, KraussV, PhalkeS, et al. (2005) Pivotal role of AtSUVH2 in heterochromatic histone methylation and gene silencing in Arabidopsis. EMBO J 24: 1418–1429.

47. AufsatzW, MetteMF, van der WindenJ, MatzkeM, MatzkeAJ (2002) HDA6, a putative histone deacetylase needed to enhance DNA methylation induced by double-stranded RNA. EMBO J 21: 6832–6841.

48. LippoldF, SanchezDH, MusialakM, SchlerethA, ScheibleW-R, et al. (2009) AtMyb41 Regulates Transcriptional and Metabolic Responses to Osmotic Stress in Arabidopsis. Plant Physiol 149: 1761–1772.

49. CzechowskiT, BariRP, StittM, ScheibleWR, UdvardiMK (2004) Real-time RT-PCR profiling of over 1400 Arabidopsis transcription factors: unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J 38: 366–379.

50. CzechowskiT, StittM, AltmannT, UdvardiMK, ScheibleWR (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139: 5–17.

51. LohseM, BolgerAM, NagelA, FernieAR, LunnJE, et al. (2012) RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res 40: W622–627.

52. UsadelB, NagelA, ThimmO, RedestigH, BlaesingOE, et al. (2005) Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses. Plant Physiol 138: 1195–1204.

53. WalterM, ChabanC, SchutzeK, BatisticO, WeckermannK, et al. (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40: 428–438.

54. HetzlJ, FoersterAM, RaidlG, Mittelsten ScheidO (2007) CyMATE: a new tool for methylation analysis of plant genomic DNA after bisulphite sequencing. Plant J 51: 526–536.

55. GruntmanE, QiY, SlotkinRK, RoederT, MartienssenRA, et al. (2008) Kismeth: analyzer of plant methylation states through bisulfite sequencing. BMC Bioinformatics 9: 371.

56. GendrelAV, LippmanZ, YordanC, ColotV, MartienssenRA (2002) Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297: 1871–1873.

57. NelsonJD, DenisenkoO, SovaP, BomsztykK (2006) Fast chromatin immunoprecipitation assay. Nucleic Acids Res 34: e2.

58. Schütze K, Harter K, Chaban C (2009) Bimolecular Fluorescence Complementation (BiFC) to Study Protein-protein Interactions in Living Plant Cells. In: Pfannschmidt T, editor. Plant Signal Transduction: Humana Press. pp.189–202.