RRP6L1 and RRP6L2 Function in Silencing Regulation of Antisense RNA Synthesis
Arabidopsis FLOWERING LOCUS C (FLC) delays flowering; therefore, repressing expression of FLC provides a critical mechanism to regulate flowering. This mechanism involves multiple levels of regulation, including genetic regulation by transcription factors, and epigenetic regulation by modifications of genomic DNA and histones at the FLC locus. This work examines the role of non-coding RNAs in the epigenetic regulation of FLC, finding that the different RNAs produced from the FLC locus may have different functions in altering the epigenetic landscape at the FLC locus, and revealing that AtRRP6L1 and AtRRP6L2, two components of the exosome, an RNA-processing complex, play roles in regulating these non-coding RNAs. Therefore, this work explores the complex ties between RNA processing, non-coding RNAs, and epigenetic regulation of FLC, a key repressor of flowering.
Vyšlo v časopise:
RRP6L1 and RRP6L2 Function in Silencing Regulation of Antisense RNA Synthesis. PLoS Genet 10(9): e32767. doi:10.1371/journal.pgen.1004612
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004612
Souhrn
Arabidopsis FLOWERING LOCUS C (FLC) delays flowering; therefore, repressing expression of FLC provides a critical mechanism to regulate flowering. This mechanism involves multiple levels of regulation, including genetic regulation by transcription factors, and epigenetic regulation by modifications of genomic DNA and histones at the FLC locus. This work examines the role of non-coding RNAs in the epigenetic regulation of FLC, finding that the different RNAs produced from the FLC locus may have different functions in altering the epigenetic landscape at the FLC locus, and revealing that AtRRP6L1 and AtRRP6L2, two components of the exosome, an RNA-processing complex, play roles in regulating these non-coding RNAs. Therefore, this work explores the complex ties between RNA processing, non-coding RNAs, and epigenetic regulation of FLC, a key repressor of flowering.
Zdroje
1. MarcheseFP, HuarteM (2014) Long non-coding RNAs and chromatin modifiers: Their place in the epigenetic code. Epigenetics 9: 21–26 doi:10.4161/epi.27472
2. CedarH, BergmanY (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 10: 295–304 doi:10.1038/nrg2540
3. MatzkeMA, BirchlerJA (2005) RNAi-mediated pathways in the nucleus. Nat Rev Genet 6: 24–35 doi:10.1038/nrg1500
4. BühlerM, HaasW, GygiSP, MoazedD (2007) RNAi-Dependent and -Independent RNA Turnover Mechanisms Contribute to Heterochromatic Gene Silencing. Cell 129: 707–721 doi:10.1016/j.cell.2007.03.038
5. MitchellP, EP, ShevchenkoA, MannM, TollerveyD (1997) The Exosome: A Conserved Eukaryotic RNA Processing Complex Containing Multiple 3″→5″ Exoribonucleases. Cell 91: 457–466.
6. BurkardKTD, ButlerJS (2000) A Nuclear 3″-5″ Exonuclease Involved in mRNA Degradation Interacts with Poly(A) Polymerase and the hnRNA Protein Npl3p. Molecular and Cellular Biology 20: 604–616 doi:10.1128/MCB.20.2.604-616.2000
7. ChekanovaJA, ShawRJ, WillsMA, BelostotskyDA (2000) Poly(A) Tail-dependent Exonuclease AtRrp41p from Arabidopsis thaliana Rescues 5.8 S rRNA Processing and mRNA Decay Defects of the Yeast ski6 Mutant and Is Found in an Exosome-sized Complex in Plant and Yeast Cells. Journal of Biological Chemistry 275: 33158–33166 doi:10.1074/jbc.M005493200
8. ChekanovaJA, GregoryBD, ReverdattoSV, ChenH, KumarR, et al. (2007) Genome-Wide High-Resolution Mapping of Exosome Substrates Reveals Hidden Features in the Arabidopsis Transcriptome. Cell 131: 1340–1353 doi:10.1016/j.cell.2007.10.056
9. BelostotskyDA, SieburthLE (2009) Kill the messenger: mRNA decay and plant development. Current Opinion in Plant Biology 12: 96–102 doi:10.1016/j.pbi.2008.09.003
10. LorentzenE, WalterP, FribourgS, Evguenieva-HackenbergE, KlugG, et al. (2005) The archaeal exosome core is a hexameric ring structure with three catalytic subunits. Nat Struct Mol Biol 12: 575–581 doi:10.1038/nsmb952
11. BelostotskyD (2009) Exosome complex and pervasive transcription in eukaryotic genomes. Current Opinion in Cell Biology 21: 352–358 doi:10.1016/j.ceb.2009.04.011
12. JanuszykK, LimaCD (2011) STRUCTURAL COMPONENTS AND ARCHITECTURES OF RNA EXOSOMES. Adv Exp Med Biol 702: 9–28.
13. ChlebowskiA, TomeckiR, Gas LópezME, SéraphinB, DziembowskiA (2011) CATALYTIC PROPERTIES OF THE EUKARYOTIC EXOSOME. Adv Exp Med Biol 702: 63–78.
14. BriggsMW, BurkardKTD, ButlerJS (1998) Rrp6p, the Yeast Homologue of the Human PM-Scl 100-kDa Autoantigen, Is Essential for Efficient 5.8 S rRNA 3′ End Formation. Journal of Biological Chemistry 273: 13255–13263.
15. AllmangC, KufelJ, ChanfreauG, MitchellP, EP, et al. (1999) Functions of the exosome in rRNA, snoRNA and snRNA synthesis. The EMBO Journal 18: 15399–54102.
16. ButlerJS, MitchellP (2011) Rrp6, Rrp47 AND COFACTORS OF THE NUCLEAR EXOSOME. Adv Exp Med Biol 702: 91–104.
17. CallahanKP, ButlerJS (2008) Evidence for core exosome independent function of the nuclear exoribonuclease Rrp6p. Nucleic Acids Research 36: 6645–6655 doi:10.1093/nar/gkn743
18. GrahamAC, KissDL, AndrulisED (2009) Core Exosome-independent Roles for Rrp6 in Cell Cycle Progression. Molecular Biology of the Cell 20: 2242–2253 doi:10.1091/mbc.E08
19. KissDL, AndrulisED (2010) Genome-wide analysis reveals distinct substrate specificities of Rrp6, Dis3, and core exosome subunits. RNA 16: 781–791 doi:10.1261/rna.1906710
20. LangeH, HolecS, CognatV, PieuchotL, Le RetM, et al. (2008) Degradation of a Polyadenylated rRNA Maturation By-Product Involves One of the Three RRP6-Like Proteins in Arabidopsis thaliana. Molecular and Cellular Biology 28: 3038–3044 doi:10.1128/MCB.02064-07
21. CamblongJ, IglesiasN, FickentscherC, DieppoisG, StutzF (2007) Antisense RNA Stabilization Induces Transcriptional Gene Silencing via Histone Deacetylation in S. cerevisiae. Cell 131: 706–717 doi:10.1016/j.cell.2007.09.014
22. VasiljevaL, KimM, TerziN, SoaresLM, BuratowskiS (2008) Transcription Termination and RNA Degradation Contribute to Silencing of RNA Polymerase II Transcription within Heterochromatin. Molecular Cell 29: 313–323 doi:10.1016/j.molcel.2008.01.011
23. ZofallM, FischerT, ZhangK, ZhouM, CuiB, et al. (2009) Histone H2A.Z cooperates with RNAi and heterochromatin factors to suppress antisense RNAs. Nature 461: 419–422 doi:10.1038/nature08321
24. ZofallM, YamanakaS, Reyes-TurcuFE, ZhangK, RubinC, et al. (2012) RNA Elimination Machinery Targeting Meiotic mRNAs Promotes Facultative Heterochromatin Formation. Science 335: 96–100 doi:10.1126/science.1211651
25. BühlerM, SpiesN, BartelDP, MoazedD (2008) TRAMP-mediated RNA surveillance prevents spurious entry of RNAs into the Schizosaccharomyces pombe siRNA pathway. Nat Struct Mol Biol 15: 1015–1023 doi:10.1038/nsmb.1481
26. BernardP, DrogatJ, DheurS, GenierS, JaverzatJP (2010) Splicing Factor Spf30 Assists Exosome-Mediated Gene Silencing in Fission Yeast. Molecular and Cellular Biology 30: 1145–1157 doi:10.1128/MCB.01317-09
27. Reyes-TurcuFE, ZhangK, ZofallM, ChenE, GrewalSIS (2011) Defects in RNA quality control factors reveal RNAi-independent nucleation of heterochromatin. Nat Struct Mol Biol 18: 1132–1138 doi:10.1038/nsmb.2122
28. UhlerJP, HertelC, SvejstrupJQ (2007) A role for noncoding transcription in activation of the yeast PHO5 gene. PNAS 104: 8011–8016.
29. HouseleyJ, KotovicK, HageAE, DT (2007) Trf4 targets ncRNAs from telomeric and rDNA spacer regions and functions in rDNA copy number control. The EMBO Journal 26: 4996–5006.
30. CamblongJ, BeyrouthyN, GuffantiE, SchlaepferG, SteinmetzLM, et al. (2009) Trans-acting antisense RNAs mediate transcriptional gene cosuppression in S. cerevisiae. Genes & Development 23: 1534–1545 doi:10.1101/gad.522509
31. ShinJ-H, WangH-LV, LeeJ, DinwiddieBL, BelostotskyDA, et al. (2013) The Role of the Arabidopsis Exosome in siRNA–Independent Silencing of Heterochromatic Loci. PLoS Genet 9: e1003411 doi:10.1371/journal.pgen.1003411.s007
32. MichaelsSD, AmazinoRM (1999) FLOWERING LOCUS C Encodes a Novel MADS Domain Protein That Acts as a Repressor of Flowering. The Plant Cell 11: 949–956.
33. SheldonCC, RouseDT, FinneganEJ, PeacockWJ, DennisES (2000) The molecular basis of vernalization: The central role of FLOWERING LOCUS C (FLC). PNAS 97: 3753–3758.
34. ShindoC, AranzanaMJ, ListerC, BaxterC, NichollsC, et al. (2005) Role of FRIGIDA and FLOWERING LOCUS C in Determining Variation in Flowering Time of Arabidopsis. PLANT PHYSIOLOGY 138: 1163–1173 doi:10.1104/pp.105.061309
35. AmasinoRM, MichaelsSD (2010) The Timing of Flowering. PLANT PHYSIOLOGY 154: 516–520 doi:10.1104/pp.110.161653
36. HeY (2012) Chromatin regulation of flowering. Trends in Plant Science 17: 556–562 doi:10.1016/j.tplants.2012.05.001
37. IetswaartR, WuZ, DeanC (2012) Flowering time control: another window to the connection between antisense RNA and chromatin. Trends in Genetics 28: 445–453 doi:10.1016/j.tig.2012.06.002
38. LiuF, MarquardtS, ListerC, SwiezewskiS, DeanC (2010) Targeted 3′ Processing of Antisense Transcripts Triggers Arabidopsis FLC Chromatin Silencing. Science 327: 94–97 doi:10.1126/science.1180278
39. LiuF, QuesadaV, CrevillénP, BäurleI, SwiezewskiS, et al. (2007) The Arabidopsis RNA-Binding Protein FCA Requires a Lysine-Specific Demethylase 1 Homolog to Downregulate FLC. Molecular Cell 28: 398–407 doi:10.1016/j.molcel.2007.10.018
40. HeoJB, SungS (2011) Vernalization-Mediated Epigenetic Silencing by a Long Intronic Noncoding RNA. Science 331: 76–79 doi:10.1126/science.1197349
41. KimD-H, SungS (2012) Environmentally coordinated epigenetic silencing of FLC by protein and long noncoding RNA components. Current Opinion in Plant Biology 15: 51–56 doi:10.1016/j.pbi.2011.10.004
42. SwiezewskiS, LiuF, MagusinA, DeanC (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462: 799–802 doi:10.1038/nature08618
43. HelliwellCA, RobertsonM, FinneganEJ, BuzasDM, DennisES (2011) Vernalization-Repression of Arabidopsis FLC Requires Promoter Sequences but Not Antisense Transcripts. PLoS ONE 6: e21513 doi:10.1371/journal.pone.0021513.s003
44. HeY, MichaeliSD, AmasinoRM (2003) Regulation of Flowering Time by Histone Acetylation in Arabidopsis. Science 302: 1751–1754 doi:10.1126/science.1091109
45. SimpsonGG, PPD, QuesadaV, HendersonI, DeanC (2003) FY Is an RNA 3′ End-Processing Factor that Interacts with FCA to Control the Arabidopsis Floral Transition. Cell 113: 777–787.
46. HornyikC, TerziLC, SimpsonGG (2010) The Spen Family Protein FPA Controls Alternative Cleavage and Polyadenylation of RNA. DEVCEL 18: 203–213 doi:10.1016/j.devcel.2009.12.009
47. LeeI, MichaeliSD, MassherdtAS, AmazinoRM (1994) The late-flowering phenotype of FRIGIDA and mutations in LUMINIDEPENDENS is suppressed in the Ladsberg erecta strain of Arabidopsis. The Plant Journal 6: 903–909.
48. KuaiL, FangF, ButlerJS, ShermanF (2004) Polyadenylation of rRNA in Saccharomyces cerevisiae. PNAS 101: 8581–8586.
49. VasiljevaL, BuratowskiS (2006) Nrd1 Interacts with the Nuclear Exosome for 3′ Processing of RNA Polymerase II Transcripts. Molecular Cell 21: 239–248 doi:10.1016/j.molcel.2005.11.028
50. CastelnuovoM, RahmanS, GuffantiE, InfantinoV, StutzF, et al. (2013) Bimodal expression of PHO84 is modulated by early termination of antisense transcription. Nat Struct Mol Biol 20: 851–858 doi:10.1038/nsmb.2598
51. SheldonCC, ConnAB, ESD, PeacockWJ (2002) Different Regulatory Regions Are Required for the Vernalization-Induced Repression of FLOWERING LOCUS C and for the Epigenetic Maintenance of Repression. THE PLANT CELL ONLINE 14: 2527–2537 doi:10.1105/tpc.004564
52. KannoT, HuettelB, MetteMF, AufsatzW, JaligotE, et al. (2005) Atypical RNA polymerase subunits required for RNA-directed DNA methylation. Nat Genet 37: 761–765 doi:10.1038/ng1580
53. WierzbickiAT, HaagJR, PikaardCS (2008) Noncoding Transcription by RNA Polymerase Pol IVb/Pol V Mediates Transcriptional Silencing of Overlapping and Adjacent Genes. Cell 135: 635–648 doi:10.1016/j.cell.2008.09.035
54. MatzkeM, KannoT, DaxingerL, HuettelB, MatzkeAJ (2009) RNA-mediated chromatin-based silencing in plants. Current Opinion in Cell Biology 21: 367–376 Available: message:%3CA233D938F69F5A49AF9FECB3A02B40AF5DBA82C5@UM-MBX-T01.um.umsystem.edu%3E.
55. HaagJR, PikaardCS (2011) Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nature Publishing Group 12: 483–492 doi:10.1038/nrm3152
56. JohnssonP, AckleyA, VidarsdottirL, LuiW-O, CorcoranM, et al. (2013) A pseudogene long-noncoding-RNA network regulates PTEN transcription and translation in human cells. Nat Struct Mol Biol 20: 440–446 doi:10.1038/nsmb.2516
57. LardenoisA, LiuY, WaltherT, ChalmelF, EvrardB, et al. (2011) Execution of the meiotic noncoding RNA expressionprogram and the onset of gametogenesis in yeastrequire the conserved exosome subunit Rrp6. PNAS 108: 1058–1063 doi:10.1073/pnas.1016459108/-/DCSupplemental/pnas.201016459SI.pdf
58. DerkachevaM, SteinbachY, WildhaberT, aacuteIM, MahrezW, et al. (2013) Arabidopsis MSI1 connects LHP1 to PRC2 complexes. The EMBO Journal 32: 2073–2085 doi:10.1038/emboj.2013.145
59. FrancisNJ (2004) Chromatin Compaction by a Polycomb Group Protein Complex. Science 306: 1574–1577 doi:10.1126/science.1100576
60. YuanW, WuT, FuH, DaiC, WuH, et al. (2012) Dense Chromatin Activates Polycomb Repressive Complex 2 to Regulate H3 Lysine 27 Methylation. Science 337: 971–975 doi:10.1126/science.1225237
61. AllmangC, EP, PodtelejnikovA, MannM, TollerveyD, et al. (1999) The yeast exosome and human PM–Scl are related complexes of 3′→5′ exonucleases. Genes & Development 13: 2148–2158.
62. SugiyamaT, Sugioka-SugiyamaR (2011) Red1 promotes the elimination of meiosis-specific mRNAs in vegetatively growing fission yeast. The EMBO Journal 30: 1027–1039 doi:10.1038/emboj.2011.32
63. GrzechnikP, KufelJ (2008) Polyadenylation Linked to Transcription Termination Directs the Processingof snoRNA Precursors in Yeast. Molecular Cell 32: 247–258 doi:10.1016/j.molcel.2008.10.003
64. SchmidM, JensenTH (2008) The exosome: a multipurpose RNA-decay machine. Trends in Biochemical Sciences 33: 501–510 doi:10.1016/j.tibs.2008.07.003
65. PienS, FleuryD, MylneJS, CrevillenP, InzeD, et al. (2008) ARABIDOPSIS TRITHORAX1 Dynamically Regulates FLOWERING LOCUS C Activation via Histone 3 Lysine 4 Trimethylation. The Plant Cell 20: 580–588 doi:10.1105/tpc.108.058172
66. DavidovichC, ZhengL, GoodrichKJ, CechTR (2013) Promiscuous RNA binding by Polycomb repressive complex 2. Nat Struct Mol Biol 20: 1250–1257 doi:10.1038/nsmb.2679
67. KanekoS, SonJ, ShenSS, ReinbergD, BonasioR (2013) PRC2 binds active promoters and contacts nascent RNAs in embryonic stem cells. Nat Struct Mol Biol 20: 1258–1264 doi:10.1038/nsmb.2700
68. SteinmetzEJ, ConradNK, BrowDA, CordenJL (2001) RNA-binding protein Nrd1 directs poly(A)-independent 3′-end formation of RNA polymerase II transcripts. Nature 413: 327–331 doi:10.1038/35095090
69. CiaudoC, BourdetA, Cohen-TannoudjiM, DietzHC, RougeulleC, et al. (2006) Nuclear mRNA Degradation Pathway(s) Are Implicated in Xist Regulation and X Chromosome Inactivation. PLoS Genet 2: e94 doi:10.1371/journal.pgen.0020094.sg001
70. HaimovichG, MedinaDA, CausseSZ, GarberM, Millán-ZambranoG, et al. (2013) Gene Expression Is Circular: Factors for mRNA Degradation Also Foster mRNA Synthesis. Cell 153: 1000–1011 doi:10.1016/j.cell.2013.05.012
71. NagarajanVK, JonesCI, NewburySF, GreenPJ (2013) XRN 5′→3′ exoribonucleases: Structure, mechanisms and functions. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms 1829: 590–603 doi:10.1016/j.bbagrm.2013.03.005
72. van DijkEL, ChenCL, d'Aubenton-CarafaY, GourvennecS, KwapiszM, et al. (2011) XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature 475: 114–117 doi:10.1038/nature10118
73. BastowR, MylneJS, ListerC, LippmanZ, MartienssenRA, et al. (2004) Vernalization requires epigeneticsilencing of FLC by histonemethylation. Nature 427: 164–167.
74. HerrAJ, JensenMB, DalmayT, BaulcombeDC (2005) RNA Polymerase IV Directs Silencing of Endogenous DNA. Science 308: 118–120 doi:10.1126/science.1106910
75. 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 & Development 19: 2030–2040 doi:10.1101/gad.348405
76. KoornneefM, HanhartCJ, van der VeenJH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229: 57–66.
77. MorohashiK, XieZ, GrotewoldE (2009) Gene-specific and genome-wide ChIP approaches to study plant transcriptional networks. Methods Mol Biol 553: 3–12 doi:_10.1007/978-1-60327-563-7_1
78. ZhuY, RowleyMJ, BöhmdorferG, WierzbickiAT (2013) A SWI/SNF Chromatin-Remodeling Complex Actsin Noncoding RNA-Mediated Transcriptional Silencing. Molecular Cell 49: 298–309 doi:10.1016/j.molcel.2012.11.011
79. TerziLC, SimpsonGG (2009) Arabidopsis RNA immunoprecipitation. The Plant Journal 59: 163–168 doi:10.1111/j.1365-313X.2009.03859.x
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2014 Číslo 9
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Admixture in Latin America: Geographic Structure, Phenotypic Diversity and Self-Perception of Ancestry Based on 7,342 Individuals
- Nipbl and Mediator Cooperatively Regulate Gene Expression to Control Limb Development
- Genome Wide Association Studies Using a New Nonparametric Model Reveal the Genetic Architecture of 17 Agronomic Traits in an Enlarged Maize Association Panel
- Histone Methyltransferase MMSET/NSD2 Alters EZH2 Binding and Reprograms the Myeloma Epigenome through Global and Focal Changes in H3K36 and H3K27 Methylation