The Role of DNA Methylation in Transposable Element Silencing and Genomic Imprinting

Chapter

Abstract

Recent studies in molecular genetics and genomics have shown the significance of DNA methylation in transposable element (TE) silencing and genomic imprinting in plants. Transcriptional silencing of TEs is maintained ubiquitously by DNA methylation, whereas repressing transposition of TEs requires additional and specific mechanisms. The host genome utilizes RNA-directed DNA methylation (RdDM) to repress TEs that is activated by transient loss of DNA methylation. In pollen vegetative cell and female central cell, which are companion cells in plant reproduction, DNA demethylation is observed and causes small interfering RNA (siRNA) accumulation. siRNAs are supposed to be the source of TE silencing in the sperm and egg cells by RdDM. Meanwhile, DNA demethylation in the central cell causes genomic imprinting. In plants, genomic imprinting is observed in the endosperm and controls seed development. Molecular action of DNA methylation in TE silencing and genomic imprinting will be applied to understanding that in developmental processes and environmental response.

Keywords

Epigenetic regulation DNA methylation/demethylation Transposable element Genomic imprinting RNA-directed DNA methylation 

Notes

Acknowledgments

We thank Dr. Olivier Mathieu (Centre National de la Recherche Scientifique, France) for his kind permission to use the photograph shown in Fig. 2.1 and Dr. Tatsuo Kanno (The National Institute of Agrobiological Sciences, Japan) for critical reading of the manuscript. Preparation of this manuscript was supported by the Programme to Disseminate Tenure Tracking System, MEXT, Japan (for YI) and Japanese Science and Technology Agency, PRESTO (for TN).

References

  1. 1.
    Law JA, Jacobsen SE. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet. 2010;11(3):204–20.PubMedCentralCrossRefPubMedGoogle Scholar
  2. 2.
    McClintock B. Chromosome organization and genic expression. Cold Spring Harbor Symp Quant Biol. 1951;16:13–47.CrossRefPubMedGoogle Scholar
  3. 3.
    Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, Chalhoub B, et al. A unified classification system for eukaryotic transposable elements. Nat Rev Genet. 2007;8(12):973–82.CrossRefPubMedGoogle Scholar
  4. 4.
    Buisine N, Quesneville H, Colot V. Improved detection and annotation of transposable elements in sequenced genomes using multiple reference sequence sets. Genomics. 2008;91(5):467–75.CrossRefPubMedGoogle Scholar
  5. 5.
    Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, et al. The B73 maize genome: complexity, diversity, and dynamics. Science. 2009;326(5956):1112–5.CrossRefPubMedGoogle Scholar
  6. 6.
    Lisch D. How important are transposons for plant evolution? Nat Rev Genet. 2013;14(1):49–61.CrossRefPubMedGoogle Scholar
  7. 7.
    Rigal M, Mathieu O. A “mille-feuille” of silencing: epigenetic control of transposable elements. Biochim Biophys Acta. 2011;1809(8):452–8.CrossRefPubMedGoogle Scholar
  8. 8.
    Banks JA, Masson P, Fedoroff N. Molecular mechanisms in the developmental regulation of the maize Suppressor-mutator transposable element. Genes Dev. 1988;2(11):1364–80.CrossRefPubMedGoogle Scholar
  9. 9.
    Chandler VL, Walbot V. DNA Modification of a maize transposable element correlates with loss of activity. Proc Natl Acad Sci U S A. 1986;83(6):1767–71.PubMedCentralCrossRefPubMedGoogle Scholar
  10. 10.
    Chomet PS, Wessler S, Dellaporta SL. Inactivation of the maize transposable element Activator (Ac) is associated with its DNA modification. EMBO J. 1987;6(2):295–302.PubMedCentralPubMedGoogle Scholar
  11. 11.
    Schwartz D, Dennis E. Transposase activity of the Ac controlling element in maize is regulated by its degree of methylation. Mol Gen Genet. 1986;205(3):476–82.CrossRefGoogle Scholar
  12. 12.
    Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature. 2008;452(7184):215–9.PubMedCentralCrossRefPubMedGoogle Scholar
  13. 13.
    Lippman Z, Martienssen R. The role of RNA interference in heterochromatic silencing. Nature. 2004;431(7006):364–70.CrossRefPubMedGoogle Scholar
  14. 14.
    Lister R, O’Malley RC, Tonti-Filippini J, Gregory BD, Berry CC, Millar AH, et al. Highly integrated single-base resolution maps of the epigenome in Arabidopsis. Cell. 2008;133(3):523–36.PubMedCentralCrossRefPubMedGoogle Scholar
  15. 15.
    Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, et al. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell. 2006;126(6):1189–201.CrossRefPubMedGoogle Scholar
  16. 16.
    Miura A, Yonebayashi S, Watanabe K, Toyama T, Shimada H, Kakutani T. Mobilization of transposons by a mutation abolishing full DNA methylation in Arabidopsis. Nature. 2001;411(6834):212–4.CrossRefPubMedGoogle Scholar
  17. 17.
    Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell. 2013;153(1):193–205.PubMedCentralCrossRefPubMedGoogle Scholar
  18. 18.
    Fu Y, Kawabe A, Etcheverry M, Ito T, Toyoda A, Fujiyama A, et al. Mobilization of a plant transposon by expression of the transposon-encoded anti-silencing factor. EMBO J. 2013;32(17):2407–17.PubMedCentralCrossRefPubMedGoogle Scholar
  19. 19.
    Singer T, Yordan C, Martienssen RA. Robertson’s Mutator transposons in A. thaliana are regulated by the chromatin-remodeling gene Decrease in DNA Methylation (DDM1). Genes Dev. 2001;15(5):591–602.PubMedCentralCrossRefPubMedGoogle Scholar
  20. 20.
    Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T. Bursts of retrotransposition reproduced in Arabidopsis. Nature. 2009;461(7262):423–6.CrossRefPubMedGoogle Scholar
  21. 21.
    Mirouze M, Reinders J, Bucher E, Nishimura T, Schneeberger K, Ossowski S, et al. Selective epigenetic control of retrotransposition in Arabidopsis. Nature. 2009;461(7262):427–30.CrossRefPubMedGoogle Scholar
  22. 22.
    Reinders J, Wulff BB, Mirouze M, Mari-Ordonez A, Dapp M, Rozhon W, et al. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 2009;23(8):939–50.PubMedCentralCrossRefPubMedGoogle Scholar
  23. 23.
    Teixeira FK, Heredia F, Sarazin A, Roudier F, Boccara M, Ciaudo C, et al. A role for RNAi in the selective correction of DNA methylation defects. Science. 2009;323(5921):1600–4.CrossRefPubMedGoogle Scholar
  24. 24.
    Pumplin N, Voinnet O. RNA silencing suppression by plant pathogens: defence, counter-defence and counter-counter-defence. Nat Rev Genet. 2013;11(11):745–60.CrossRefGoogle Scholar
  25. 25.
    Garcia D, Garcia S, Pontier D, Marchais A, Renou JP, Lagrange T, et al. Ago hook and RNA helicase motifs underpin dual roles for SDE3 in antiviral defense and silencing of nonconserved intergenic regions. Mol Cell. 2012;48(1):109–20.CrossRefPubMedGoogle Scholar
  26. 26.
    Pontier D, Picart C, Roudier F, Garcia D, Lahmy S, Azevedo J, et al. NERD, a plant-specific GW protein, defines an additional RNAi-dependent chromatin-based pathway in Arabidopsis. Mol Cell. 2012;48(1):121–32.CrossRefPubMedGoogle Scholar
  27. 27.
    Nuthikattu S, McCue AD, Panda K, Fultz D, DeFraia C, Thomas EN, et al. The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21–22 nucleotide small interfering RNAs. Plant Physiol. 2013;162(1):116–31.PubMedCentralCrossRefPubMedGoogle Scholar
  28. 28.
    Mari-Ordonez A, Marchais A, Etcheverry M, Martin A, Colot V, Voinnet O. Reconstructing de novo silencing of an active plant retrotransposon. Nat Genet. 2013;45(9):1029–39.CrossRefPubMedGoogle Scholar
  29. 29.
    Feng S, Jacobsen SE, Reik W. Epigenetic reprogramming in plant and animal development. Science. 2010;330(6004):622–7.PubMedCentralCrossRefPubMedGoogle Scholar
  30. 30.
    Calarco JP, Borges F, Donoghue MT, Van Ex F, Jullien PE, Lopes T, et al. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell. 2012;151(1):194–205.PubMedCentralCrossRefPubMedGoogle Scholar
  31. 31.
    Ibarra CA, Feng X, Schoft VK, Hsieh TF, Uzawa R, Rodrigues JA, et al. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science. 2012;337(6100):1360–4.PubMedCentralCrossRefPubMedGoogle Scholar
  32. 32.
    Schoft VK, Chumak N, Choi Y, Hannon M, Garcia-Aguilar M, Machlicova A, et al. Function of the DEMETER DNA glycosylase in the Arabidopsis thaliana male gametophyte. Proc Natl Acad Sci U S A. 2011;108(19):8042–7.PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijo JA, et al. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell. 2009;136(3):461–72.PubMedCentralCrossRefPubMedGoogle Scholar
  34. 34.
    Kinoshita T, Miura A, Choi Y, Kinoshita Y, Cao X, Jacobsen SE, et al. One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science. 2004;303(5657):521–3.CrossRefPubMedGoogle Scholar
  35. 35.
    Kinoshita Y, Saze H, Kinoshita T, Miura A, Soppe WJ, Koornneef M, et al. Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J. 2007;49(1):38–45.CrossRefPubMedGoogle Scholar
  36. 36.
    Gehring M, Bubb KL, Henikoff S. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science. 2009;324(5933):1447–51.PubMedCentralCrossRefPubMedGoogle Scholar
  37. 37.
    Hsieh TF, Ibarra CA, Silva P, Zemach A, Eshed-Williams L, Fischer RL, et al. Genome-wide demethylation of Arabidopsis endosperm. Science. 2009;324(5933):1451–4.PubMedCentralCrossRefPubMedGoogle Scholar
  38. 38.
    Jullien PE, Mosquna A, Ingouff M, Sakata T, Ohad N, Berger F. Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biol. 2008;6(8):e194.PubMedCentralCrossRefPubMedGoogle Scholar
  39. 39.
    Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ, Goldberg RB, et al. DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell. 2002;110(1):33–42.CrossRefPubMedGoogle Scholar
  40. 40.
    Gehring M, Huh JH, Hsieh TF, Penterman J, Choi Y, Harada JJ, et al. DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell. 2006;124(3):495–506.PubMedCentralCrossRefPubMedGoogle Scholar
  41. 41.
    Andreuzza S, Li J, Guitton AE, Faure JE, Casanova S, Park JS, et al. DNA LIGASE I exerts a maternal effect on seed development in Arabidopsis thaliana. Development. 2010;137(1):73–81.CrossRefPubMedGoogle Scholar
  42. 42.
    Martinez-Macias MI, Cordoba-Canero D, Ariza RR, Roldan-Arjona T. The DNA repair protein XRCC1 functions in the plant DNA demethylation pathway by stimulating cytosine methylation (5-meC) excision, gap tailoring, and DNA ligation. J Biol Chem. 2013;288(8):5496–505.PubMedCentralCrossRefPubMedGoogle Scholar
  43. 43.
    Martinez-Macias MI, Qian W, Miki D, Pontes O, Liu Y, Tang K, et al. A DNA 3ʹ phosphatase functions in active DNA demethylation in Arabidopsis. Mol Cell. 2012;45(3):357–70.PubMedCentralCrossRefPubMedGoogle Scholar
  44. 44.
    Kinoshita T, Yadegari R, Harada JJ, Goldberg RB, Fischer RL. Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell. 1999;11(10):1945–52.PubMedCentralCrossRefPubMedGoogle Scholar
  45. 45.
    Vielle-Calzada JP, Thomas J, Spillane C, Coluccio A, Hoeppner MA, Grossniklaus U. Maintenance of genomic imprinting at the Arabidopsis medea locus requires zygotic DDM1 activity. Genes Dev. 1999;13(22):2971–82.PubMedCentralCrossRefPubMedGoogle Scholar
  46. 46.
    Xiao W, Gehring M, Choi Y, Margossian L, Pu H, Harada JJ, et al. Imprinting of the MEA Polycomb gene is controlled by antagonism between MET1 methyltransferase and DME glycosylase. Dev Cell. 2003;5(6):891–901.CrossRefPubMedGoogle Scholar
  47. 47.
    Wohrmann HJ, Gagliardini V, Raissig MT, Wehrle W, Arand J, Schmidt A, et al. Identification of a DNA methylation-independent imprinting control region at the Arabidopsis MEDEA locus. Genes Dev. 2012;26(16):1837–50.PubMedCentralCrossRefPubMedGoogle Scholar
  48. 48.
    Makarevich G, Villar CB, Erilova A, Kohler C. Mechanism of PHERES1 imprinting in Arabidopsis. J Cell Sci. 2008;121(6):906–12.CrossRefPubMedGoogle Scholar
  49. 49.
    Weinhofer I, Hehenberger E, Roszak P, Hennig L, Kohler C. H3K27me3 profiling of the endosperm implies exclusion of polycomb group protein targeting by DNA methylation. PLoS Genet. 2010;6(10):e1001152.PubMedCentralCrossRefPubMedGoogle Scholar
  50. 50.
    Baroux C, Gagliardini V, Page DR, Grossniklaus U. Dynamic regulatory interactions of Polycomb group genes: MEDEA autoregulation is required for imprinted gene expression in Arabidopsis. Genes Dev. 2006;20(9):1081–6.PubMedCentralCrossRefPubMedGoogle Scholar
  51. 51.
    Jullien PE, Katz A, Oliva M, Ohad N, Berger F. Polycomb group complexes self-regulate imprinting of the Polycomb group gene MEDEA in Arabidopsis. Curr Biol. 2006;16(5):486–92.CrossRefPubMedGoogle Scholar
  52. 52.
    Ikeda Y, Kinoshita Y, Susaki D, Iwano M, Takayama S, Higashiyama T, et al. HMG domain containing SSRP1 is required for DNA demethylation and genomic imprinting in Arabidopsis. Dev Cell. 2011;21(3):589–96.CrossRefPubMedGoogle Scholar
  53. 53.
    Rea M, Zheng W, Chen M, Braud C, Bhangu D, Rognan TN, et al. Histone H1 affects gene imprinting and DNA methylation in Arabidopsis. Plant J. 2012;71(5):776–86.PubMedCentralCrossRefPubMedGoogle Scholar
  54. 54.
    Qian W, Miki D, Zhang H, Liu Y, Zhang X, Tang K, et al. A histone acetyltransferase regulates active DNA demethylation in Arabidopsis. Science. 2012;336(6087):1445–8.PubMedCentralCrossRefPubMedGoogle Scholar
  55. 55.
    Zheng X, Pontes O, Zhu J, Miki D, Zhang F, Li WX, et al. ROS3 is an RNA-binding protein required for DNA demethylation in Arabidopsis. Nature. 2008;455(7217):1259–62.PubMedCentralCrossRefPubMedGoogle Scholar
  56. 56.
    Jahnke S, Scholten S. Epigenetic resetting of a gene imprinted in plant embryos. Curr Biol. 2009;19(19):1677–81.CrossRefPubMedGoogle Scholar
  57. 57.
    Luo M, Taylor JM, Spriggs A, Zhang H, Wu X, Russell S, et al. A genome-wide survey of imprinted genes in rice seeds reveals imprinting primarily occurs in the endosperm. PLoS Genet. 2011;7(6):e1002125.PubMedCentralCrossRefPubMedGoogle Scholar
  58. 58.
    Gehring M, Missirian V, Henikoff S. Genomic analysis of parent-of-origin allelic expression in Arabidopsis thaliana seeds. PLoS One. 2011;6(8):e23687.PubMedCentralCrossRefPubMedGoogle Scholar
  59. 59.
    Hsieh TF, Shin J, Uzawa R, Silva P, Cohen S, Bauer MJ, et al. Regulation of imprinted gene expression in Arabidopsis endosperm. Proc Natl Acad Sci U S A. 2011;108(5):1755–62.PubMedCentralCrossRefPubMedGoogle Scholar
  60. 60.
    Nodine MD, Bartel DP. Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature. 2012;482(7383):94–7.PubMedCentralCrossRefPubMedGoogle Scholar
  61. 61.
    Jullien PE, Susaki D, Yelagandula R, Higashiyama T, Berger F. DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr Biol. 2012;22(19):1825–30.CrossRefPubMedGoogle Scholar
  62. 62.
    Vu TM, Nakamura M, Calarco JP, Susaki D, Lim PQ, Kinoshita T, et al. RNA-directed DNA methylation regulates parental genomic imprinting at several loci in Arabidopsis. Development. 2013;140(14):2953–60.PubMedCentralCrossRefPubMedGoogle Scholar
  63. 63.
    Mosher RA, Melnyk CW, Kelly KA, Dunn RM, Studholme DJ, Baulcombe DC. Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature. 2009;460(7252):283–6.CrossRefPubMedGoogle Scholar
  64. 64.
    Lu J, Zhang C, Baulcombe DC, Chen ZJ. Maternal siRNAs as regulators of parental genome imbalance and gene expression in endosperm of Arabidopsis seeds. Proc Natl Acad Sci U S A. 2012;109(14):5529–34.PubMedCentralCrossRefPubMedGoogle Scholar
  65. 65.
    Ikeda Y. Plant imprinted genes identified by genome-wide approaches and their regulatory mechanisms. Plant Cell Physiol. 2012;53(5):809–16.CrossRefPubMedGoogle Scholar
  66. 66.
    Pignatta D, Gehring M. Imprinting meets genomics: new insights and new challenges. Curr Opin Plant Biol. 2012;15(5):530–5.CrossRefPubMedGoogle Scholar
  67. 67.
    Waters AJ, Bilinski P, Eichten SR, Vaughn MW, Ross-Ibarra J, Gehring M, et al. Comprehensive analysis of imprinted genes in maize reveals allelic variation for imprinting and limited conservation with other species. Proc Natl Acad Sci U S A. 2013;110(48):19639–44.PubMedCentralCrossRefPubMedGoogle Scholar
  68. 68.
    Wolff P, Weinhofer I, Seguin J, Roszak P, Beisel C, Donoghue MT, et al. High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis Endosperm. PLoS Genet. 2011;7(6):e1002126.PubMedCentralCrossRefPubMedGoogle Scholar
  69. 69.
    Zhang M, Zhao H, Xie S, Chen J, Xu Y, Wang K, et al. Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm. Proc Natl Acad Sci U S A. 2011;108(50):20042–7.PubMedCentralCrossRefPubMedGoogle Scholar
  70. 70.
    Kawabe A, Fujimoto R, Charlesworth D. High diversity due to balancing selection in the promoter region of the Medea gene in Arabidopsis lyrata. Curr Biol. 2007;17(21):1885–9.CrossRefPubMedGoogle Scholar
  71. 71.
    Miyake T, Takebayashi N, Wolf DE. Possible diversifying selection in the imprinted gene, MEDEA, in Arabidopsis. Mol Biol Evol. 2009;26(4):843–57.PubMedCentralCrossRefPubMedGoogle Scholar
  72. 72.
    Spillane C, Schmid KJ, Laoueille-Duprat S, Pien S, Escobar-Restrepo JM, Baroux C, et al. Positive Darwinian selection at the imprinted MEDEA locus in plants. Nature. 2007;448(7151):349–52.CrossRefPubMedGoogle Scholar
  73. 73.
    Yoshida T, Kawabe A. Importance of gene duplication in the evolution of genomic imprinting revealed by molecular evolutionary analysis of the type I MADS-box gene family in Arabidopsis species. PLoS One. 2013;8(9):e73588.PubMedCentralCrossRefPubMedGoogle Scholar
  74. 74.
    Smith ZD, Meissner A. DNA methylation: roles in mammalian development. Nat Rev Genet. 2013;14(3):204–20.CrossRefPubMedGoogle Scholar
  75. 75.
    Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, et al. Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet. 2009;5(6):e1000530.PubMedCentralCrossRefPubMedGoogle Scholar
  76. 76.
    Li W, Liu H, Cheng ZJ, Su YH, Han HN, Zhang Y, et al. DNA methylation and histone modifications regulate de novo shoot regeneration in Arabidopsis by modulating WUSCHEL expression and auxin signaling. PLoS Genet. 2011;7(8):e1002243.PubMedCentralCrossRefPubMedGoogle Scholar
  77. 77.
    Iwasaki M, Takahashi H, Iwakawa H, Nakagawa A, Ishikawa T, Tanaka H, et al. Dual regulation of ETTIN (ARF3) gene expression by AS1-AS2, which maintains the DNA methylation level, is involved in stabilization of leaf adaxial-abaxial partitioning in Arabidopsis. Development. 2013;140(9):1958–69.CrossRefPubMedGoogle Scholar
  78. 78.
    Dowen RH, Pelizzola M, Schmitz RJ, Lister R, Dowen JM, Nery JR, et al. Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci U S A. 2012;109(32):E2183–91.PubMedCentralCrossRefPubMedGoogle Scholar
  79. 79.
    Haun WJ, Laoueille-Duprat S, O’Connell M J, Spillane C, Grossniklaus U, Phillips AR, et al. Genomic imprinting, methylation and molecular evolution of maize Enhancer of zeste (Mez) homologs. Plant J. 2007;49(2):325–37.CrossRefPubMedGoogle Scholar
  80. 80.
    Haun WJ, Springer NM. Maternal and paternal alleles exhibit differential histone methylation and acetylation at maize imprinted genes. Plant J. 2008;56(6):903–12.CrossRefPubMedGoogle Scholar
  81. 81.
    Gutierrez-Marcos JF, Costa LM, Dal Pra M, Scholten S, Kranz E, Perez P, et al. Epigenetic asymmetry of imprinted genes in plant gametes. Nat Genet. 2006;38(8):876–8.CrossRefPubMedGoogle Scholar
  82. 82.
    Ishikawa R, Ohnishi T, Kinoshita Y, Eiguchi M, Kurata N, Kinoshita T. Rice interspecies hybrids show precocious or delayed developmental transitions in the endosperm without change to the rate of syncytial nuclear division. Plant J. 2011;65(5):798–806.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Institute of Plant Science and ResourcesOkayama UniversityOkayamaJapan
  2. 2.PRESTO, Japanese Science and Technology AgencyTokyoJapan
  3. 3.Bioscience and Biotechnology CenterNagoya UniversityNagoyaJapan
  4. 4.Nagaoka University of TechnologyNagaokaJapan

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