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Nuclear Functions in Plant Transcription, Signaling and Development pp 93–118Cite as

Setting the Stage for the Next Generation: Epigenetic Reprogramming During Sexual Plant Reproduction

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Abstract

During their life cycle, plants are faced with multiple environmental challenges which they have to contend with in order to survive and be able to reproduce. The way plants respond to stress results from modifications in gene expression that seem to be at least partially mediated by changes in the epigenetic landscape. Epigenetic marks can be stably propagated through cell divisions, be transmitted to the next generation, or just be transiently established but erased later in the plant life cycle. The transition from sporophyte to a gametophytic life phase is marked by an extensive epigenetic reconfiguration that leads to specification and differentiation of haploid male and female gametes holding distinct epigenetic states. Reshuffling of the parental epigenomes through fertilization tailors the fate of two distinct fertilization products, the zygote and the nourishing endosperm, ultimately contributing to re-establish embryo pluripotency and epiallele inheritance to the next generation. In this chapter, we describe recent advances obtained by genome-wide, cell-type-specific DNA methylomes of gametophytic stages and discuss how previously unknown (epi) genetic regulatory mechanisms occurring during gametogenesis may contribute to understand how genome integrity and stability is preserved during gametogenesis and fertilization and its impact in post-fertilization development.

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References

  1. Grant-Downton RT, Dickinson HG. Epigenetics and its implications for plant biology 2. The ʻepigenetic epiphany’: epigenetics, evolution and beyond. Ann Bot. 2006;97(1):11–27.

    PubMed Central  CAS  PubMed  Google Scholar 

  2. Pereira PA, Navarro-Costa P, Martinho RG, Becker JD. Evolutionarily-conserved mechanisms of male germline development in flowering plants and animals. Biochem Soc Trans. 2014;42:377–82.

    CAS  PubMed  Google Scholar 

  3. Huijser P, Schmid M. The control of developmental phase transitions in plants. Development. 2011;138(19):4117–29.

    CAS  PubMed  Google Scholar 

  4. Madlung A, Comai L. The effect of stress on genome regulation and structure. Ann Bot. 2004;94(4):481–95.

    PubMed Central  CAS  PubMed  Google Scholar 

  5. Boyko A, Kovalchuk I. Transgenerational response to stress in Arabidopsis thaliana. Plant Signal Behav. 2010;5(8):995–8.

    PubMed Central  CAS  PubMed  Google Scholar 

  6. Saze H. Epigenetic memory transmission through mitosis and meiosis in plants. Semin Cell Dev Biol. 2008;19(6):527–36.

    PubMed  Google Scholar 

  7. Eichten S, Borevitz J. Epigenomics: methylation’s mark on inheritance. Nature. 2013;495(7440):181–2.

    CAS  PubMed  Google Scholar 

  8. Jacobsen SE, Meyerowitz EM. Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science. 1997;277(5329):1100–3.

    CAS  PubMed  Google Scholar 

  9. Finnegan EJ, Peacock WJ, Dennis ES. Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc Natl Acad Sci U S A. 1996;93(16):8449–54.

    PubMed Central  CAS  PubMed  Google Scholar 

  10. Hirsch S, Baumberger R, Grossniklaus U. Epigenetic variation, inheritance, and selection in plant populations. Cold Spring Harb Symp Quant Biol. 2012;77:97–104.

    CAS  PubMed  Google Scholar 

  11. 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.

    CAS  PubMed  Google Scholar 

  12. Oliver KR, McComb JA, Greene WK. Transposable elements: powerful contributors to angiosperm evolution and diversity. Genome Biol Evol. 2013;5(10):1886–901.

    PubMed Central  PubMed  Google Scholar 

  13. Amasino RM, Michaels SD. The timing of flowering. Plant Physiol. 2010;154(2):516–20.

    PubMed Central  CAS  PubMed  Google Scholar 

  14. Deng W, Ying H, Helliwell CA, Taylor JM, Peacock WJ, Dennis ES. FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc Natl Acad Sci U S A. 2011;108(16):6680–5.

    PubMed Central  CAS  PubMed  Google Scholar 

  15. Willmann MR, Poethig RS. The effect of the floral repressor FLC on the timing and progression of vegetative phase change in Arabidopsis. Development. 2011;138(4):677–85.

    PubMed Central  CAS  PubMed  Google Scholar 

  16. He Y, Amasino RM. Role of chromatin modification in flowering-time control. Trends Plant Sci. 2005;10(1):30–5.

    CAS  PubMed  Google Scholar 

  17. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature. 2004;427(6970):164–7.

    CAS  PubMed  Google Scholar 

  18. He Y, Michaels SD, Amasino RM. Regulation of flowering time by histone acetylation in Arabidopsis. Science. 2003;302(5651):1751–4.

    CAS  PubMed  Google Scholar 

  19. He Y. Control of the transition to flowering by chromatin modifications. Mol Plant. 2009;2(4):554–64.

    CAS  PubMed  Google Scholar 

  20. Sung S, Amasino RM. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature. 2004;427(6970):159–64.

    CAS  PubMed  Google Scholar 

  21. De Lucia F, Crevillen P, Jones AM, Greb T, Dean C. A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci U S A. 2008;105(44):16831–6.

    PubMed Central  PubMed  Google Scholar 

  22. Schubert D, Primavesi L, Bishopp A, Roberts G, Doonan J, Jenuwein T, et al. Silencing by plant polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. EMBO J. 2006;25(19):4638–49.

    PubMed Central  CAS  PubMed  Google Scholar 

  23. Angel A, Song J, Dean C, Howard M. A polycomb-based switch underlying quantitative epigenetic memory. Nature. 2011;476(7358):105–8.

    CAS  PubMed  Google Scholar 

  24. Liu F, Marquardt S, Lister C, Swiezewski S, Dean C. Targeted 3' processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science. 2010;327(5961):94–7.

    CAS  PubMed  Google Scholar 

  25. Swiezewski S, Liu F, Magusin A, Dean C. Cold-induced silencing by long antisense transcripts of an Arabidopsis polycomb target. Nature. 2009;462(7274):799–802.

    CAS  PubMed  Google Scholar 

  26. Sheldon CC, Hills MJ, Lister C, Dean C, Dennis ES, Peacock WJ. Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proc Natl Acad Sci U S A. 2008;105(6):2214–9.

    PubMed Central  CAS  PubMed  Google Scholar 

  27. Choi J, Hyun Y, Kang MJ, In Yun H, Yun JY, Lister C, et al. Resetting and regulation of Flowering Locus C expression during Arabidopsis reproductive development. Plant J. 2009;57(5):918–31.

    CAS  PubMed  Google Scholar 

  28. Turck F, Fornara F, Coupland G. Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol. 2008;59:573–94.

    CAS  PubMed  Google Scholar 

  29. Smaczniak C, Immink RG, Muino JM, Blanvillain R, Busscher M, Busscher-Lange J, et al. Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci U S A. 2012;109(5):1560–5.

    PubMed Central  CAS  PubMed  Google Scholar 

  30. Feng X, Zilberman D, Dickinson H. A conversation across generations: soma-germ cell crosstalk in plants. Dev Cell. 2013;24(3):215–25.

    CAS  PubMed  Google Scholar 

  31. Boavida LC, Becker JD, Feijo JA. The making of gametes in higher plants. Int J Dev Biol. 2005;49(5–6):595–614.

    CAS  PubMed  Google Scholar 

  32. Horvitz HR, Herskowitz I. Mechanisms of asymmetric cell division: two Bs or not two Bs, that is the question. Cell. 1992;68(2):237–55.

    CAS  PubMed  Google Scholar 

  33. Eady C, Lindsey K, Twell D. The significance of microspore division and division symmetry for vegetative cell-specific transcription and generative cell differentiation. Plant Cell. 1995;7(1):65–74.

    PubMed Central  CAS  PubMed  Google Scholar 

  34. McCue AD, Cresti M, Feijo JA, Slotkin RK. Cytoplasmic connection of sperm cells to the pollen vegetative cell nucleus: potential roles of the male germ unit revisited. J Exp Bot. 2011;62(5):1621–31.

    CAS  PubMed  Google Scholar 

  35. 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.

    PubMed Central  CAS  PubMed  Google Scholar 

  36. Boavida LC, Qin P, Broz M, Becker JD, McCormick S. Arabidopsis tetraspanins are confined to discrete expression domains and cell types in reproductive tissues and form homo- and heterodimers when expressed in yeast. Plant Physiol. 2013;163(2):696–712.

    PubMed Central  CAS  PubMed  Google Scholar 

  37. Palanivelu R, Preuss D. Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro. BMC Plant Biol. 2006;6:7.

    PubMed Central  PubMed  Google Scholar 

  38. Friedman WE. Expression of the cell cycle in sperm of Arabidopsis: implications for understanding patterns of gametogenesis and fertilization in plants and other eukaryotes. Development. 1999;126(5):1065–75.

    CAS  PubMed  Google Scholar 

  39. Ingouff M, Sakata T, Li J, Sprunck S, Dresselhaus T, Berger F. The two male gametes share equal ability to fertilize the egg cell in Arabidopsis thaliana. Curr Biol. 2009;19(1):R19–20.

    CAS  PubMed  Google Scholar 

  40. Solis MT, Chakrabarti N, Corredor E, Cortes-Eslava J, Rodriguez-Serrano M, Biggiogera M, et al. Epigenetic changes accompany developmental programmed cell death in tapetum cells. Plant Cell Physiol. 2014;55(1):16–29.

    CAS  PubMed  Google Scholar 

  41. Millar AA, Gubler F. The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell. 2005;17(3):705–21.

    PubMed Central  CAS  PubMed  Google Scholar 

  42. Grini PE, Thorstensen T, Alm V, Vizcay-Barrena G, Windju SS, Jorstad TS, et al. The ASH1 HOMOLOG 2 (ASHH2) histone H3 methyltransferase is required for ovule and anther development in Arabidopsis. PloS One. 2009;4(11):e7817.

    PubMed Central  PubMed  Google Scholar 

  43. Tarutani Y, Shiba H, Iwano M, Kakizaki T, Suzuki G, Watanabe M, et al. Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility. Nature. 2010;466(7309):983–6.

    CAS  PubMed  Google Scholar 

  44. Mirouze M, Lieberman-Lazarovich M, Aversano R, Bucher E, Nicolet J, Reinders J, et al. Loss of DNA methylation affects the recombination landscape in Arabidopsis. Proc Natl Acad Sci U S A. 2012;109(15):5880–5.

    PubMed Central  CAS  PubMed  Google Scholar 

  45. Yelina NE, Choi K, Chelysheva L, Macaulay M, de Snoo B, Wijnker E, et al. Epigenetic remodeling of meiotic crossover frequency in Arabidopsis thaliana DNA methyltransferase mutants. PLoS Genet. 2012;8(8):e1002844.

    PubMed Central  CAS  PubMed  Google Scholar 

  46. Perrella G, Consiglio MF, Aiese-Cigliano R, Cremona G, Sanchez-Moran E, Barra L, et al. Histone hyperacetylation affects meiotic recombination and chromosome segregation in Arabidopsis. Plant J. 2010;62(5):796–806.

    CAS  PubMed  Google Scholar 

  47. Melamed-Bessudo C, Levy AA. Deficiency in DNA methylation increases meiotic crossover rates in euchromatic but not in heterochromatic regions in Arabidopsis. Proc Natl Acad Sci U S A. 2012;109(16):E981–8.

    PubMed Central  CAS  PubMed  Google Scholar 

  48. Nonomura K, Morohoshi A, Nakano M, Eiguchi M, Miyao A, Hirochika H, et al. A germ cell specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell. 2007;19(8):2583–94.

    PubMed Central  CAS  PubMed  Google Scholar 

  49. Tucker MR, Okada T, Hu Y, Scholefield A, Taylor JM, Koltunow AM. Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in Arabidopsis. Development. 2012;139(8):1399–404.

    CAS  PubMed  Google Scholar 

  50. Chen C, Retzel EF. Analyzing the meiotic transcriptome using isolated meiocytes of Arabidopsis thaliana. Methods Mol Biol. 2013;990:203–13.

    CAS  PubMed  Google Scholar 

  51. Yang H, Lu P, Wang Y, Ma H. The transcriptome landscape of Arabidopsis male meiocytes from high-throughput sequencing: the complexity and evolution of the meiotic process. Plant J. 2011;65(4):503–16.

    CAS  PubMed  Google Scholar 

  52. Ingouff M, Rademacher S, Holec S, Soljic L, Xin N, Readshaw A, et al. Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr Biol. 2010;20(23):2137–43.

    CAS  PubMed  Google Scholar 

  53. Ingouff M, Hamamura Y, Gourgues M, Higashiyama T, Berger F. Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr Biol. 2007;17(12):1032–7.

    CAS  PubMed  Google Scholar 

  54. Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijo JA, et al. Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol. 2008;148(2):1168–81.

    PubMed Central  CAS  PubMed  Google Scholar 

  55. Borges F, Pereira PA, Slotkin RK, Martienssen RA, Becker JD. MicroRNA activity in the Arabidopsis male germline. J Exp Bot. 2011;62(5):1611–20.

    CAS  PubMed  Google Scholar 

  56. Borges F, Gardner R, Lopes T, Calarco JP, Boavida LC, Slotkin RK, et al. FACS-based purification of Arabidopsis microspores, sperm cells and vegetative nuclei. Plant Methods. 2012;8(1):44.

    PubMed Central  CAS  PubMed  Google Scholar 

  57. 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.

    PubMed Central  CAS  PubMed  Google Scholar 

  58. 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.

    PubMed Central  CAS  PubMed  Google Scholar 

  59. 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.

    PubMed Central  CAS  PubMed  Google Scholar 

  60. Schoft VK, Chumak N, Mosiolek M, Slusarz L, Komnenovic V, Brownfield L, et al. Induction of RNA-directed DNA methylation upon decondensation of constitutive heterochromatin. EMBO Rep. 2009;10(9):1015–21.

    PubMed Central  CAS  PubMed  Google Scholar 

  61. 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.

    PubMed Central  CAS  PubMed  Google Scholar 

  62. Kakutani T, Jeddeloh JA, Flowers SK, Munakata K, Richards EJ. Developmental abnormalities and epimutations associated with DNA hypomethylation mutations. Proc Natl Acad Sci U S A. 1996;93(22):12406–11.

    PubMed Central  CAS  PubMed  Google Scholar 

  63. McCue AD, Nuthikattu S, Reeder SH, Slotkin RK. Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLoS Genet. 2012;8(2):e1002474.

    PubMed Central  CAS  PubMed  Google Scholar 

  64. McCue AD, Nuthikattu S, Slotkin RK. Genome-wide identification of genes regulated in trans by transposable element small interfering RNAs. RNA Biol. 2013;10(8):1379–95.

    PubMed Central  CAS  PubMed  Google Scholar 

  65. Honys D, Twell D. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 2004;5(11):R85.

    PubMed Central  PubMed  Google Scholar 

  66. Gehring M, Bubb KL, Henikoff S. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science. 2009;324(5933):1447–51.

    PubMed Central  CAS  PubMed  Google Scholar 

  67. 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.

    PubMed Central  CAS  PubMed  Google Scholar 

  68. Becker C, Hagmann J, Muller J, Koenig D, Stegle O, Borgwardt K, et al. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature. 2011;480(7376):245–9.

    CAS  PubMed  Google Scholar 

  69. Schmitz RJ, Schultz MD, Lewsey MG, O'Malley RC, Urich MA, Libiger O, et al. Transgenerational epigenetic instability is a source of novel methylation variants. Science. 2011;334(6054):369–73.

    PubMed Central  CAS  PubMed  Google Scholar 

  70. Grant-Downton R, Kourmpetli S, Hafidh S, Khatab H, Le Trionnaire G, Dickinson H, et al. Artificial microRNAs reveal cell-specific differences in small RNA activity in pollen. Curr Biol. 2013;23(14):R599–601.

    CAS  PubMed  Google Scholar 

  71. She W, Grimanelli D, Rutowicz K, Whitehead MW, Puzio M, Kotlinski M, et al. Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants. Development. 2013;140(19):4008–19.

    CAS  PubMed  Google Scholar 

  72. Olmedo-Monfil V, Duran-Figueroa N, Arteaga-Vazquez M, Demesa-Arevalo E, Autran D, Grimanelli D, et al. Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature. 2010;464(7288):628–32.

    CAS  PubMed  Google Scholar 

  73. Singh M, Goel S, Meeley RB, Dantec C, Parrinello H, Michaud C, et al. Production of viable gametes without meiosis in maize deficient for an ARGONAUTE protein. Plant Cell. 2011;23(2):443–58.

    PubMed Central  CAS  PubMed  Google Scholar 

  74. Duran-Figueroa N, Vielle-Calzada JP. ARGONAUTE9-dependent silencing of transposable elements in pericentromeric regions of Arabidopsis. Plant Signal Behav. 2010;5(11):1476–9.

    PubMed Central  CAS  PubMed  Google Scholar 

  75. Dunoyer P, Lecellier CH, Parizotto EA, Himber C, Voinnet O. Probing the microRNA and small interfering RNA pathways with virus-encoded suppressors of RNA silencing. Plant Cell. 2004;16(5):1235–50.

    PubMed Central  CAS  PubMed  Google Scholar 

  76. Garcia-Aguilar M, Michaud C, Leblanc O, Grimanelli D. Inactivation of a DNA methylation pathway in maize reproductive organs results in apomixis-like phenotypes. Plant Cell. 2010;22(10):3249–67.

    PubMed Central  CAS  PubMed  Google Scholar 

  77. Pillot M, Baroux C, Vazquez MA, Autran D, Leblanc O, Vielle-Calzada JP, et al. Embryo and endosperm inherit distinct chromatin and transcriptional states from the female gametes in Arabidopsis. Plant Cell. 2010;22(2):307–20.

    PubMed Central  CAS  PubMed  Google Scholar 

  78. 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.

    CAS  PubMed  Google Scholar 

  79. Calarco JP, Martienssen RA. Imprinting: DNA methyltransferases illuminate reprogramming. Curr Biol. 2012;22(21):R929–31.

    CAS  PubMed  Google Scholar 

  80. Ikeda Y. Plant imprinted genes identified by genome-wide approaches and their regulatory mechanisms. Plant Cell Physiol. 2012;53(5):809–16.

    CAS  PubMed  Google Scholar 

  81. Pillot M, Autran D, Leblanc O, Grimanelli D. A role for CHROMOMETHYLASE3 in mediating transposon and euchromatin silencing during egg cell reprogramming in Arabidopsis. Plant Signal Behav. 2010;5(10):1167–70.

    PubMed Central  CAS  PubMed  Google Scholar 

  82. 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.

    CAS  PubMed  Google Scholar 

  83. 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.

    PubMed Central  CAS  PubMed  Google Scholar 

  84. Jullien PE, Kinoshita T, Ohad N, Berger F. Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. Plant Cell. 2006;18(6):1360–72.

    PubMed Central  CAS  PubMed  Google Scholar 

  85. Costa LM, Gutierrez-Marcos JF. Retinoblastoma makes its mark on imprinting in plants. PLoS Biol. 2008;6(8):e212.

    PubMed Central  PubMed  Google Scholar 

  86. 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.

    CAS  PubMed  Google Scholar 

  87. Eamens A, Vaistij FE, Jones L. NRPD1a and NRPD1b are required to maintain post-transcriptional RNA silencing and RNA-directed DNA methylation in Arabidopsis. Plant J. 2008;55(4):596–606.

    CAS  PubMed  Google Scholar 

  88. 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.

    CAS  PubMed  Google Scholar 

  89. Berger F, Grini PE, Schnittger A. Endosperm: an integrator of seed growth and development. Curr Opin Plant Biol. 2006;9(6):664–70.

    CAS  PubMed  Google Scholar 

  90. Hsieh TF, Ibarra CA, Silva P, Zemach A, Eshed-Williams L, Fischer RL, et al. Genomewide demethylation of Arabidopsis endosperm. Science. 2009;324(5933):1451–4.

    PubMed Central  CAS  PubMed  Google Scholar 

  91. 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.

    PubMed Central  PubMed  Google Scholar 

  92. Martienssen RA. Heterochromatin, small RNA and post-fertilization dysgenesis in allopolyploid and interploid hybrids of Arabidopsis. New Phytol. 2010;186(1):46–53.

    PubMed Central  CAS  PubMed  Google Scholar 

  93. Bourc'his D, Voinnet O. A small-RNA perspective on gametogenesis, fertilization, and early zygotic development. Science. 2010;330(6004):617–22.

    PubMed  Google Scholar 

  94. Ng DW, Lu J, Chen ZJ. Big roles for small RNAs in polyploidy, hybrid vigor, and hybrid incompatibility. Curr Opin Plant Biol. 2012;15(2):154–61.

    CAS  PubMed  Google Scholar 

  95. Josefsson C, Dilkes B, Comai L. Parent-dependent loss of gene silencing during interspecies hybridization. Curr Biol. 2006;16(13):1322–8.

    CAS  PubMed  Google Scholar 

  96. Ha M, Lu J, Tian L, Ramachandran V, Kasschau KD, Chapman EJ, et al. Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc Natl Acad Sci U S A. 2009;106(42):17835–40.

    PubMed Central  CAS  PubMed  Google Scholar 

  97. Brennecke J, Malone CD, Aravin AA, Sachidanandam R, Stark A, Hannon GJ. An epigenetic role for maternally inherited piRNAs in transposon silencing. Science. 2008;322(5906):1387–92.

    PubMed Central  CAS  PubMed  Google Scholar 

  98. Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W. Paternal control of embryonic patterning in Arabidopsis thaliana. Science. 2009;323(5920):1485–8.

    CAS  PubMed  Google Scholar 

  99. Krawetz SA, Kruger A, Lalancette C, Tagett R, Anton E, Draghici S, et al. A survey of small RNAs in human sperm. Hum Reprod. 2011;26(12):3401–12.

    PubMed Central  CAS  PubMed  Google Scholar 

  100. Sendler E, Johnson GD, Mao S, Goodrich RJ, Diamond MP, Hauser R, et al. Stability, delivery and functions of human sperm RNAs at fertilization. Nuc Acids Res. 2013;41(7):4104–17.

    CAS  Google Scholar 

  101. Conine CC, Moresco JJ, Gu W, Shirayama M, Conte D, Jr., Yates JR, 3rd, et al. Argonautes promote male fertility and provide a paternal memory of germline gene expression in C. elegans. Cell. 2013;155(7):1532–44.

    PubMed Central  CAS  PubMed  Google Scholar 

  102. Baroux C, Autran D, Gillmor CS, Grimanelli D, Grossniklaus U. The maternal to zygotic transition in animals and plants. Cold Spring Harb Symp Quant Biol. 2008;73:89–100.

    CAS  PubMed  Google Scholar 

  103. Autran D, Baroux C, Raissig MT, Lenormand T, Wittig M, Grob S, et al. Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Cell. 2011;145(5):707–19.

    CAS  PubMed  Google Scholar 

  104. Vielle-Calzada JP, Baskar R, Grossniklaus U. Delayed activation of the paternal genome during seed development. Nature. 2000;404(6773):91–4.

    CAS  PubMed  Google Scholar 

  105. Grimanelli D, Perotti E, Ramirez J, Leblanc O. Timing of the maternal-to-zygotic transition during early seed development in maize. Plant Cell. 2005;17(4):1061–72.

    PubMed Central  CAS  PubMed  Google Scholar 

  106. Feng S, Jacobsen SE, Reik W. Epigenetic reprogramming in plant and animal development. Science. 2010;330(6004):622–7.

    PubMed Central  CAS  PubMed  Google Scholar 

  107. Saze H, Mittelsten Scheid O, Paszkowski J. Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nat Genet. 2003;34(1):65–9.

    CAS  PubMed  Google Scholar 

  108. Meyer S, Scholten S. Equivalent parental contribution to early plant zygotic development. Curr Biol. 2007;17(19):1686–91.

    CAS  PubMed  Google Scholar 

  109. Scott RJ, Spielman M. Genomic imprinting in plants and mammals: how life history constrains convergence. Cytogenet Genome Res. 2006;113(1–4):53–67.

    CAS  PubMed  Google Scholar 

  110. Kohler C, Wolff P, Spillane C. Epigenetic mechanisms underlying genomic imprinting in plants. Annu Rev Plant Biol. 2012;63:331–52.

    PubMed  Google Scholar 

  111. Jahnke S, Scholten S. Epigenetic resetting of a gene imprinted in plant embryos. Curr Biol. 2009;19(19):1677–81.

    CAS  PubMed  Google Scholar 

  112. Jiang H, Kohler C. Evolution, function, and regulation of genomic imprinting in plant seed development. J Exp Bot. 2012;63(13):4713–22.

    CAS  PubMed  Google Scholar 

  113. 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.

    PubMed Central  CAS  PubMed  Google Scholar 

  114. Raissig MT, Bemer M, Baroux C, Grossniklaus U. Genomic imprinting in the Arabidopsis embryo is partly regulated by PRC2. PLoS Genet. 2013;9(12):e1003862.

    PubMed Central  PubMed  Google Scholar 

  115. Kohler C, Weinhofer-Molisch I. Mechanisms and evolution of genomic imprinting in plants. Heredity. 2010;105(1):57–63.

    CAS  PubMed  Google Scholar 

  116. 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.

    PubMed Central  CAS  PubMed  Google Scholar 

  117. Belmonte MF, Kirkbride RC, Stone SL, Pelletier JM, Bui AQ, Yeung EC, et al. Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc Natl Acad Sci U S A. 2013;110(5):E435–44.

    Google Scholar 

  118. Zhang H, Chaudhury A, Wu X. Imprinting in plants and its underlying mechanisms. J Genet Genomics. 2013;40(5):239–47.

    CAS  PubMed  Google Scholar 

  119. Costa LM, Yuan J, Rouster J, Paul W, Dickinson H, Gutierrez-Marcos JF. Maternal control of nutrient allocation in plant seeds by genomic imprinting. Curr Biol. 2012;22(2):160–5.

    CAS  PubMed  Google Scholar 

  120. Berger F, Vu TM, Li J, Chen B. Hypothesis: selection of imprinted genes is driven by silencing deleterious gene activity in somatic tissues. Cold Spring Harb Symp Quant Biol. 2012;77:23–9.

    CAS  PubMed  Google Scholar 

  121. Ikeda Y, Kobayashi Y, Yamaguchi A, Abe M, Araki T. Molecular basis of late-flowering phenotype caused by dominant epi-alleles of the FWA locus in Arabidopsis. Plant Cell Physiol. 2007;48(2):205–20.

    CAS  PubMed  Google Scholar 

  122. Borges F, Martienssen RA. Establishing epigenetic variation during genome reprogramming. RNA Biol. 2013;10(4):490–4.

    PubMed Central  CAS  PubMed  Google Scholar 

  123. Dunoyer P, Brosnan CA, Schott G, Wang Y, Jay F, Alioua A, et al. An endogenous, systemic RNAi pathway in plants. EMBO J. 2010;29(10):1699–712.

    PubMed Central  CAS  PubMed  Google Scholar 

  124. Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science. 2010;328(5980):872–5.

    CAS  PubMed  Google Scholar 

  125. Dunoyer P, Schott G, Himber C, Meyer D, Takeda A, Carrington JC, et al. Small RNA duplexes function as mobile silencing signals between plant cells. Science. 2010;328(5980):912–6.

    CAS  PubMed  Google Scholar 

  126. Molinier J, Ries G, Zipfel C, Hohn B. Transgeneration memory of stress in plants. Nature. 2006;442(7106):1046–9.

    CAS  PubMed  Google Scholar 

  127. 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.

    PubMed Central  CAS  PubMed  Google Scholar 

  128. Christensen CA, King EJ, Jordan JR, Drews GN. Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sex Plant Reprod. 1997;10:49–64.

    Google Scholar 

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Authors and Affiliations

  1. Instituto Gulbenkian de Ciencia, Rua da Quinta Grande 6, 2780–156, Oeiras, Portugal

    Dr. Leonor C. Boavida, Marcela Hernandez-Coronado & Dr. Jörg D. Becker

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  1. Dr. Leonor C. Boavida
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  2. Marcela Hernandez-Coronado
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  3. Dr. Jörg D. Becker
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Correspondence to Jörg D. Becker .

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  1. Shanghai Center for Plant Stress Biology (PSC), Shanghai, China

    Olga Pontes

  2. Plant Pathology and Microbiology, University of California, Riverside, California, USA

    Hailing Jin

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Boavida, L., Hernandez-Coronado, M., Becker, J. (2015). Setting the Stage for the Next Generation: Epigenetic Reprogramming During Sexual Plant Reproduction. In: Pontes, O., Jin, H. (eds) Nuclear Functions in Plant Transcription, Signaling and Development. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-2386-1_6

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