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A Genome-Wide Survey of Imprinted Genes in Rice Seeds Reveals Imprinting Primarily Occurs in the Endosperm


Genomic imprinting causes the expression of an allele depending on its parental origin. In plants, most imprinted genes have been identified in Arabidopsis endosperm, a transient structure consumed by the embryo during seed formation. We identified imprinted genes in rice seed where both the endosperm and embryo are present at seed maturity. RNA was extracted from embryos and endosperm of seeds obtained from reciprocal crosses between two subspecies Nipponbare (Japonica rice) and 93-11 (Indica rice). Sequenced reads from cDNA libraries were aligned to their respective parental genomes using single-nucleotide polymorphisms (SNPs). Reads across SNPs enabled derivation of parental expression bias ratios. A continuum of parental expression bias states was observed. Statistical analyses indicated 262 candidate imprinted loci in the endosperm and three in the embryo (168 genic and 97 non-genic). Fifty-six of the 67 loci investigated were confirmed to be imprinted in the seed. Imprinted loci are not clustered in the rice genome as found in mammals. All of these imprinted loci were expressed in the endosperm, and one of these was also imprinted in the embryo, confirming that in both rice and Arabidopsis imprinted expression is primarily confined to the endosperm. Some rice imprinted genes were also expressed in vegetative tissues, indicating that they have additional roles in plant growth. Comparison of candidate imprinted genes found in rice with imprinted candidate loci obtained from genome-wide surveys of imprinted genes in Arabidopsis to date shows a low degree of conservation, suggesting that imprinting has evolved independently in eudicots and monocots.


Vyšlo v časopise: A Genome-Wide Survey of Imprinted Genes in Rice Seeds Reveals Imprinting Primarily Occurs in the Endosperm. PLoS Genet 7(6): e32767. doi:10.1371/journal.pgen.1002125
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002125

Souhrn

Genomic imprinting causes the expression of an allele depending on its parental origin. In plants, most imprinted genes have been identified in Arabidopsis endosperm, a transient structure consumed by the embryo during seed formation. We identified imprinted genes in rice seed where both the endosperm and embryo are present at seed maturity. RNA was extracted from embryos and endosperm of seeds obtained from reciprocal crosses between two subspecies Nipponbare (Japonica rice) and 93-11 (Indica rice). Sequenced reads from cDNA libraries were aligned to their respective parental genomes using single-nucleotide polymorphisms (SNPs). Reads across SNPs enabled derivation of parental expression bias ratios. A continuum of parental expression bias states was observed. Statistical analyses indicated 262 candidate imprinted loci in the endosperm and three in the embryo (168 genic and 97 non-genic). Fifty-six of the 67 loci investigated were confirmed to be imprinted in the seed. Imprinted loci are not clustered in the rice genome as found in mammals. All of these imprinted loci were expressed in the endosperm, and one of these was also imprinted in the embryo, confirming that in both rice and Arabidopsis imprinted expression is primarily confined to the endosperm. Some rice imprinted genes were also expressed in vegetative tissues, indicating that they have additional roles in plant growth. Comparison of candidate imprinted genes found in rice with imprinted candidate loci obtained from genome-wide surveys of imprinted genes in Arabidopsis to date shows a low degree of conservation, suggesting that imprinting has evolved independently in eudicots and monocots.


Zdroje

1. FeilRBergerF 2007 Convergent evolution of genomic imprinting in plants and mammals. Trends Genet 23 192 9

2. RaissigMTBarouxCGrossniklausU 2011 Regulation and Flexibility of Genomic Imprinting during Seed Development. Plant Cell 10.1105/tpc.110.081018. [Epub ahead of print]

3. KöhlerCWeinhofer-MolischI 2010 Mechanisms and evolution of genomic imprinting in plants. Heredity 105 57 63

4. IderaabdullahFYVigneauSBartolomeiMS 2008 Genomic imprinting mechanisms in mammals. Mutat Res 647 77 85

5. ChoiYGehringMJohnsonLHannonMHaradaJJ 2002 DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110 33 42

6. GehringMHuhJHHsiehTFPentermanJChoiY 2006 DEMETER DNA glycosylase establishes MEDEA Polycomb gene self-imprinting by allele-specific demethylation. Cell 124 495 506

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

8. JullienPEKinoshitaTOhadNBergerF 2006 Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. Plant Cell 18 1360 1372

9. JullienPEMosqunaAIngouffMSakataTOhadN 2008 Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biol 6 e194 doi:10.1371/journal.pbio.0060194

10. JullienPEKatzAOlivaMOhadNBergerF 2006 Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA in Arabidopsis. Curr Biol 16 486 492

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

12. BarouxCGagliardiniVPageDRGrossniklausU 2006 Dynamic regulatory interactions of Polycomb group genes: MEDEA autoregulation is required for imprinted gene expression in Arabidopsis. Genes Dev 20 1081 1086

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

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

15. Gutiérrez-MarcosJFCostaLMDal PràMScholtenSKranzE 2006 Epigenetic asymmetry of imprinted genes in plant gametes. Nat Genet 38 876 8

16. HaunWJSpringerNM 2008 Maternal and paternal alleles exhibit differential histone methylation and acetylation at maize imprinted genes. Plant J 56 903 12

17. BabakTDevealeBArmourCRaymondCClearyMA 2008 Global survey of genomic imprinting by transcriptome sequencing. Curr Biol 18 1735 41

18. GreggCZhangJWeissbourdBLuoSSchrothGP 2010 High-Resolution Analysis of Parent-of-Origin Allelic Expression in the Mouse Brain. Science 329 643 648

19. TyckoBMorisonIM 2002 Physiological functions of imprinted genes. Journal of Cellular Physiology 192 245 58

20. WoodAJOakeyRJ 2006 Genomic Imprinting in Mammals: Emerging Themes and Established Theories. PLoS Genet 2 e147 doi:10.1371/journal.pgen.0020147

21. HirasawaRFeilR 2010 Genomic imprinting and human disease. Essays Biochem 48 187 200

22. FrostJMMooreGE 2010 The importance of imprinting in the human placenta. PLoS Genet 6 e1001015 doi:10.1371/journal.pgen.1001015

23. ScottRJSpielmanMBaileyJDickinsonHG 1998 Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125 3329 41

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

25. BirchlerJA 1993 Dosage analysis of maize endosperm development. Ann Rev Genet 27 181 204

26. DrewsGNYadegariR 2002 Development and function of the angiosperm female gametophyte. Annu Rev Genet 36 99 124

27. JahnkeSScholtenS 2009 Epigenetic resetting of a gene imprinted in plant embryos. Curr Biol 19 1677 1681

28. HsiehTFShinJUzawaRSilvaPCohenS 2011 Inaugural Article: Regulation of imprinted gene expression in Arabidopsis endosperm. Proc Natl Acad Sci U S A 108 1755 1762

29. HaigDWestobyM 1989 Parent specific gene expression and the triploid endosperm. Am Nature 134 147 155

30. ChaudhuryAMMingLMillerCCraigSDennisES 1997 Fertilization-independent seed development in Arabidopsis thaliana. Proc Natl Acad Sci USA 94 4223 4228

31. GrossniklausUVielle-CalzadaJPHoeppnerMAGaglianoWB 1998 Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science 280 446 450

32. DilkesBComaiL 2004 A Differential Dosage Hypothesis for Parental Effects in Seed Development. The Plant Cell 16 3174 3180

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

34. KinoshitaT 2007 Reproductive barrier and genomic imprinting in the endosperm of flowering plants. Genes Genet Syst 82 177 86

35. Gutierrez-MarcosJFPenningtonPDCostaLMDickinsonHG 2003 Imprinting in the endosperm: a possible role in preventing wide hybridization. Philos Trans R Soc Lond B Biol Sci 358 1105 11 Review

36. GuoMRupeMADanilevskayaONYangXHuZ 2003 Genome-wide mRNA profiling reveals heterochronic allelic variation and a new imprinted gene in hybrid maize endosperm. Plant J 36 30 44

37. StuparRMHermansonPJSpringerNM 2007 Nonadditive expression and parent-of-origin effects identified by microarray and allele-specific expression profiling of maize endosperm. Plant Physiol 145 411 25

38. DanilevskayaONHermonPHantkeSMuszynskiMGKolliparaK 2003 Duplicated fie genes in maize: expression pattern and imprinting suggest distinct functions. Plant Cell 15 425 438

39. Gutiérrez-MarcosJFCostaLMBiderre-PetitCKhbayaBO'SullivanDM 2004 maternally expressed gene1 is a novel maize endosperm transfer cell-specific gene with a maternal parent-of-origin pattern of expression. Plant Cell 16 1288 1301

40. HermonPSrilunchangKOZouJDresselhausTDanilevskayaON 2007 Activation of the imprinted Polycomb group Fie1 gene in maize endosperm requires demethylation of the maternal allele. Plant Mol Biol 64 387 395

41. LuoMPlattenDChaudhuryAPeacockWJDennisES 2009 Expression, imprinting, and evolution of rice homologs of the polycomb group genes. Mol Plant 2 711 23

42. IshikawaROhnishiTKinoshitaYEiguchiMKurataN 2010 Rice interspecies hybrids show precocious or delayed developmental transitions in the endosperm without change to the rate of syncytial nuclear division. Plant J 65 798 806

43. ItohJNonomuraKIkedaKYamakiSInukaiY 2005 Rice plant development: from zygote to spikelet. Plant Cell Physiol 46 23 47

44. WoodAJSchulzRWoodfineKKoltowskaKBeecheyCV 2008 Regulation of alternative polyadenylation by genomic imprinting. Genes Dev 22 1141 6

45. ThorvaldsenJLBartolomeiMS 2007 SnapShot: Imprinted gene clusters. Cell 130 958

46. de Dios AlchéJM'rani-AlaouiMCastroAJRodríguez-GarcíaMI 2004 Ole e 1, the major allergen from olive (Olea europaea L.) pollen, increases its expression and is released to the culture medium during in vitro germination. Plant Cell Physiol 45 1149 57

47. BayerMNawyTGiglioneCGalliMMeinnelT 2009 Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323 1485 8

48. DenisCLChenJ 2003 The CCR4-NOT complex plays diverse roles in mRNA metabolism. Prog Nucleic Acid Res Mol Biol 73 221 50

49. SpassovDJurecicR 2003 The PUF family of RNA-binding proteins: does evolutionarily conserved structure equal conserved function? IUBMB Life 55 359 366

50. GonzalezDBowenAJCarrollTSConlanRS 2007 The transcription corepressor LEUNIG interacts with the histone deacetylase HDA19 and mediator components MED14 (SWP) and CDK8 (HEN3) to repress transcription. Mol Cell Biol 27 5306 5315

51. KatoHTjernbergAZhangWKrutchinskyANAnW 2002 SYT associates with human SNF/SWI complexes and the C-terminal region of its fusion partner SSX1 targets histones. J Biol Chem 277 5498 505

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

53. XieZJohansenLKGustafsonAMKasschauKDLellisAD 2004 Genetic and Functional Diversification of Small RNA Pathways in Plants. PLoS Biol 2 e104 doi:10.1371/journal.pbio.0020104

54. JacksonJPJohnsonLJasencakovaZZhangXPerezBurgosL 2004 Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112 308 315

55. OgasJKaufmannSHendersonJSomervilleC 1999 PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci U S A 96 13839 44

56. HeGZhuXEllingAAChenLWangX 2010 Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. The Plant Cell 22 17 33

57. RenfreeMBAgerEIShawGPaskAJ 2008 Genomic imprinting in marsupial placentation. Reproduction 136 523 31

58. HsiehTFIbarraCASilvaPZemachAEshed-WilliamsL 2009 Genome-wide demethylation of Arabidopsis endosperm. Science 324 1451 1454

59. KraftEBostickMJacobsenSECallisJ 2008 ORTH/VIM proteins that regulate DNA methylation are functional ubiquitin E3 ligases. Plant J 56 704 715

60. ZemachAKimMYSilvaPRodriguesJADotsonB 2010 Local DNA hypomethylation activates genes in rice endosperm. Proc Natl Acad Sci U S A 107 18729 34

61. LiRLiYKristiansenKWangJ 2008 SOAP: short oligonucleotide alignment program. Bioinformatics 24 713 4

62. International Rice Genome Sequencing Project 2005 The map-based sequence of the rice genome. Nature 436 793 800

63. YuJHuSWangJWongGKLiS 2002 A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Sciense 296 79 92

64. AltschulSFGishWMillerWMyersEWLipmanDJ 1990 Basic local alignment search tool. J Mol Biol 215 403 10

65. GouXPWangSHChenF 1999 Isolation and cytological observation of viable sperm cells of rice. Acta Botanica Sinica 41 669 674

66. XuHTheerakulpisutPGouldingNSuphiogluCSinghMB 1995 Cloning, expression and immunological characterization of Ory s 1, the major allergen of rice pollen. Gene 164 255 9

67. von BesserKFrankACJohnsonMAPreussD 2006 Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development 133 4761 9

68. LiC 2008 Automating dChip: toward reproducible sharing of microarray data analysis. BMC Bioinformatics 9 231

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