The SET-Domain Protein SUVR5 Mediates H3K9me2 Deposition and Silencing at Stimulus Response Genes in a DNA Methylation–Independent Manner
In eukaryotic cells, environmental and developmental signals alter chromatin structure and modulate gene expression. Heterochromatin constitutes the transcriptionally inactive state of the genome and in plants and mammals is generally characterized by DNA methylation and histone modifications such as histone H3 lysine 9 (H3K9) methylation. In Arabidopsis thaliana, DNA methylation and H3K9 methylation are usually colocated and set up a mutually self-reinforcing and stable state. Here, in contrast, we found that SUVR5, a plant Su(var)3–9 homolog with a SET histone methyltransferase domain, mediates H3K9me2 deposition and regulates gene expression in a DNA methylation–independent manner. SUVR5 binds DNA through its zinc fingers and represses the expression of a subset of stimulus response genes. This represents a novel mechanism for plants to regulate their chromatin and transcriptional state, which may allow for the adaptability and modulation necessary to rapidly respond to extracellular cues.
Vyšlo v časopise:
The SET-Domain Protein SUVR5 Mediates H3K9me2 Deposition and Silencing at Stimulus Response Genes in a DNA Methylation–Independent Manner. PLoS Genet 8(10): e32767. doi:10.1371/journal.pgen.1002995
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002995
Souhrn
In eukaryotic cells, environmental and developmental signals alter chromatin structure and modulate gene expression. Heterochromatin constitutes the transcriptionally inactive state of the genome and in plants and mammals is generally characterized by DNA methylation and histone modifications such as histone H3 lysine 9 (H3K9) methylation. In Arabidopsis thaliana, DNA methylation and H3K9 methylation are usually colocated and set up a mutually self-reinforcing and stable state. Here, in contrast, we found that SUVR5, a plant Su(var)3–9 homolog with a SET histone methyltransferase domain, mediates H3K9me2 deposition and regulates gene expression in a DNA methylation–independent manner. SUVR5 binds DNA through its zinc fingers and represses the expression of a subset of stimulus response genes. This represents a novel mechanism for plants to regulate their chromatin and transcriptional state, which may allow for the adaptability and modulation necessary to rapidly respond to extracellular cues.
Zdroje
1. JenuweinT, AllisCD (2001) Translating the histone code. Science 293: 1074–1080.
2. JenuweinT, LaibleG, DornR, ReuterG (1998) SET domain proteins modulate chromatin domains in eu- and heterochromatin. Cell Mol Life Sci 54: 80–93.
3. ReaS, EisenhaberF, O'CarrollD, StrahlBD, SunZW, et al. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature 406: 593–599.
4. BaumbuschLO, ThorstensenT, KraussV, FischerA, NaumannK, et al. (2001) The Arabidopsis thaliana genome contains at least 29 active genes encoding SET domain proteins that can be assigned to four evolutionarily conserved classes. Nucleic Acids Res 29: 4319–4333.
5. CaoX, JacobsenSE (2002) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Current Biology 12: 1138–1144.
6. LawJA, JacobsenSE Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204–220.
7. HendersonIR, JacobsenSE (2007) Epigenetic inheritance in plants. Nature 447: 418–424.
8. WooHR, PontesO, PikaardCS, RichardsEJ (2007) VIM1, a methylcytosine-binding protein required for centromeric heterochromatinization. Genes Dev 21: 267–277.
9. WooHR, DittmerTA, RichardsEJ (2008) Three SRA-domain methylcytosine-binding proteins cooperate to maintain global CpG methylation and epigenetic silencing in Arabidopsis. PLoS Genet 4: e1000156 doi:10.1371/journal.pgen.1000156.
10. KraftE, BostickM, JacobsenSE, CallisJ (2008) ORTH/VIM proteins that regulate DNA methylation are functional ubiquitin E3 ligases. Plant J 56: 704–715.
11. JohnsonLM, BostickM, ZhangX, KraftE, HendersonI, et al. (2007) The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol 17: 379–384.
12. BostickM, KimJK, EstevePO, ClarkA, PradhanS, et al. (2007) UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317: 1760–1764.
13. SharifJ, MutoM, TakebayashiS, SuetakeI, IwamatsuA, et al. (2007) The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450: 908–912.
14. JacksonJP, LindrothAM, CaoX, JacobsenSE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556–560.
15. MalagnacF, BarteeL, BenderJ (2002) An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. Embo J 21: 6842–6852.
16. EbbsML, BenderJ (2006) Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18: 1166–1176.
17. EbbsML, BarteeL, BenderJ (2005) H3 lysine 9 methylation is maintained on a transcribed inverted repeat by combined action of SUVH6 and SUVH4 methyltransferases. Mol Cell Biol 25: 10507–10515.
18. RajakumaraE, LawJA, SimanshuDK, VoigtP, JohnsonLM, et al. A dual flip-out mechanism for 5mC recognition by the Arabidopsis SUVH5 SRA domain and its impact on DNA methylation and H3K9 dimethylation in vivo. Genes Dev 25: 137–152.
19. LawJA, AusinI, JohnsonLM, VashishtAA, ZhuJK, et al. A protein complex required for polymerase V transcripts and RNA- directed DNA methylation in Arabidopsis. Curr Biol 20: 951–956.
20. BernatavichuteYV, ZhangX, CokusS, PellegriniM, JacobsenSE (2008) Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS ONE 3: e3156 doi:10.1371/journal.pone.0003156.
21. JacksonJP, JohnsonL, JasencakovaZ, ZhangX, PerezBurgosL, et al. (2004) Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112: 308–315.
22. TariqM, SazeH, ProbstAV, LichotaJ, HabuY, et al. (2003) Erasure of CpG methylation in Arabidopsis alters patterns of histone H3 methylation in heterochromatin. Proc Natl Acad Sci U S A 100: 8823–8827.
23. KrichevskyA, GutgartsH, KozlovskySV, TzfiraT, SuttonA, et al. (2007) C2H2 zinc finger-SET histone methyltransferase is a plant-specific chromatin modifier. Dev Biol 303: 259–269.
24. PavletichNP, PaboCO (1993) Crystal structure of a five-finger GLI-DNA complex: new perspectives on zinc fingers. Science 261: 1701–1707.
25. MullerJ, HartCM, FrancisNJ, VargasML, SenguptaA, et al. (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197–208.
26. SchmitgesFW, PrustyAB, FatyM, StutzerA, LingarajuGM, et al. Histone methylation by PRC2 is inhibited by active chromatin marks. Mol Cell 42: 330–341.
27. WoodwardAW, BartelB (2005) Auxin: regulation, action, and interaction. Ann Bot 95: 707–735.
28. VannesteS, FrimlJ (2009) Auxin: a trigger for change in plant development. Cell 136: 1005–1016.
29. OvervoordeP, FukakiH, BeeckmanT Auxin control of root development. Cold Spring Harb Perspect Biol 2: a001537.
30. KrichevskyA, KozlovskySV, GutgartsH, CitovskyV (2007) Arabidopsis co-repressor complexes containing polyamine oxidase-like proteins and plant-specific histone methyltransferases. Plant Signal Behav 2: 174–177.
31. SchoenherrCJ, PaquetteAJ, AndersonDJ (1996) Identification of potential target genes for the neuron-restrictive silencer factor. Proc Natl Acad Sci U S A 93: 9881–9886.
32. GrimesJA, NielsenSJ, BattaglioliE, MiskaEA, SpehJC, et al. (2000) The co-repressor mSin3A is a functional component of the REST-CoREST repressor complex. J Biol Chem 275: 9461–9467.
33. HuangY, MyersSJ, DingledineR (1999) Transcriptional repression by REST: recruitment of Sin3A and histone deacetylase to neuronal genes. Nat Neurosci 2: 867–872.
34. NaruseY, AokiT, KojimaT, MoriN (1999) Neural restrictive silencer factor recruits mSin3 and histone deacetylase complex to repress neuron-specific target genes. Proc Natl Acad Sci U S A 96: 13691–13696.
35. RoopraA, SharlingL, WoodIC, BriggsT, BachfischerU, et al. (2000) Transcriptional repression by neuron-restrictive silencer factor is mediated via the Sin3-histone deacetylase complex. Mol Cell Biol 20: 2147–2157.
36. ShiY, LanF, MatsonC, MulliganP, WhetstineJR, et al. (2004) Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119: 941–953.
37. TachibanaM, SugimotoK, FukushimaT, ShinkaiY (2001) Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3. J Biol Chem 276: 25309–25317.
38. FogCK, GalliGG, LundAH PRDM proteins: Important players in differentiation and disease. Bioessays
39. KimKC, HuangS (2003) Histone methyltransferases in tumor suppression. Cancer Biol Ther 2: 491–499.
40. GrewalSI, MoazedD (2003) Heterochromatin and epigenetic control of gene expression. Science 301: 798–802.
41. JiangD, YangW, HeY, AmasinoRM (2007) Arabidopsis relatives of the human lysine-specific Demethylase1 repress the expression of FWA and FLOWERING LOCUS C and thus promote the floral transition. Plant Cell 19: 2975–2987.
42. SasaiN, NakaoM, DefossezPA Sequence-specific recognition of methylated DNA by human zinc-finger proteins. Nucleic Acids Res 38: 5015–5022.
43. JohnsonL, CaoX, JacobsenS (2002) Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12: 1360–1367.
44. CokusSJ, FengS, ZhangX, ChenZ, MerrimanB, et al. (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452: 215–219.
45. DuZ, ZhouX, LingY, ZhangZ, SuZ agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38: W64–70.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2012 Číslo 10
- 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
- A Mutation in the Gene Causes Alternative Splicing Defects and Deafness in the Bronx Waltzer Mouse
- Classical Genetics Meets Next-Generation Sequencing: Uncovering a Genome-Wide Recombination Map in
- Mutations in (Hhat) Perturb Hedgehog Signaling, Resulting in Severe Acrania-Holoprosencephaly-Agnathia Craniofacial Defects
- Regulation of ATG4B Stability by RNF5 Limits Basal Levels of Autophagy and Influences Susceptibility to Bacterial Infection