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Parental Genome Dosage Imbalance Deregulates Imprinting in


In mammals and in plants, parental genome dosage imbalance deregulates embryo growth and might be involved in reproductive isolation between emerging new species. Increased dosage of maternal genomes represses growth while an increased dosage of paternal genomes has the opposite effect. These observations led to the discovery of imprinted genes, which are expressed by a single parental allele. It was further proposed in the frame of the parental conflict theory that parental genome imbalances are directly mirrored by antagonistic regulations of imprinted genes encoding maternal growth inhibitors and paternal growth enhancers. However these hypotheses were never tested directly. Here, we investigated the effect of parental genome imbalance on the expression of Arabidopsis imprinted genes FERTILIZATION INDEPENDENT SEED2 (FIS2) and FLOWERING WAGENINGEN (FWA) controlled by DNA methylation, and MEDEA (MEA) and PHERES1 (PHE1) controlled by histone methylation. Genome dosage imbalance deregulated the expression of FIS2 and PHE1 in an antagonistic manner. In addition increased dosage of inactive alleles caused a loss of imprinting of FIS2 and MEA. Although FIS2 controls histone methylation, which represses MEA and PHE1 expression, the changes of PHE1 and MEA expression could not be fully accounted for by the corresponding fluctuations of FIS2 expression. Our results show that parental genome dosage imbalance deregulates imprinting using mechanisms, which are independent from known regulators of imprinting. The complexity of the network of regulations between expressed and silenced alleles of imprinted genes activated in response to parental dosage imbalance does not support simple models derived from the parental conflict hypothesis.


Vyšlo v časopise: Parental Genome Dosage Imbalance Deregulates Imprinting in. PLoS Genet 6(3): e32767. doi:10.1371/journal.pgen.1000885
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000885

Souhrn

In mammals and in plants, parental genome dosage imbalance deregulates embryo growth and might be involved in reproductive isolation between emerging new species. Increased dosage of maternal genomes represses growth while an increased dosage of paternal genomes has the opposite effect. These observations led to the discovery of imprinted genes, which are expressed by a single parental allele. It was further proposed in the frame of the parental conflict theory that parental genome imbalances are directly mirrored by antagonistic regulations of imprinted genes encoding maternal growth inhibitors and paternal growth enhancers. However these hypotheses were never tested directly. Here, we investigated the effect of parental genome imbalance on the expression of Arabidopsis imprinted genes FERTILIZATION INDEPENDENT SEED2 (FIS2) and FLOWERING WAGENINGEN (FWA) controlled by DNA methylation, and MEDEA (MEA) and PHERES1 (PHE1) controlled by histone methylation. Genome dosage imbalance deregulated the expression of FIS2 and PHE1 in an antagonistic manner. In addition increased dosage of inactive alleles caused a loss of imprinting of FIS2 and MEA. Although FIS2 controls histone methylation, which represses MEA and PHE1 expression, the changes of PHE1 and MEA expression could not be fully accounted for by the corresponding fluctuations of FIS2 expression. Our results show that parental genome dosage imbalance deregulates imprinting using mechanisms, which are independent from known regulators of imprinting. The complexity of the network of regulations between expressed and silenced alleles of imprinted genes activated in response to parental dosage imbalance does not support simple models derived from the parental conflict hypothesis.


Zdroje

1. FeilR

BergerF

2007 Convergent evolution of genomic imprinting in plants and mammals. Trends Genet 23 192 199

2. HaigD

2004 Genomic imprinting and kinship: how good is the evidence? Annu Rev Genet 38 553 585

3. WilkinsJF

HaigD

2003 What good is genomic imprinting: the function of parent-specific gene expression. Nat Rev Genet 4 359 368

4. LinB-Y

1984 Ploidy barrier to endosperm development in maize. Genetics 107 103 115

5. ScottRJ

SpielmanM

BaileyJ

DickinsonHG

1998 Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125 3329 3341

6. SuraniMA

BartonSC

NorrisML

1984 Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis. Nature 308 548 550

7. McGrathJ

SolterD

1984 Completion of mouse embryogenesis requires both the maternal and paternal genomes. Cell 37 179 183

8. LeblancO

PointeC

HernandezM

2002 Cell cycle progression during endosperm development in Zea mays depends on parental dosage effects. Plant J 32 1057 1066

9. ScottRJ

SpielmanM

2004 Epigenetics: imprinting in plants and mammals, the same but different? Curr Biol 14 R201 203

10. BergerF

ChaudhuryA

2009 Parental memories shape seeds. Trends Plant Sci 14 550 556

11. SpielmanM

VinkenoogR

DickinsonHG

ScottRJ

2001 The epigenetic basis of gender in flowering plants and mammals. Trends Genet 17 705 711

12. de JongTJ

ScottRJ

2007 Parental conflict does not necessarily lead to the evolution of imprinting. Trends Plant Sci 12 439 443

13. GehringM

ChoiY

FischerRL

2004 Imprinting and seed development. Plant Cell16Suppl S203 213

14. DilkesBP

ComaiL

2004 A differential dosage hypothesis for parental effects in seed development. Plant Cell 16 3174 3180

15. KinoshitaT

IkedaY

IshikawaR

2008 Genomic imprinting: a balance between antagonistic roles of parental chromosomes. Semin Cell Dev Biol 19 574 579

16. ReikW

WalterJ

2001 Genomic imprinting: parental influence on the genome. Nature Reviews 2 21 32

17. KawabeA

FujimotoR

CharlesworthD

2007 High diversity due to balancing selection in the promoter region of the Medea gene in Arabidopsis lyrata. Curr Biol 17 1885 1889

18. MiyakeT

TakebayashiN

WolfDE

2009 Possible diversifying selection in the imprinted gene, MEDEA, in Arabidopsis. Mol Biol Evol

19. SpillaneC

SchmidKJ

Laoueille-DupratS

PienS

Escobar-RestrepoJM

2007 Positive darwinian selection at the imprinted MEDEA locus in plants. Nature 448 349 352

20. JosefssonC

DilkesB

ComaiL

2006 Parent-dependent loss of gene silencing during interspecies hybridization. Curr Biol 16 1322 1328

21. WaliaH

JosefssonC

DilkesB

KirkbrideR

HaradaJ

2009 Dosage-dependent deregulation of an AGAMOUS-LIKE gene cluster contributes to interspecific incompatibility. Curr Biol 19 1128 1132

22. ErilovaA

BrownfieldL

ExnerV

RosaM

TwellD

2009 Imprinting of the polycomb group gene MEDEA serves as a ploidy sensor in Arabidopsis. PLoS Genet 5 e1000663 doi:10.1371/journal.pgen.1000663

23. KinoshitaT

YadegariR

HaradaJJ

GoldbergRB

FischerRL

1999 Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell 11 1945 1952

24. TiwariS

SchulzR

IkedaY

DythamL

BravoJ

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

25. JullienPE

KinoshitaT

OhadN

BergerF

2006 Maintenance of DNA Methylation during the Arabidopsis Life Cycle Is Essential for Parental Imprinting. Plant Cell 18 1360 1372

26. KinoshitaT

MiuraA

ChoiY

KinoshitaY

CaoX

2004 One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303 521 523

27. Fitz GeraldJN

HuiPS

BergerF

2009 Polycomb group-dependent imprinting of the actin regulator AtFH5 regulates morphogenesis in Arabidopsis thaliana. Development 136 3399 3404

28. IngouffM

HaseloffJ

BergerF

2005 Polycomb group genes control developmental timing of endosperm. Plant J 42 663 674

29. KiyosueT

OhadN

YadegariR

HannonM

DinnenyJ

1999 Control of fertilization-independent endosperm development by the MEDEA polycomb gene in Arabidopsis. Proc Natl Acad Sci USA 96 4186 4191

30. KohlerC

HennigL

SpillaneC

PienS

GruissemW

2003 The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes and development 17 1540 1553

31. MakarevichG

VillarCB

ErilovaA

KohlerC

2008 Mechanism of PHERES1 imprinting in Arabidopsis. J Cell Sci 121 906 912

32. GehringM

BubbKL

HenikoffS

2009 Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324 1447 1451

33. BergerF

HamamuraY

IngouffM

HigashiyamaT

2008 Double fertilization - caught in the act. Trends Plant Sci 13 437 443

34. 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

35. GehringM

HuhJH

HsiehTF

PentermanJ

ChoiY

2006 DEMETER DNA Glycosylase Establishes MEDEA Polycomb Gene Self-Imprinting by Allele-Specific Demethylation. Cell 124 495 506

36. JullienPE

KatzA

OlivaM

OhadN

BergerF

2006 Polycomb Group Complexes Self-Regulate Imprinting of the Polycomb Group Gene MEDEA in Arabidopsis. Curr Biol 16 486 492

37. LuoM

DennisES

BergerF

PeacockWJ

ChaudhuryA

2005 MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. Proc Natl Acad Sci U S A 102 17531 17536

38. ChoiY

GehringM

JohnsonL

HannonM

HaradaJJ

2002 DEMETER, a DNA Glycosylase Domain Protein, Is Required for Endosperm Gene Imprinting and Seed Viability in Arabidopsis. Cell 110 33 42

39. FinneganEJ

PeacockWJ

DennisES

1996 Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc Natl Acad Sci U S A 93 8449 8454

40. 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

41. ChanSW

ZhangX

BernatavichuteYV

JacobsenSE

2006 Two-step recruitment of RNA-directed DNA methylation to tandem repeats. PLoS Biol 4 e363 doi:10.1371/journal.pbio.0040363

42. ChandlerVL

2007 Paramutation: from maize to mice. Cell 128 641 645

43. ComaiL

2005 The advantages and disadvantages of being polyploid. Nat Rev Genet 6 836 846

44. Mittelsten ScheidO

AfsarK

PaszkowskiJ

2003 Formation of stable epialleles and their paramutation-like interaction in tetraploid Arabidopsis thaliana. Nat Genet 34 450 454

45. AllemanM

SidorenkoL

McGinnisK

SeshadriV

DorweilerJE

2006 An RNA-dependent RNA polymerase is required for paramutation in maize. Nature 442 295 298

46. MakarevichG

LeroyO

AkinciU

SchubertD

ClarenzO

2006 Different Polycomb group complexes regulate common target genes in Arabidopsis. EMBO Rep 7 947 952

47. LuoM

BilodeauP

KoltunowA

DennisES

PeacockWJ

1999 Genes controlling fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci U S A 96 296 301

48. WangD

TysonMD

JacksonSS

YadegariR

2006 Partially redundant functions of two SET-domain polycomb-group proteins in controlling initiation of seed development in Arabidopsis. Proc Natl Acad Sci U S A 103 13244 13249

49. AllenND

BartonSC

HiltonK

NorrisML

SuraniMA

1994 A functional analysis of imprinting in parthenogenetic embryonic stem cells. Development 120 1473 1482

50. SasakiH

Ferguson-SmithAC

ShumAS

BartonSC

SuraniMA

1995 Temporal and spatial regulation of H19 imprinting in normal and uniparental mouse embryos. Development 121 4195 4202

51. SotomaruY

KatsuzawaY

HatadaI

ObataY

SasakiH

2002 Unregulated expression of the imprinted genes H19 and Igf2r in mouse uniparental fetuses. J Biol Chem 277 12474 12478

52. SotomaruY

KawaseY

UedaT

ObataY

SuzukiH

2001 Disruption of imprinted expression of U2afbp-rs/U2af1-rs1 gene in mouse parthenogenetic fetuses. J Biol Chem 276 26694 26698

53. HenryIM

DilkesBP

YoungK

WatsonB

WuH

2005 Aneuploidy and genetic variation in the Arabidopsis thaliana triploid response. Genetics 170 1979 1988

54. ChanSW

HendersonIR

JacobsenSE

2005 Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6 351 360

55. MosherRA

MelnykCW

KellyKA

DunnRM

StudholmeDJ

2009 Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 460 283 286

56. SlotkinRK

VaughnM

BorgesF

TanurdzicM

BeckerJD

2009 Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136 461 472

57. DittRF

KerrKF

de FigueiredoP

DelrowJ

ComaiL

2006 The Arabidopsis thaliana transcriptome in response to Agrobacterium tumefaciens. Mol Plant Microbe Interact 19 665 681

58. MadlungA

TyagiAP

WatsonB

JiangH

KagochiT

2005 Genomic changes in synthetic Arabidopsis polyploids. Plant J 41 221 230

59. GuittonAE

PageDR

ChambrierP

LionnetC

FaureJE

2004 Identification of new members of Fertilisation Independent Seed Polycomb Group pathway involved in the control of seed development in Arabidopsis thaliana. Development 131 2971 2981

60. KohlerC

PageDR

GagliardiniV

GrossniklausU

2005 The Arabidopsis thaliana MEDEA Polycomb group protein controls expression of PHERES1 by parental imprinting. Nat Genet 37 28 30

61. RuijterJM

RamakersC

HoogaarsWM

KarlenY

BakkerO

2009 Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37 e45

62. LivakKJ

SchmittgenTD

2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 402 408

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