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DEMETER-mediated DNA Demethylation in Gamete Companion Cells and the Endosperm, and its Possible Role in Embryo Development in Arabidopsis

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Abstract

Seed development begins upon double fertilization, producing the embryo and endosperm, which are genetically identical, except for their ploidy level. DEMETER (DME), a member of the DNA glycosylase family, functions as a DNA demethylase via the base excision repair pathway. DME is specifically expressed prior to fertilization in two gamete companion cells, central cell of the female gametophyte and vegetative cell of the male gametophyte, but not in the heritable gamete cells or embryo. Mutations in the DME gene cause hypermethylation in the endosperm, leading to endosperm overproliferation and seed abortion after fertilization. DME-mediated DNA demethylation preferentially targets euchromatic transposable elements (TEs), resulting in TE activation and initiation of de novo methylation through RNA-directed DNA methylation, and provides FERTILIZATION-INDEPENDENT SEED 2 (FIS2)-Polycomb Repressive Complex 2-binding sites, resulting in histone modifications and genomic imprinting during reproduction. The global demethylation of TEs in gamete companion cells and active de novo methylation in the embryo suggest a new role of sexual companion cells in reinforcing the genome integrity of the heritable tissue. In this review, we provide an overview of demethylation in sexual companion cells and the endosperm, and discuss its evolutionary effect on the heritable gamete cells and embryo.

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References

  • Ashapkin VV, Kutueva LI, Aleksandrushkina NI, Vanyushin BF (2019) Epigenetic regulation of plant gametophyte development. Int J Mol Sci 20(12):3051

    Article  CAS  PubMed Central  Google Scholar 

  • Batista RA, Figueiredo DD, Santos-Gonzalez J, Kohler C (2019) Auxin regulates endosperm cellularization in Arabidopsis. Genes Dev 33(7–8):466–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borges F, Gomes G, Gardner R, Moreno N, McCormick S, Feijo JA, Becker JD (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 148(2):1168–1181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borges F, Parent JS, van Ex F, Wolff P, Martinez G, Kohler C, Martienssen RA (2018) Transposon-derived small RNAs triggered by miR845 mediate genome dosage response in Arabidopsis. Nat Genet 50(2):186–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calarco JP, Borges F, Donoghue MT, Van Ex F, Jullien PE, Lopes T, Gardner R, Berger F, Feijo JA, Becker JD, Martienssen RA (2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151(1):194–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi Y, Gehring M, Johnson L, Hannon M, Harada JJ, Goldberg RB, Jacobsen SE, Fischer RL (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110(1):33–42

    Article  CAS  PubMed  Google Scholar 

  • Clark SJ, Smallwood SA, Lee HJ, Krueger F, Reik W, Kelsey G (2017) Genome-wide base-resolution mapping of DNA methylation in single cells using single-cell bisulfite sequencing(scBS-seq). Nat Protoc 12(3):534-U159

    Article  CAS  Google Scholar 

  • de Felippes FF, Ott F, Weigel D (2011) Comparative analysis of non-autonomous effects of tasiRNAs and miRNAs in Arabidopsis thaliana. Nucleic Acids Res 39(7):2880–2889

    Article  PubMed  CAS  Google Scholar 

  • de Mendoza A, Lister R, Bogdanovic O (2019) Evolution of DNA methylome diversity in eukaryotes. J Mol Biol 432(6):1687–1705

    Article  CAS  Google Scholar 

  • Deniz O, Frost JM, Branco MR (2019) Regulation of transposable elements by DNA modifications. Nat Rev Genet 20(7):417–431

    Article  CAS  PubMed  Google Scholar 

  • Dunoyer P, Melnyk C, Molnar A, Slotkin RK (2013) Plant Mobile Small RNAs. CSH Perspect Biol 5(7):a017897

    Google Scholar 

  • Erdmann RM, Hoffmann A, Walter HK, Wagenknecht HA, Gross-Hardt R, Gehring M (2017) Molecular movement in the Arabidopsis thaliana female gametophyte. Plant Reprod 30(3):141–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frost JM, Kim MY, Park GT, Hsieh PH, Nakamura M, Lin SJH, Yoo H, Choi J, Ikeda Y, Kinoshita T, Choi Y, Zilberman D, Fischer RL (2018) FACT complex is required for DNA demethylation at heterochromatin during reproduction in Arabidopsis. Proc Natl Acad Sci USA 115(20):E4720–E4729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gehring M, Huh JH, Hsieh TF, Penterman J, Choi Y, Harada JJ, Goldberg RB, Fischer RL (2006) DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124(3):495–506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gehring M, Bubb KL, Henikoff S (2009) Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324(5933):1447–1451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gehring M, Missirian V, Henikoff S (2011) Genomic analysis of parent-of-origin allelic expression in Arabidopsis thaliana seeds. PLoS One 6(8):e23687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo JU, Su YJ, Shin JH, Shin JH, Li HD, Xie B, Zhong C, Hu SH, Le T, Fan GP, Zhu H, Chang Q, Gao Y, Ming GL, Song HJ (2014) Distribution, recognition and regulation of non-CpG methylation in the adult mammalian brain. Nat Neurosci 17(2):215–222

    Article  CAS  PubMed  Google Scholar 

  • Han Q, Bartels A, Cheng X, Meyer A, An YC, Hsieh TF, Xiao W (2019) Epigenetics regulates reproductive development in plants. Plants (Basel) 8(12):564

    Article  CAS  Google Scholar 

  • Hehenberger E, Kradolfer D, Kohler C (2012) Endosperm cellularization defines an important developmental transition for embryo development. Development 139(11):2031–2039

    Article  CAS  PubMed  Google Scholar 

  • Hsieh TF, Ibarra CA, Silva P, Zemach A, Eshed-Williams L, Fischer RL, Zilberman D (2009) Genome-wide demethylation of Arabidopsis endosperm. Science 324(5933):1451–1454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsieh TF, Shin J, Uzawa R, Silva P, Cohen S, Bauer MJ, Hashimoto M, Kirkbride RC, Harada JJ, Zilberman D, Fischer RL (2011) Regulation of imprinted gene expression in Arabidopsis endosperm. Proc Natl Acad Sci USA 108(5):1755–1762

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ibarra CA, Feng X, Schoft VK, Hsieh TF, Uzawa R, Rodrigues JA, Zemach A, Chumak N, Machlicova A, Nishimura T, Rojas D, Fischer RL, Tamaru H, Zilberman D (2012) Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337(6100):1360–1364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ingouff M, Rademacher S, Holec S, Soljic L, Xin N, Readshaw A, Foo SH, Lahouze B, Sprunck S, Berger F (2010) Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr Biol 20(23):2137–2143

    Article  CAS  PubMed  Google Scholar 

  • Jackson JP, Lindroth AM, Cao XF, Jacobsen SE (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416(6880):556–560

    Article  CAS  PubMed  Google Scholar 

  • Jiang FW, Feng ZH, Liu HL, Zhu J (2015) Involvement of plant stem cells or stem cell-like cells in dedifferentiation. Front Plant Sci 6:1028

    PubMed  PubMed Central  Google Scholar 

  • Jullien PE, Mosquna A, Ingouff M, Sakata T, Ohad N, Berger F (2008) Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biol 6(8):e194

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jullien PE, Susaki D, Yelagandula R, Higashiyama T, Berger F (2012) DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr Biol 22(19):1825–1830

    Article  CAS  PubMed  Google Scholar 

  • Kehr J, Kragler F (2018) Long distance RNA movement. New Phytol 218(1):29–40

    Article  CAS  PubMed  Google Scholar 

  • Kim MY, Ono A, Scholten S, Kinoshita T, Zilberman D, Okamoto T, Fischer RL (2019) DNA demethylation by ROS1a in rice vegetative cells promotes methylation in sperm. Proc Natl Acad Sci USA 116(19):9652–9657

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kinoshita T, Yadegari R, Harada JJ, Goldberg RB, Fischer RL (1999) Imprinting of the MEDEA polycomb gene in the Arabidopsis endosperm. Plant Cell 11(10):1945–1952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kinoshita H, Shi Y, Sandefur C, Meisner LF, Chang CS, Choon A, Reznikoff CR, Bova GS, Friedl A, Jarrard DF (2000) Methylation of the androgen receptor minimal promoter silences transcription in human prostate cancer. Cancer Res 60(13):3623–3630

    CAS  PubMed  Google Scholar 

  • Kinoshita T, Miura A, Choi Y, Kinoshita Y, Cao X, Jacobsen SE, Fischer RL, Kakutani T (2004) One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303(5657):521–523. https://doi.org/10.1126/science.1089835

    Article  CAS  PubMed  Google Scholar 

  • Kohler C, Hennig L, Spillane C, Pien S, Gruissem W, Grossniklaus U (2003) The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes Dev 17:1540–1553

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kohler C, Page DR, Gagliardini V, Grossniklaus U (2005) The Arabidopsis thaliana MEDEA Polycomb group protein controls expression of PHERES1 by parental imprinting. Nat Genet 37(1):28–30

    Article  PubMed  CAS  Google Scholar 

  • Lafon-Placette C, Kohler C (2014) Embryo and endosperm, partners in seed development. Curr Opin Plant Biol 17:64–69

    Article  PubMed  Google Scholar 

  • Lafon-Placette C, Kohler C (2016) Endosperm-based postzygotic hybridization barriers: developmental mechanisms and evolutionary drivers. Mol Ecol 25(11):2620–2629

    Article  PubMed  Google Scholar 

  • Laurent L, Wong E, Li G, Huynh T, Tsirigos A, Ong CT, Low HM, Sung KWK, Rigoutsos I, Loring J, Wei CL (2010) Dynamic changes in the human methylome during differentiation. Genome Res 20(3):320–331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin JY, Le BH, Chen M, Henry KF, Hur J, Hsieh TF, Chen PY, Pelletier JM, Pellegrini M, Fischer RL, Harada JJ, Goldberg RB (2017) Similarity between soybean and Arabidopsis seed methylomes and loss of non-CG methylation does not affect seed development. P Natl Acad Sci USA 114(45):E9730–E9739

    Article  CAS  Google Scholar 

  • Lister R, Mukamel EA, Nery JR, Urich M, Puddifoot CA, Johnson ND, Lucero J, Huang Y, Dwork AJ, Schultz MD, Yu M, Tonti-Filippini J, Heyn H, Hu SJ, Wu JC, Rao A, Esteller M, He C, Haghighi FG, Sejnowski TJ, Behrens MM, Ecker JR (2013) Global epigenomic reconfiguration during mammalian brain development. Science 341(6146):629

    Article  CAS  Google Scholar 

  • Makarevich G, Villar CB, Erilova A, Kohler C (2008) Mechanism of PHERES1 imprinting in Arabidopsis. J Cell Sci 121(Pt 6):906–912

    Article  CAS  PubMed  Google Scholar 

  • Malagnac F, Bartee L, Bender J (2002) An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J 21:6842–6852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez G, Panda K, Kohler C, Slotkin RK (2016) Silencing in sperm cells is directed by RNA movement from the surrounding nurse cell. Nat Plants 2(4):1–8

    Article  CAS  Google Scholar 

  • Martinez G, Wolff P, Wang ZX, Moreno-Romero J, Santos-Gonzalez J, Conze LL, DeFraia C, Slotkin RK, Kohler C (2018) Paternal easiRNAs regulate parental genome dosage in Arabidopsis. Nat Genet 50(2):193

    Article  CAS  PubMed  Google Scholar 

  • Miki D, Zhang WX, Zeng WJ, Feng ZY, Zhu JK (2018) CRISPR/Cas9-mediated gene targeting in Arabidopsis using sequential transformation. Nat Commun 9:1967

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Moreno-Romero J, Jiang H, Santos-Gonzalez J, Kohler C (2016) Parental epigenetic asymmetry of PRC2-mediated histone modifications in the Arabidopsis endosperm. EMBO J 35(12):1298–1311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreno-Romero J, Del Toro-De Leon G, Yadav VK, Santos-Gonzalez J, Köhler C (2019) Epigenetic signatures associated with imprinted paternally expressed genes in the Arabidopsis endosperm. Genome Biol 20:41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palovaara J, Saiga S, Wendrich JR, Hofland NV, van Schayck JP, Hater F, Mutte S, Sjollema J, Boekschoten M, Hooiveld GJ, Weijers D (2017) Transcriptome dynamics revealed by a gene expression atlas of the early Arabidopsis embryo. Nat Plants 3(11):894–904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park K, Frost JM, Adair AJ, Kim DM, Yun H, Brooks JS, Fischer RL, Choi Y (2016a) Optimized methods for the isolation of Arabidopsis female central cells and their nuclei. Mol Cells 39(10):768–775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park K, Kim MY, Vickers M, Park JS, Hyun Y, Okamoto T, Zilberman D, Fischer RL, Feng X, Choi Y, Scholten S (2016b) DNA demethylation is initiated in the central cells of Arabidopsis and rice. Proc Natl Acad Sci USA 113(52):15138–15143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park JS, Frost JM, Park K, Ohr H, Park GT, Kim S, Eom H, Lee I, Brooks JS, Fischer RL, Choi Y (2017) Control of DEMETER DNA demethylase gene transcription in male and female gamete companion cells in Arabidopsis thaliana. Proc Natl Acad Sci USA 114(8):2078–2083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patil V, Ward RL, Hesson LB (2014) The evidence for functional non-CpG methylation in mammalian cells. Epigenetics 9(6):823–828

    Article  PubMed  PubMed Central  Google Scholar 

  • Pillot M, Baroux C, Vazquez MA, Autran D, Leblanc O, Vielle-Calzada JP, Grossniklaus U, Grimanelli D (2010) Embryo and endosperm inherit distinct chromatin and transcriptional states from the female gametes in Arabidopsis. Plant Cell 22(2):307–320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shirane K, Toh H, Kobayashi H, Miura F, Chiba H, Ito T, Kono T, Sasaki H (2013) Mouse oocyte methylomes at base resolution reveal genome-wide accumulation of non-CpG methylation and role of DNA methyltransferases. Plos Genet 9(4):e1003439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shulse CN, Cole BJ, Ciobanu D, Lin JY, Yoshinaga Y, Gouran M, Turco GM, Zhu YW, O’Malley RC, Brady SM, Dickel DE (2019) High-throughput single-cell transcriptome profiling of plant cell types. Cell Rep 27(7):2241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slotkin RK, Vaughn M, Borges F, Tanurdzic M, Becker JD, Feijo JA, Martienssen RA (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136(3):461–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stroud H, Do T, Du J, Zhong X, Feng S, Johnson L, Patel DJ, Jacobsen SE (2014) Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nat Struct Mol Biol 21(1):64–72

    Article  CAS  PubMed  Google Scholar 

  • Tsukahara S, Kobayashi A, Kawabe A, Mathieu O, Miura A, Kakutani T (2009) Bursts of retrotransposition reproduced in Arabidopsis. Nature 461(7262):423–426

    Article  CAS  PubMed  Google Scholar 

  • Villar CBR, Erilova A, Makarevich G, Trosch R, Kohler C (2009) Control of PHERES1 imprinting in Arabidopsis by direct tandem repeats. Mol Plant 2(4):654–660

    Article  CAS  PubMed  Google Scholar 

  • Yelagandula R, Stroud H, Holec S, Zhou K, Feng S, Zhong X, Muthurajan UM, Nie X, Kawashima T, Groth M, Luger K, Jacobsen SE, Berger F (2014) The histone variant H2A.W defines heterochromatin and promotes chromatin condensation in Arabidopsis. Cell 158(1):98–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu B, Dong X, Gravina S, Kartal O, Schimmel T, Cohen J, Tortoriello D, Zody R, Hawkins RD, Vijg J (2017) Genome-wide, single-cell DNA methylomics reveals increased non-CpG methylation during human oocyte maturation. Stem Cell Rep 9(1):397–407

    Article  CAS  Google Scholar 

  • Zemach A, Zilberman D (2010) Evolution of eukaryotic DNA methylation and the pursuit of safer sex. Curr Biol 20(17):R780–R785

    Article  CAS  PubMed  Google Scholar 

  • Zemach A, McDaniel IE, Silva P, Zilberman D (2010) Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328(5980):916–919

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Lang Z, Zhu JK (2018a) Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol 19(8):489–506

    Article  CAS  PubMed  Google Scholar 

  • Zhang SS, Wang DF, Zhang HJ, Skaggs MI, Lloyd A, Ran D, An LL, Schumaker KS, Drews GN, Yadegari R (2018b) FERTILIZATION-INDEPENDENT SEED-polycomb repressive complex 2 plays a dual role in regulating type I MADS-Box genes in early endosperm development. Plant Physiol 177(1):285–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang CQ, Hung YH, Rim HJ, Zhang DP, Frost JM, Shin H, Jang HS, Liu F, Xiao WY, Iyer LM, Aravind L, Zhang XQ, Fischer RL, Huh JH, Hsieh TF (2019) The catalytic core of DEMETER guides active DNA demethylation in Arabidopsis. Proc Natl Acad Sci USA 116(35):17563–17571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2009) Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet 43:143–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The work was supported by the National Research Foundation (NRF) of Korea (2020R1A2C2009382) and the Next Generation BioGreen 21 Program Grant (PJ013127).

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  1. Department of Biological Sciences, Seoul National University, Seoul, 08826, South Korea

    Kyunghyuk Park, Seunga Lee, Hyunjin Yoo & Yeonhee Choi

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  1. Kyunghyuk Park
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  2. Seunga Lee
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KP conceived and designed the review paper, and wrote the first draft; SL designed the review paper and added a new idea; HY collected the relevant literature; YC critically evaluated the manuscript.

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Correspondence to Yeonhee Choi.

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Park, K., Lee, S., Yoo, H. et al. DEMETER-mediated DNA Demethylation in Gamete Companion Cells and the Endosperm, and its Possible Role in Embryo Development in Arabidopsis. J. Plant Biol. 63, 321–329 (2020). https://doi.org/10.1007/s12374-020-09258-2

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