Gene Expression and Stress Response Mediated by the Epigenetic Regulation of a Transposable Element Small RNA
The epigenetic activity of transposable elements (TEs) can influence the regulation of genes; though, this regulation is confined to the genes, promoters, and enhancers that neighbor the TE. This local cis regulation of genes therefore limits the influence of the TE's epigenetic regulation on the genome. TE activity is suppressed by small RNAs, which also inhibit viruses and regulate the expression of genes. The production of TE heterochromatin-associated endogenous small interfering RNAs (siRNAs) in the reference plant Arabidopsis thaliana is mechanistically distinct from gene-regulating small RNAs, such as microRNAs or trans-acting siRNAs (tasiRNAs). Previous research identified a TE small RNA that potentially regulates the UBP1b mRNA, which encodes an RNA–binding protein involved in stress granule formation. We demonstrate that this siRNA, siRNA854, is under the same trans-generational epigenetic control as the Athila family LTR retrotransposons from which it is produced. The epigenetic activation of Athila elements results in a shift in small RNA processing pathways, and new 21–22 nucleotide versions of Athila siRNAs are produced by protein components normally not responsible for processing TE siRNAs. This processing results in siRNA854's incorporation into ARGONAUTE1 protein complexes in a similar fashion to gene-regulating tasiRNAs. We have used reporter transgenes to demonstrate that the UPB1b 3′ untranslated region directly responds to the epigenetic status of Athila TEs and the accumulation of siRNA854. The regulation of the UPB1b 3′ untranslated region occurs both on the post-transcriptional and translational levels when Athila TEs are epigenetically activated, and this regulation results in the phenocopy of the ubp1b mutant stress-sensitive phenotype. This demonstrates that a TE's epigenetic activity can modulate the host organism's stress response. In addition, the ability of this TE siRNA to regulate a gene's expression in trans blurs the lines between TE and gene-regulating small RNAs.
Vyšlo v časopise:
Gene Expression and Stress Response Mediated by the Epigenetic Regulation of a Transposable Element Small RNA. PLoS Genet 8(2): e32767. doi:10.1371/journal.pgen.1002474
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002474
Souhrn
The epigenetic activity of transposable elements (TEs) can influence the regulation of genes; though, this regulation is confined to the genes, promoters, and enhancers that neighbor the TE. This local cis regulation of genes therefore limits the influence of the TE's epigenetic regulation on the genome. TE activity is suppressed by small RNAs, which also inhibit viruses and regulate the expression of genes. The production of TE heterochromatin-associated endogenous small interfering RNAs (siRNAs) in the reference plant Arabidopsis thaliana is mechanistically distinct from gene-regulating small RNAs, such as microRNAs or trans-acting siRNAs (tasiRNAs). Previous research identified a TE small RNA that potentially regulates the UBP1b mRNA, which encodes an RNA–binding protein involved in stress granule formation. We demonstrate that this siRNA, siRNA854, is under the same trans-generational epigenetic control as the Athila family LTR retrotransposons from which it is produced. The epigenetic activation of Athila elements results in a shift in small RNA processing pathways, and new 21–22 nucleotide versions of Athila siRNAs are produced by protein components normally not responsible for processing TE siRNAs. This processing results in siRNA854's incorporation into ARGONAUTE1 protein complexes in a similar fashion to gene-regulating tasiRNAs. We have used reporter transgenes to demonstrate that the UPB1b 3′ untranslated region directly responds to the epigenetic status of Athila TEs and the accumulation of siRNA854. The regulation of the UPB1b 3′ untranslated region occurs both on the post-transcriptional and translational levels when Athila TEs are epigenetically activated, and this regulation results in the phenocopy of the ubp1b mutant stress-sensitive phenotype. This demonstrates that a TE's epigenetic activity can modulate the host organism's stress response. In addition, the ability of this TE siRNA to regulate a gene's expression in trans blurs the lines between TE and gene-regulating small RNAs.
Zdroje
1. LanderESLintonLMBirrenBNusbaumCZodyMC 2001 Initial sequencing and analysis of the human genome. Nature 409 860 921 doi:10.1038/35057062
2. RoudierFCOAhmedIBerardCBESarazinAMary-HuardT 2011 Integrative epigenomic mapping defines four main chromatin states in Arabidopsis. EMBO J 30 1928 1938 doi:doi:10.1038/emboj.2011.103
3. SlotkinRKMartienssenR 2007 Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8 272 285 doi:10.1038/nrg2072
4. LippmanZGendrelA-VBlackMVaughnMWDedhiaN 2004 Role of transposable elements in heterochromatin and epigenetic control. Nature 430 471 476 doi:10.1038/nature02651
5. SunF-LHaynesKSimpsonCLLeeSDCollinsL 2004 cis-Acting determinants of heterochromatin formation on Drosophila melanogaster chromosome four. Mol Cell Biol 24 8210 8220 doi:10.1128/MCB.24.18.8210-8220.2004
6. AravinAASachidanandamRBourc'hisDSchaeferCPezicD 2008 A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31 785 799 doi:10.1016/j.molcel.2008.09.003
7. LawJAJacobsenSE 2010 Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet doi:10.1038/nrg2719
8. HaveckerERWallbridgeLMHardcastleTJBushMSKellyKA 2010 The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22 321 334 doi:10.1105/tpc.109.072199
9. PereiraV 2004 Insertion bias and purifying selection of retrotransposons in the Arabidopsis thaliana genome. Genome Biol 5 R79 doi:10.1186/gb-2004-5-10-r79
10. WrightDAVoytasDF 1998 Potential retroviruses in plants: Tat1 is related to a group of Arabidopsis thaliana Ty3/gypsy retrotransposons that encode envelope-like proteins. Genetics 149 703 715
11. SteimerAAmedeoPAfsarKFranszPMittelsten ScheidO 2000 Endogenous targets of transcriptional gene silencing in Arabidopsis. Plant Cell 12 1165 1178
12. SlotkinRKVaughnMBorgesFTanurdzicMBeckerJD 2009 Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136 461 472 doi:10.1016/j.cell.2008.12.038
13. ListerRO'MalleyRTonti-FilippiniJGregoryBBerryC 2008 Highly Integrated Single-Base Resolution Maps of the Epigenome in Arabidopsis. Cell 133 523 536 doi:10.1016/j.cell.2008.03.029
14. LippmanZMayBYordanCSingerTMartienssenR 2003 Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification. PLoS Biol 1 e67 doi:10.1371/journal.pbio.0000067
15. MirouzeMReindersJBucherENishimuraTSchneebergerK 2009 Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461 427 430 doi:10.1038/nature08328
16. TanurdzicMVaughnMWJiangHLeeT-JSlotkinRK 2008 Epigenomic consequences of immortalized plant cell suspension culture. PLoS Biol 6 e302 doi:10.1371/journal.pbio.0060302
17. CzechBHannonGJ 2011 Small RNA sorting: matchmaking for Argonautes. Nat Rev Genet 12 19 31 doi:10.1038/nrg2916
18. RougetCPapinCBoureuxAMeunierA-CFrancoB 2010 Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 467 1128 1132 doi:doi:10.1038/nature09465
19. WatanabeTTomizawaS-IMitsuyaKTotokiYYamamotoY 2011 Role for piRNAs and noncoding RNA in de novo DNA methylation of the imprinted mouse Rasgrf1 locus. Science 332 848 852 doi:10.1126/science.1203919
20. SmithNAEamensALWangM-B 2011 Viral small interfering RNAs target host genes to mediate disease symptoms in plants. PLoS Pathog 7 e1002022 doi:10.1371/journal.ppat.1002022
21. XieZJohansenLKGustafsonAMKasschauKDLellisAD 2004 Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2 e104 doi:10.1371/journal.pbio.0020104
22. DunoyerPBrosnanCASchottGWangYJayF 2010 An endogenous, systemic RNAi pathway in plants. EMBO J 29 1699 1712 doi:10.1038/emboj.2010.65
23. ChapmanEJCarringtonJC 2007 Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8 884 896 doi:10.1038/nrg2179
24. DunoyerPHimberCVoinnetO 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 doi:10.1038/ng1675
25. SchwachFVaistijFEJonesLBaulcombeDC 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 doi:10.1104/pp.105.063537
26. DelerisAGallego-BartolomeJBaoJKasschauKDCarringtonJC 2006 Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313 68 71 doi:10.1126/science.1128214
27. Garcia-RuizHTakedaAChapmanEJSullivanCMFahlgrenN 2010 Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip Mosaic Virus infection. Plant Cell 22 481 496 doi:10.1105/tpc.109.073056
28. DunoyerPSchottGHimberCMeyerDTakedaA 2010 Small RNA duplexes function as mobile silencing signals between plant cells. Science 328 912 916 doi:10.1126/science.1185880
29. Arteaga-VázquezMCaballero-PérezJVielle-CalzadaJ-P 2006 A family of microRNAs present in plants and animals. Plant Cell 18 3355 3369 doi:10.1105/tpc.106.044420
30. KedershaNLGuptaMLiWMillerIAndersonP 1999 RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol 147 1431 1442
31. WeberCNoverLFauthM 2008 Plant stress granules and mRNA processing bodies are distinct from heat stress granules. Plant J 56 517 530 doi:10.1111/j.1365-313X.2008.03623.x
32. MeyersBCAxtellMJBartelBBartelDPBaulcombeD 2008 Criteria for annotation of plant MicroRNAs. Plant Cell 20 3186 3190 doi:10.1105/tpc.108.064311
33. NakanoMNobutaKVemarajuKTejSSSkogenJW 2006 Plant MPSS databases: signature-based transcriptional resources for analyses of mRNA and small RNA. Nucleic Acids Res 34 D731 5 doi:10.1093/nar/gkj077
34. JohnsonLCaoXJacobsenS 2002 Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12 1360 1367
35. HirochikaHOkamotoHKakutaniT 2000 Silencing of retrotransposons in arabidopsis and reactivation by the ddm1 mutation. Plant Cell 12 357 369
36. KakutaniTJeddelohJAFlowersSKMunakataKRichardsEJ 1996 Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc Natl Acad Sci USA 93 12406 12411
37. BoutetSVazquezFLiuJBéclinCFagardM 2003 Arabidopsis HEN1: a genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus resistance. Curr Biol 13 843 848
38. KannoTHuettelBMetteMFAufsatzWJaligotE 2005 Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet 37 761 765 doi:10.1038/ng1580
39. GasciolliVMalloryACBartelDPVaucheretH 2005 Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr Biol 15 1494 1500 doi:10.1016/j.cub.2005.07.024
40. VongsAKakutaniTMartienssenRARichardsEJ 1993 Arabidopsis thaliana DNA methylation mutants. Science 260 1926 1928
41. KakutaniTMunakataKRichardsEJHirochikaH 1999 Meiotically and mitotically stable inheritance of DNA hypomethylation induced by ddm1 mutation of Arabidopsis thaliana. Genetics 151 831 838
42. TeixeiraFKHerediaFSarazinARoudierFBoccaraM 2009 A role for RNAi in the selective correction of DNA methylation defects. Science 323 1600 1604 doi:10.1126/science.1165313
43. DidianoDHobertO 2006 Perfect seed pairing is not a generally reliable predictor for miRNA-target interactions. Nat Struct Mol Biol 13 849 851 doi:10.1038/nsmb1138
44. SchwabROssowskiSRiesterMWarthmannNWeigelD 2006 Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18 1121 1133 doi:10.1105/tpc.105.039834
45. LuoZChenZ 2007 Improperly terminated, unpolyadenylated mRNA of sense transgenes is targeted by RDR6-mediated RNA silencing in Arabidopsis. Plant Cell 19 943 958 doi:10.1105/tpc.106.045724
46. LiuJ 2008 Control of protein synthesis and mRNA degradation by microRNAs. Curr Opin Cell Biol 20 214 221 Available: http://www.sciencedirect.com/science/article/pii/S095506740800015X. Accessed 30 Aug. 2011
47. Addo-QuayeCEshooTWBartelDPAxtellMJ 2008 Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18 758 762 doi:10.1016/j.cub.2008.04.042
48. GermanMAPillayMJeongD-HHetawalALuoS 2008 Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol 26 941 946 doi:10.1038/nbt1417
49. McCueADCrestiMFeijóJASlotkinRK 2011 Cytoplasmic connection of sperm cells to the pollen vegetative cell nucleus: potential roles of the male germ unit revisited. J Exp Bot 62 1621 1631 doi:10.1093/jxb/err032
50. BorgesFGomesGGardnerRMorenoNMcCormickS 2008 Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 148 1168 1181 doi:10.1104/pp.108.125229
51. BaumbergerNBaulcombeDC 2005 Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc Natl Acad Sci USA 102 11928 11933 doi:10.1073/pnas.0505461102
52. WangHZhangXLiuJKibaTWooJ 2011 Deep sequencing of small RNAs specifically associated with Arabidopsis AGO1 and AGO4 uncovers new AGO functions. Plant J 67 292 304 doi:10.1111/j.1365-313X.2011.04594.x
53. PiecykMWaxSBeckARKedershaNGuptaM 2000 TIA-1 is a translational silencer that selectively regulates the expression of TNF-alpha. EMBO J 19 4154 4163 doi:10.1093/emboj/19.15.4154
54. Eisinger-MathasonTSKAndradeJGroehlerALClarkDEMuratore-SchroederTL 2008 Codependent functions of RSK2 and the apoptosis-promoting factor TIA-1 in stress granule assembly and cell survival. Mol Cell 31 722 736 doi:10.1016/j.molcel.2008.06.025
55. ZouTYangXPanDHuangJSahinM 2011 SMN deficiency reduces cellular ability to form stress granules, sensitizing cells to stress. Cell Mol Neurobiol 31 541 550 doi:10.1007/s10571-011-9647-8
56. GilksNKedershaNAyodeleMShenLStoecklinG 2004 Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol Biol Cell 15 5383 5398 doi:10.1091/mbc.E04-08-0715
57. BuchanJRParkerR 2009 Eukaryotic stress granules: the ins and outs of translation. Mol Cell 36 932 941 doi:10.1016/j.molcel.2009.11.020
58. BeckhamCJParkerR 2008 P bodies, stress granules, and viral life cycles. Cell Host Microbe 3 206 212 doi:10.1016/j.chom.2008.03.004
59. KedershaNChoMRLiWYaconoPWChenS 2000 Dynamic shuttling of TIA-1 accompanies the recruitment of mRNA to mammalian stress granules. J Cell Biol 151 1257 1268
60. GendrelA-VLippmanZYordanCColotVMartienssenRA 2002 Dependence of heterochromatic histone H3 methylation patterns on the Arabidopsis gene DDM1. Science 297 1871 1873 doi:10.1126/science.1074950
61. WrightDAVoytasDF 2002 Athila4 of Arabidopsis and Calypso of soybean define a lineage of endogenous plant retroviruses. Genome Res 12 122 131 doi:10.1101/gr.196001
62. SlotkinRK 2010 The epigenetic control of the Athila family of retrotransposons in Arabidopsis. Epigenetics 5 483 490
63. BorsaniOZhuJVersluesPESunkarRZhuJ-K 2005 Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123 1279 1291 doi:10.1016/j.cell.2005.11.035
64. RonMAlandete-SaezMEshed-WilliamsLFletcherJCMcCormickS 2010 Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis. Genes Dev 24 1010 1021 doi:10.1101/gad.1882810
65. SongXLiPZhaiJZhouMMaL 2011 Roles of DCL4 and DCL3b in Rice Phased Small RNA Biogenesis. Plant J in press.
66. CuperusJTCarbonellAFahlgrenNGarcia-RuizHBurkeRT 2010 Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat Struct Mol Biol 17 997 1003 doi:10.1038/nsmb.1866
67. MiuraAYonebayashiSWatanabeKToyamaTShimadaH 2001 Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature 411 212 214 doi:10.1038/35075612
68. GrandbastienM-A 2004 Stress activation and genomic impact of plant retrotransposons. J Soc Biol 198 425 432
69. BeauregardACurcioMJBelfortM 2008 The take and give between retrotransposable elements and their hosts. Annu Rev Genet 42 587 617 doi:10.1146/annurev.genet.42.110807.091549
70. AparicioOCarneroEAbadXRazquinNGuruceagaE 2010 Adenovirus VA RNA-derived miRNAs target cellular genes involved in cell growth, gene expression and DNA repair. Nucleic Acids Res 38 750 763 doi:10.1093/nar/gkp1028
71. WhiteJPCardenasAMMarissenWELloydRE 2007 Inhibition of cytoplasmic mRNA stress granule formation by a viral proteinase. Cell Host Microbe 2 295 305 doi:10.1016/j.chom.2007.08.006
72. EsclatineATaddeoBRoizmanB 2004 Herpes simplex virus 1 induces cytoplasmic accumulation of TIA-1/TIAR and both synthesis and cytoplasmic accumulation of tristetraprolin, two cellular proteins that bind and destabilize AU-rich RNAs. J Virol 78 8582 8592 doi:10.1128/JVI.78.16.8582-8592.2004
73. GoodierJLZhangLVetterMRKazazianHH 2007 LINE-1 ORF1 protein localizes in stress granules with other RNA-binding proteins, including components of RNA interference RNA-induced silencing complex. Mol Cell Biol 27 6469 6483 doi:10.1128/MCB.00332-07
74. VazquezFVaucheretHRajagopalanRLepersCGasciolliV 2004 Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol Cell 16 69 79 doi:10.1016/j.molcel.2004.09.028
75. MontgomeryTAYooSJFahlgrenNGilbertSDHowellMD 2008 AGO1-miR173 complex initiates phased siRNA formation in plants. Proc Natl Acad Sci USA 105 20055 20062 doi:10.1073/pnas.0810241105
76. HutvágnerGSimardMJ 2008 Argonaute proteins: key players in RNA silencing. Nature Reviews Molecular Cell Biology 9 22 32 doi:10.1038/nrm2321
77. MiSCaiTHuYChenYHodgesE 2008 Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133 116 127 doi:10.1016/j.cell.2008.02.034
78. GrundhoffASullivanCS 2011 Virus-encoded microRNAs. Virology 411 325 343 doi:10.1016/j.virol.2011.01.002
79. PallGSCodony-ServatCByrneJRitchieLHamiltonA 2007 Carbodiimide-mediated cross-linking of RNA to nylon membranes improves the detection of siRNA, miRNA and piRNA by northern blot. Nucleic Acids Res 35 e60 doi:10.1093/nar/gkm112
80. SlotkinRKFreelingMLischD 2005 Heritable transposon silencing initiated by a naturally occurring transposon inverted duplication. Nat Genet 37 641 644 doi:10.1038/ng1576
81. SundaresanVSpringerPVolpeTHawardSJonesJD 1995 Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev 9 1797 1810
82. JeffersonRA 1987 Assaying Chimeric Genes in Plants: The GUS Gene Fusion System. Plant Molecular Biology Reporter 5 387 405
83. TwellDYamaguchiJMcCormickS 1990 Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Development 109 705 713
84. BaumbergerNTsaiC-HLieMHaveckerEBaulcombeDC 2007 The Polerovirus silencing suppressor P0 targets ARGONAUTE proteins for degradation. Curr Biol 17 1609 1614 doi:10.1016/j.cub.2007.08.039
85. KidnerCAMartienssenRA 2004 Spatially restricted microRNA directs leaf polarity through ARGONAUTE1. Nature 428 81 84 doi:10.1038/nature02366
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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