Genomic Imprinting in the Embryo Is Partly Regulated by PRC2
Genomic imprinting results in monoallelic gene expression in a parent-of-origin-dependent manner and is regulated by the differential epigenetic marking of the parental alleles. In plants, genomic imprinting has been primarily described for genes expressed in the endosperm, a tissue nourishing the developing embryo that does not contribute to the next generation. In Arabidopsis, the genes MEDEA (MEA) and PHERES1 (PHE1), which are imprinted in the endosperm, are also expressed in the embryo; whether their embryonic expression is regulated by imprinting or not, however, remains controversial. In contrast, the maternally expressed in embryo 1 (mee1) gene of maize is clearly imprinted in the embryo. We identified several imprinted candidate genes in an allele-specific transcriptome of hybrid Arabidopsis embryos and confirmed parent-of-origin-dependent, monoallelic expression for eleven maternally expressed genes (MEGs) and one paternally expressed gene (PEG) in the embryo, using allele-specific expression analyses and reporter gene assays. Genetic studies indicate that the Polycomb Repressive Complex 2 (PRC2) but not the DNA METHYLTRANSFERASE1 (MET1) is involved in regulating imprinted expression in the embryo. In the seedling, all embryonic MEGs and the PEG are expressed from both parents, suggesting that the imprint is erased during late embryogenesis or early vegetative development. Our finding that several genes are regulated by genomic imprinting in the Arabidopsis embryo clearly demonstrates that this epigenetic phenomenon is not a unique feature of the endosperm in both monocots and dicots.
Vyšlo v časopise:
Genomic Imprinting in the Embryo Is Partly Regulated by PRC2. PLoS Genet 9(12): e32767. doi:10.1371/journal.pgen.1003862
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003862
Souhrn
Genomic imprinting results in monoallelic gene expression in a parent-of-origin-dependent manner and is regulated by the differential epigenetic marking of the parental alleles. In plants, genomic imprinting has been primarily described for genes expressed in the endosperm, a tissue nourishing the developing embryo that does not contribute to the next generation. In Arabidopsis, the genes MEDEA (MEA) and PHERES1 (PHE1), which are imprinted in the endosperm, are also expressed in the embryo; whether their embryonic expression is regulated by imprinting or not, however, remains controversial. In contrast, the maternally expressed in embryo 1 (mee1) gene of maize is clearly imprinted in the embryo. We identified several imprinted candidate genes in an allele-specific transcriptome of hybrid Arabidopsis embryos and confirmed parent-of-origin-dependent, monoallelic expression for eleven maternally expressed genes (MEGs) and one paternally expressed gene (PEG) in the embryo, using allele-specific expression analyses and reporter gene assays. Genetic studies indicate that the Polycomb Repressive Complex 2 (PRC2) but not the DNA METHYLTRANSFERASE1 (MET1) is involved in regulating imprinted expression in the embryo. In the seedling, all embryonic MEGs and the PEG are expressed from both parents, suggesting that the imprint is erased during late embryogenesis or early vegetative development. Our finding that several genes are regulated by genomic imprinting in the Arabidopsis embryo clearly demonstrates that this epigenetic phenomenon is not a unique feature of the endosperm in both monocots and dicots.
Zdroje
1. ReikW, WalterJ (2001) Genomic imprinting: parental influence on the genome. Nat Rev Genet 2: 21–32.
2. BarlowDP (2011) Genomic imprinting: a mammalian epigenetic discovery model. Annu Rev Genet 45: 379–403.
3. FengS, JacobsenSE, ReikW (2010) Epigenetic reprogramming in plant and animal development. Science 330: 622–627.
4. FrostJM, MooreGE (2010) The importance of imprinting in the human placenta. PLoS Genet 6: e1001015.
5. FeilR, BergerF (2007) Convergent evolution of genomic imprinting in plants and mammals. Trends Genet 23: 192–199.
6. JullienPE, BergerF (2009) Gamete-specific epigenetic mechanisms shape genomic imprinting. Curr Opin Plant Biol 12: 637–642.
7. JahnkeS, ScholtenS (2009) Epigenetic resetting of a gene imprinted in plant embryos. Curr Biol 19: 1677–1681.
8. LuoM, TaylorJ, SpriggsA, ZhangH, WuX, et al. (2011) A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm. PLoS Genet 7: e1002125.
9. KöhlerC, PageDR, GagliardiniV, GrossniklausU (2005) The Arabidopsis thaliana MEDEA Polycomb group protein controls expression of PHERES1 by parental imprinting. Nat Genet 37: 28–30.
10. RaissigMT, BarouxC, GrossniklausU (2011) Regulation and flexibility of genomic imprinting during seed development. Plant Cell 23: 16–26.
11. SpillaneC, SchmidKJ, Laoueillé-DupratS, PienS, Escobar-RestrepoJM, et al. (2007) Positive darwinian selection at the imprinted MEDEA locus in plants. Nature 448: 349–352.
12. BartolomeiMS, Ferguson-SmithAC (2011) Mammalian genomic imprinting. Cold Spring Harb Perspect Biol 3: pii: a002592.
13. Ferguson-SmithAC (2011) Genomic imprinting: the emergence of an epigenetic paradigm. Nat Rev Genet 12: 565–575.
14. ChoiY, GehringM, JohnsonL, HannonM, HaradaJJ, et al. (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110: 33–42.
15. XiaoW, GehringM, ChoiY, MargossianL, PuH, et al. (2003) Imprinting of the MEA Polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase. Dev Cell 5: 891–901.
16. KinoshitaT, MiuraA, ChoiY, KinoshitaY, CaoX, et al. (2004) One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303: 521–523.
17. GehringM, HuhJH, HsiehTF, PentermanJ, ChoiY, et al. (2006) DEMETER DNA glycosylase establishes MEDEA Polycomb gene self-imprinting by allele-specific demethylation. Cell 124: 495–506.
18. JullienP, KinoshitaT, OhadN, BergerF (2006) Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. Plant Cell 18: 1360–1372.
19. TiwariS, SchulzR, IkedaY, DythamL, BravoJ, et al. (2008) MATERNALLY EXPRESSED PAB C-TERMINAL, a novel imprinted gene in Arabidopsis, encodes the conserved C-terminal domain of polyadenylate binding proteins. Plant Cell 20: 2387–2398.
20. WöhrmannHJ, GagliardiniV, RaissigMT, WehrleW, ArandJ, et al. (2012) Identification of a DNA methylation-independent imprinting control region at the Arabidopsis MEDEA locus. Genes Dev 26: 1837–1850.
21. Gutiérrez-MarcosJF, CostaLM, Dal PràM, ScholtenS, KranzE, et al. (2006) Epigenetic asymmetry of imprinted genes in plant gametes. Nat Genet 38: 876–878.
22. HaunWJ, Laoueillé-DupratS, O'connellMJ, SpillaneC, GrossniklausU, et al. (2007) Genomic imprinting, methylation and molecular evolution of maize Enhancer of zeste (Mez) homologs. Plant J 49: 325–337.
23. HermonP, SrilunchangKO, ZouJ, DresselhausT, DanilevskayaON (2007) Activation of the imprinted Polycomb group Fie1 gene in maize endosperm requires demethylation of the maternal allele. Plant Mol Biol 64: 387–395.
24. BarouxC, GagliardiniV, PageDR, GrossniklausU (2006) Dynamic regulatory interactions of Polycomb group genes: MEDEA autoregulation is required for imprinted gene expression in Arabidopsis. Genes Dev 20: 1081–1086.
25. Fitz GeraldJN, HuiPS, BergerF, GeraldJNF, HuiPS, et al. (2009) Polycomb group-dependent imprinting of the actin regulator AtFH5 regulates morphogenesis in Arabidopsis thaliana. Development 136: 3399–3404.
26. JullienP, KatzA, OlivaM, OhadN, BergerF (2006) Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA in Arabidopsis. Curr Biol 16: 486–492.
27. HsiehTF, ShinJ, UzawaR, SilvaP, CohenS, et al. (2011) Regulation of imprinted gene expression in Arabidopsis endosperm. Proc Natl Acad Sci USA 108: 1755–1762.
28. GehringM, MissirianV, HenikoffS (2011) Genomic analysis of parent-of-origin allelic expression in Arabidopsis thaliana seeds. PLoS ONE 6: e23687.
29. WolffP, WeinhoferI, SeguinJ, RoszakP, BeiselC, et al. (2011) High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis endosperm. PLoS Genet 7: e1002126.
30. McKeownPC, Laouielle-DupratS, PrinsP, WolffP, SchmidMW, et al. (2011) Identification of imprinted genes subject to parent-of-origin specific expression in Arabidopsis thaliana seeds. BMC Plant Biol 11: 113.
31. WatersAJ, MakarevitchI, EichtenSR, Swanson-WagnerRA, YehCT, et al. (2011) Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm. Plant Cell 23: 4221–4233.
32. ZhangM, ZhaoH, XieS, ChenJ, XuY, et al. (2011) Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm. Proc Natl Acad Sci USA 108: 20042–20047.
33. AutranD, BarouxC, RaissigMT, LenormandT, WittigM, et al. (2011) Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Cell 145: 707–719.
34. NodineMD, BartelDP (2012) Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature 482: 94–97.
35. WuestSE, VijverbergK, SchmidtA, WeissM, GheyselinckJ, et al. (2010) Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr Biol 20: 506–512.
36. BorgesF, GomesG, GardnerR, MorenoN, McCormickS, et al. (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Phys 148: 1168–1181.
37. PourcelL, RoutaboulJ-M, KerhoasL, CabocheM, LepiniecL, et al. (2005) TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell 17: 2966–2980.
38. BemerM, HeijmansK, AiroldiC, DaviesB, AngenentGC (2010) An atlas of type I MADS box gene expression during female gametophyte and seed development in Arabidopsis. Plant Phys 154: 287–300.
39. KangI-H, SteffenJG, PortereikoMF, LloydA, DrewsGN (2008) The AGL62 MADS domain protein regulates cellularization during endosperm development in Arabidopsis. Plant Cell 20: 635–647.
40. JeffersonRA, KavanaghTA, BevanMW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907.
41. ReidtW, WohlfarthT, EllerströmM, CzihalA, TewesA, et al. (2000) Gene regulation during late embryogenesis: the RY motif of maturation-specific gene promoters is a direct target of the FUS3 gene product. Plant J 21: 401–408.
42. ChaudhuryAM, MingL, MillerC, CraigS, DennisES, et al. (1997) Fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci USA 94: 4223–4228.
43. GrossniklausU, Vielle-CalzadaJP, HoeppnerMA, GaglianoWB (1998) Maternal control of embryogenesis by MEDEA, a Polycomb group gene in Arabidopsis. Science 280: 446–450.
44. RazV, BergervoetJH, KoornneefM (2001) Sequential steps for developmental arrest in Arabidopsis seeds. Development 128: 243–252.
45. XiangD, VenglatP, TibicheC, YangH, RisseeuwE, et al. (2011) Genome-wide analysis reveals gene expression and metabolic network dynamics during embryo development in Arabidopsis. Plant Phys 156: 346–356.
46. SchmidMW, SchmidtA, KlostermeierUC, BarannM, RosenstielP, et al. (2012) A powerful method for transcriptional profiling of specific cell types in eukaryotes: laser-assisted microdissection and RNA sequencing. PLoS ONE 7: e29685.
47. KraglerF (2013) Plasmodesmata: intercellular tunnels facilitating transport of macromolecules in plants. Cell Tiss Res 352: 49–58.
48. Kozieradzka-KiszkurnoM, PłachnoBJ (2012) Are there symplastic connections between the endosperm and embryo in some angiosperms?–a lesson from the Crassulaceae family. Protoplasma 249: 1081–1089.
49. PignattaD, GehringM (2012) Imprinting meets genomics: new insights and new challenges. Curr Opin Plant Biol 15: 530–535.
50. DevealeB, Van Der KooyD, BabakT (2012) Critical evaluation of imprinted gene expression by RNA–Seq: a new perspective. PLoS Genet 8: e1002600.
51. BarouxC, AutranD, RaissigMT, GrimanelliD, GrossniklausU (2013) Parental contributions to the transcriptome of early plant embryos. Curr Opin Genet Dev 23: 72–74.
52. Vielle-CalzadaJP, BaskarR, GrossniklausU (2000) Delayed activation of the paternal genome during seed development. Nature 404: 91–94.
53. MakarevichG, VillarCB, ErilovaA, KohlerC (2008) Mechanism of PHERES1 imprinting in Arabidopsis. J Cell Sci 121: 906–912.
54. JacksonJP, LindrothAM, CaoX, JacobsenSE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556–560.
55. CedarH, BergmanY (2009) Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 10: 295–304.
56. HaunWJ, SpringerNM (2008) Maternal and paternal alleles exhibit differential histone methylation and acetylation at maize imprinted genes. Plant J 56: 903–912.
57. BemerM, GrossniklausU (2012) Dynamic regulation of Polycomb group activity during plant development. Curr Opin Plant Biol 15: 523–529.
58. LudwigT, EggenschwilerJ, FisherP, D'ErcoleAJ, DavenportML, et al. (1996) Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Dev Biol 177: 517–535.
59. LauMM, StewartCE, LiuZ, BhattH, RotweinP, et al. (1994) Loss of the imprinted IGF2/cation-independent mannose 6-phosphate receptor results in fetal overgrowth and perinatal lethality. Genes Dev 8: 2953–2963.
60. IngouffM, HaseloffJ, BergerF (2005) Polycomb group genes control developmental timing of endosperm. Plant J 42: 663–674.
61. KinoshitaT, YadegariR, HaradaJJ, GoldbergRB, FischerRL (1999) Imprinting of the MEDEA Polycomb gene in the Arabidopsis endosperm. Plant Cell 11: 1945–1952.
62. KiyosueT, OhadN, YadegariR, HannonM, DinnenyJ, et al. (1999) Control of fertilization-independent endosperm development by the MEDEA Polycomb gene in Arabidopsis. Proc Natl Acad Sci USA 96: 4186–4191.
63. LuoM, BilodeauP, DennisES, PeacockWJ, ChaudhuryA (2000) Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. Proc Natl Acad Sci USA 97: 10637–10642.
64. TyckoB, MorisonIM (2002) Physiological functions of imprinted genes. J Cell Physiol 192: 245–258.
65. HaigD, WestobyM (1989) Parent-specific gene expression and the triploid endosperm. Am Nat 134: 147–155.
66. BatesonP (1994) The dynamics of parent-offspring relationships in mammals. Trends Ecol Evol 9: 399–403.
67. WolfJB, HagerR (2006) A maternal-offspring coadaptation theory for the evolution of genomic imprinting. PLoS Biol 4: e380.
68. BouyerD, RoudierF, HeeseM, AndersenED, GeyD, et al. (2011) Polycomb Repressive Complex 2 controls the embryo-to-seedling phase transition. PLoS Genet 7: e1002014.
69. SazeH, Mittelsten ScheidO, PaszkowskiJ (2003) Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet 34: 65–69.
70. WuX, ChoryJ, WeigelD (2007) Combinations of WOX activities regulate tissue proliferation during Arabidopsis embryonic development. Dev Biol 309: 306–316.
71. CloughSJ, BentAF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735–743.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2013 Číslo 12
- 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
- The NuRD Chromatin-Remodeling Enzyme CHD4 Promotes Embryonic Vascular Integrity by Transcriptionally Regulating Extracellular Matrix Proteolysis
- Comprehensive Analysis of Transcriptome Variation Uncovers Known and Novel Driver Events in T-Cell Acute Lymphoblastic Leukemia
- Quantifying Missing Heritability at Known GWAS Loci
- Smc5/6-Mms21 Prevents and Eliminates Inappropriate Recombination Intermediates in Meiosis