Recent evidence has accumulated to support the partial reprogramming of epigenetic marks in plants.
Both male and female gametogenesis is marked by a loss of DNA methylation.
Companion cells that are associated with gametes undergo marked reprogramming events, which lead to DNA demethylation and activation of transposable elements, as well as activation of flanking genes in the pollen vegetative cell and possibly in the female central cell.
DNA methylation is acquired de novo during embryogenesis, which restores methylation to the levels of somatic adult tissues.
Histone variant replacement is likely to reprogramme chromatin modification in the zygote in plants and animals.
Reprogramming accompanies zygotic genome activation immediately after fertilization in plants.
Epigenetic reprogramming consists of global changes in DNA methylation and histone modifications. In mammals, epigenetic reprogramming is primarily associated with sexual reproduction and occurs during both gametogenesis and early embryonic development. Such reprogramming is crucial not only to maintain genomic integrity through silencing transposable elements but also to reset the silenced status of imprinted genes. In plants, observations of stable transgenerational inheritance of epialleles have argued against reprogramming. However, emerging evidence supports that epigenetic reprogramming indeed occurs during sexual reproduction in plants and that it has a major role in maintaining genome integrity and a potential contribution to epiallelic variation.
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Hathaway, N. A. et al. Dynamics and memory of heterochromatin in living cells. Cell 149, 1447–1460 (2012).
Law, J. A. & Jacobsen, S. E. Dynamic DNA methylation. Science 323, 1568–1569 (2009).
Sharif, J. & Koseki, H. Recruitment of Dnmt1 roles of the SRA protein Np95 (Uhrf1) and other factors. Prog. Mol. Biol. Transl. Sci. 101, 289–310 (2011).
Greer, E. L. & Shi, Y. Histone methylation: a dynamic mark in health, disease and inheritance. Nature Rev. Genet. 13, 343–357 (2012).
Martin, C. & Zhang, Y. Mechanisms of epigenetic inheritance. Curr. Opin. Cell Biol. 19, 266–272 (2007).
Hajkova, P. Epigenetic reprogramming in the germline: towards the ground state of the epigenome. Phil. Trans. R. Soc. B. 366, 2266–2273 (2011).
Kota, S. K. & Feil, R. Epigenetic transitions in germ cell development and meiosis. Dev. Cell 19, 675–686 (2010).
Berger, F. & Twell, D. Germline specification and function in plants. Annu. Rev. Plant Biol. 62, 461–484 (2011).
Chen, C. et al. Meiosis-specific gene discovery in plants: RNA-seq applied to isolated Arabidopsis male meiocytes. BMC Plant Biol. 10, 280 (2010).
Crismani, W., Girard, C. & Mercier, R. Tinkering with meiosis. J. Exp. Bot. 64, 55–65 (2013).
Brownfield, L. & Kohler, C. Unreduced gamete formation in plants: mechanisms and prospects. J. Exp. Bot. 62, 1659–1668 (2011).
Twell, D. Male gametogenesis and germline specification in flowering plants. Sex. Plant Reprod. 24, 149–160 (2011).
Palovaara, J., Saiga, S. & Weijers, D. Transcriptomics approaches in the early Arabidopsis embryo. Trends Plant Sci. 18, 514–521 (2013).
Li, J. & Berger, F. Endosperm: food for humankind and fodder for scientific discoveries. New Phytol. 195, 290–305 (2012).
Drews, G. N. & Koltunow, A. M. The female gametophyte. Arabidopsis Book 9, e0155 (2011).
Leitch, H. G., Tang, W. W. & Surani, M. A. Primordial germ-cell development and epigenetic reprogramming in mammals. Curr. Top. Dev. Biol. 104, 149–187 (2013).
Seisenberger, S. et al. Reprogramming DNA methylation in the mammalian life cycle: building and breaking epigenetic barriers. Phil. Trans. R. Soc. B 368, 20110330 (2013).
Cantone, I. & Fisher, A. G. Epigenetic programming and reprogramming during development. Nature Struct. Mol. Biol. 20, 282–289 (2013).
Chedin, F. The DNMT3 family of mammalian de novo DNA methyltransferases. Prog. Mol. Biol. Transl. Sci. 101, 255–285 (2011).
Smallwood, S. A. & Kelsey, G. De novo DNA methylation: a germ cell perspective. Trends Genet. 28, 33–42 (2012).
Cubas, P., Vincent, C. & Coen, E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401, 157–161 (1999).
Hauser, M. T., Aufsatz, W., Jonak, C. & Luschnig, C. Transgenerational epigenetic inheritance in plants. Biochim. Biophys. 1809, 459–468 (2011).
Saze, H., Mittelsten Scheid, O. & Paszkowski, J. Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nature Genet. 34, 65–69 (2003).
Gehring, M. et al. DEMETER DNA glycosylase establishes MEDEA Polycomb gene self-imprinting by allele-specific demethylation. Cell 124, 495–506 (2006).
Gong, Z. et al. ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase. Cell 111, 803–814 (2002).
Castel, S. E. & Martienssen, R. A. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nature Rev. Genet. 14, 100–112 (2013).
Haag, J. R. & Pikaard, C. S. Multisubunit RNA polymerases IV and V: purveyors of non-coding RNA for plant gene silencing. Nature Rev. Mol. Cell. Biol. 12, 483–492 (2011).
Law, J. A. & Jacobsen, S. E. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nature Rev. Genet. 11, 204–220 (2010).
Stroud, H. et al. Non-CG methylation patterns shape the epigenetic landscape in Arabidopsis. Nature Struct. Mol. Biol. 21, 64–72 (2014). This paper provides a comprehensive account of all DNA methyltransferase activities that are responsible for non-CG methylation in A. thaliana.
Cokus, S. J. et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452, 215–219 (2008).
Zemach, A., McDaniel, I. E., Silva, P. & Zilberman, D. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328, 916–919 (2010).
Finnegan, E. J., Peacock, W. J. & Dennis, E. S. Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc. Natl Acad. Sci. USA 93, 8449–8454 (1996).
Johnson, L. M. et al. The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr. Biol. 17, 379–384 (2007).
Coleman-Derr, D. & Zilberman, D. DNA methylation, H2A.Z, and the regulation of constitutive expression. Cold Spring Harb. Symp. Quant. Biol. 77, 147–154 (2012).
Zemach, A. et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell 153, 193–205 (2013).
Lindroth, A. M. et al. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292, 2077–2080 (2001).
Du, J. et al. Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell 151, 167–180 (2012).
Matzke, M. A. & Mosher, R. A. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nature Rev. Genet. 15, 394–408 (2014).
Law, J. A., Vashisht, A. A., Wohlschlegel, J. A. & Jacobsen, S. E. SHH1, a homeodomain protein required for DNA methylation, as well as RDR2, RDM4, and chromatin remodeling factors, associate with RNA polymerase IV. PLoS Genet. 7, e1002195 (2011).
Zhong, X. et al. Molecular mechanism of action of plant DRM de novo DNA methyltransferases. Cell 157, 1050–1060 (2014).
Brzeski, J. & Jerzmanowski, A. Deficient in DNA methylation 1 (DDM1) defines a novel family of chromatin-remodeling factors. J. Biol. Chem. 278, 823–828 (2003).
Kawashima, T. & Berger, F. Green love talks; cell–cell communication during double fertilization in flowering plants. AoB Plants 2011, plr015 (2011).
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. 65, 503–516 (2011).
Ito, H. et al. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472, 115–119 (2011).
Calarco, J. P. et al. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151, 194–205 (2012). This study provides evidence for dynamic changes of DNA methylation during male gametogenesis in A. thaliana.
Ibarra, C. A. et al. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337, 1360–1364 (2012). This paper shows demethylation in plant gamete companion cells.
Jullien, P. E., Kinoshita, T., Ohad, N. & Berger, F. Maintenance of DNA methylation during the Arabidopsis life cycle is essential for parental imprinting. Plant Cell 18, 1360–1372 (2006).
Jullien, P. E. et al. Retinoblastoma and its binding partner MSI1 control imprinting in Arabidopsis. PLoS Biol. 6, e194 (2008).
Jullien, P. E., Susaki, D., Yelagandula, R., Higashiyama, T. & Berger, F. DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr. Biol. 22, 1825–1830 (2012). This study reports the first evidence for a cycle of DNA methylation reprogramming at specific loci in A. thaliana.
Schoft, V. K. et al. Induction of RNA-directed DNA methylation upon decondensation of constitutive heterochromatin. EMBO Rep. 10, 1015–1021 (2009).
Schoft, V. K. et al. Function of the DEMETER DNA glycosylase in the Arabidopsis thaliana male gametophyte. Proc. Natl Acad. Sci. USA 108, 8042–8047 (2011).
Slotkin, R. K. et al. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136, 461–472 (2009).
Martinez, G. & Slotkin, R. K. Developmental relaxation of transposable element silencing in plants: functional or byproduct? Curr. Opin. Plant Biol. 15, 496–502 (2012).
Lippman, Z. et al. Role of transposable elements in heterochromatin and epigenetic control. Nature 430, 471–476 (2004).
Nuthikattu, S. et al. The initiation of epigenetic silencing of active transposable elements is triggered by RDR6 and 21–22 nucleotide small interfering RNAs. Plant Physiol. 162, 116–131 (2013).
Stroud, H., Greenberg, M. V., Feng, S., Bernatavichute, Y. V. & Jacobsen, S. E. Comprehensive analysis of silencing mutants reveals complex regulation of the Arabidopsis methylome. Cell 152, 352–364 (2013). This is a global analysis of all pathways that control DNA methylation and their interaction with other silencing mechanisms.
Grant-Downton, R., Hafidh, S., Twell, D. & Dickinson, H. G. Small RNA pathways are present and functional in the angiosperm male gametophyte. Mol. Plant 2, 500–512 (2009).
Grant-Downton, R. et al. Artificial microRNAs reveal cell-specific differences in small RNA activity in pollen. Curr. Biol. 23, R599–R601 (2013). This report provides a new insight into the controversy related to the movement of non-coding RNAs in pollen.
Russell, S. D. Ultrastructure of the sperm of plumbago-zeylanica: II. Quantitative cytology and 3-dimensional organization. Planta 162, 385–391 (1984).
McCue, A. D., Cresti, M., Feijo, J. A. & Slotkin, R. K. Cytoplasmic connection of sperm cells to the pollen vegetative cell nucleus: potential roles of the male germ unit revisited. J. Exp. Bot. 62, 1621–1631 (2011).
Kragler, F. Plasmodesmata: intercellular tunnels facilitating transport of macromolecules in plants. Cell Tissue Res. 352, 49–58 (2013).
Kubo, T. et al. Transcriptome analysis of developing ovules in rice isolated by laser microdissection. Plant Cell Physiol. 54, 750–765 (2013).
Schmidt, A. et al. Transcriptome analysis of the Arabidopsis megaspore mother cell uncovers the importance of RNA helicases for plant germline development. PLoS Biol. 9, e1001155 (2011).
She, W. et al. Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants. Development 140, 4008–4019 (2013).
Olmedo-Monfil, V. et al. Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464, 628–632 (2010).
Singh, M. et al. Production of viable gametes without meiosis in maize deficient for an ARGONAUTE protein. Plant Cell 23, 443–458 (2011).
Tucker, M. R. et al. Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in Arabidopsis. Development 139, 1399–1404 (2012).
Borges, F., Pereira, P. A., Slotkin, R. K., Martienssen, R. A. & Becker, J. D. MicroRNA activity in the Arabidopsis male germline. J. Exp. Bot. 62, 1611–1620 (2011).
Mi, S. et al. Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133, 116–127 (2008).
Takeda, A., Iwasaki, S., Watanabe, T., Utsumi, M. & Watanabe, Y. The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol. 49, 493–500 (2008).
Dunoyer, P. et al. Small RNA duplexes function as mobile silencing signals between plant cells. Science 328, 912–916 (2010).
Melnyk, C. W., Molnar, A., Bassett, A. & Baulcombe, D. C. Mobile 24 nt small RNAs direct transcriptional gene silencing in the root meristems of Arabidopsis thaliana. Curr. Biol. 21, 1678–1683 (2011).
Molnar, A. et al. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328, 872–875 (2010).
Bajon, C., Horlow, C., Motamayor, J. C., Sauvanet, A. & Robert, D. Megasporogenesis in Arabidopsis thaliana L.: an ultrastructural study. Sex. Plant Reprod. 12, 99–109 (1999).
Gehring, M. Genomic imprinting: insights from plants. Annu. Rev. Genet. 47, 187–208 (2013).
Gehring, M., Bubb, K. L. & Henikoff, S. Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324, 1447–1451 (2009).
Kinoshita, T. et al. One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303, 521–523 (2004).
Hsieh, T. F. et al. Genome-wide demethylation of Arabidopsis endosperm. Science 324, 1451–1454 (2009).
Ikeda, Y. et al. HMG domain containing SSRP1 is required for DNA demethylation and genomic imprinting in Arabidopsis. Dev. Cell 21, 589–596 (2011).
Choi, Y. et al. DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110, 33–42 (2002).
Ingouff, M., Haseloff, J. & Berger, F. Polycomb group genes control developmental timing of endosperm. Plant J. 42, 663–674 (2005).
Wolff, P. et al. High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis endosperm. PLoS Genet. 7, e1002126 (2011).
Berger, F., Vu, T. M., 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. 77, 23–29 (2012).
Wuest, S. E. et al. Arabidopsis female gametophyte gene expression map reveals similarities between plant and animal gametes. Curr. Biol. 20, 506–512 (2010).
Ishizu, H., Siomi, H. & Siomi, M. C. Biology of PIWI-interacting RNAs: new insights into biogenesis and function inside and outside of germlines. Genes Dev. 26, 2361–2373 (2012).
Aravin, A. et al. A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442, 203–207 (2006).
Houwing, S. et al. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish. Cell 129, 69–82 (2007).
Watanabe, T. et al. Identification and characterization of two novel classes of small RNAs in the mouse germline: retrotransposon-derived siRNAs in oocytes and germline small RNAs in testes. Genes Dev. 20, 1732–1743 (2006).
Belmonte, M. F. et al. Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc. Natl Acad. Sci. USA 110, E435–E444 (2013). This paper presents an 'atlas' of gene expression profiles in the major components of A. thaliana developing seeds, which provides new insights into the gene activity that regulates DNA methylation.
Costa, L. M. et al. Central cell-derived peptides regulate early embryo patterning in flowering plants. Science 344, 168–172 (2014).
Xing, Q. et al. ZHOUPI controls embryonic cuticle formation via a signalling pathway involving the subtilisin protease ABNORMAL LEAF-SHAPE1 and the receptor kinases GASSHO1 and GASSHO2. Development 140, 770–779 (2013).
Rodrigues, J. A. et al. Imprinted expression of genes and small RNA is associated with localized hypomethylation of the maternal genome in rice endosperm. Proc. Natl Acad. Sci. USA 110, 7934–7939 (2013).
Mari-Ordonez, A. et al. Reconstructing de novo silencing of an active plant retrotransposon. Nature Genet. 45, 1029–1039 (2013). This elegant work shows that TEs can mobilize to new loci and create de novo epialleles in A. thaliana , which causes genome diversification and provides a potential source of adaptive traits.
Reinders, J. et al. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 23, 939–950 (2009).
Teixeira, F. K. et al. A role for RNAi in the selective correction of DNA methylation defects. Science 323, 1600–1604 (2009).
Probst, A. V., Dunleavy, E. & Almouzni, G. Epigenetic inheritance during the cell cycle. Nature Rev. Mol. Cell. Biol. 10, 192–206 (2009).
Okano, Y. et al. A Polycomb repressive complex 2 gene regulates apogamy and gives evolutionary insights into early land plant evolution. Proc. Natl Acad. Sci. USA 106, 16321–16326 (2009).
Mosquna, A. et al. Regulation of stem cell maintenance by the Polycomb protein FIE has been conserved during land plant evolution. Development 136, 2433–2444 (2009).
Filipescu, D., Szenker, E. & Almouzni, G. Developmental roles of histone H3 variants and their chaperones. Trends Genet. 29, 630–640 (2013).
Ingouff, M. & Berger, F. Histone3 variants in plants. Chromosoma 119, 27–33 (2010).
Akiyama, T., Suzuki, O., Matsuda, J. & Aoki, F. Dynamic replacement of histone H3 variants reprograms epigenetic marks in early mouse embryos. PLoS Genet. 7, e1002279 (2011).
Banaszynski, L. A., Allis, C. D. & Lewis, P. W. Histone variants in metazoan development. Dev. Cell 19, 662–674 (2010).
Orsi, G. A. et al. Drosophila Yemanuclein and HIRA cooperate for de novo assembly of H3.3-containing nucleosomes in the male pronucleus. PLoS Genet. 9, e1003285 (2013).
Santenard, A. et al. Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3. Nature Cell Biol. 12, 853–862 (2010).
Ingouff, M. et al. Zygotic resetting of the HISTONE 3 variant repertoire participates in epigenetic reprogramming in Arabidopsis. Curr. Biol. 20, 2137–2143 (2010). This paper provides evidence that H3 inherited from chromatin in gametes are removed from the zygotic chromatin by de novo synthesized H3, which suggests reprogramming of chromatin marks after fertilization.
Dalal, Y., Furuyama, T., Vermaak, D. & Henikoff, S. Structure, dynamics, and evolution of centromeric nucleosomes. Proc. Natl Acad. Sci. USA 104, 15974–15981 (2007).
Aw, S. J., Hamamura, Y., Chen, Z., Schnittger, A. & Berger, F. Sperm entry is sufficient to trigger division of the central cell but the paternal genome is required for endosperm development in Arabidopsis. Development 137, 2683–2690 (2010).
Stellfox, M. E., Bailey, A. O. & Foltz, D. R. Putting CENP-A in its place. Cell. Mol. Life Sci. 70, 387–406 (2013).
Olszak, A. M. et al. Heterochromatin boundaries are hotspots for de novo kinetochore formation. Nature Cell Biol. 13, 799–808 (2011).
Zaratiegui, M. et al. RNAi promotes heterochromatic silencing through replication-coupled release of RNA Pol II. Nature 479, 135–138 (2011).
Zaratiegui, M. et al. CENP-B preserves genome integrity at replication forks paused by retrotransposon LTR. Nature 469, 112–115 (2011).
Becker, C. et al. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature 480, 245–249 (2011).
Schmitz, R. J. et al. Transgenerational epigenetic instability is a source of novel methylation variants. Science 334, 369–373 (2011).
Feil, R. & Fraga, M. F. Epigenetics and the environment: emerging patterns and implications. Nature Rev. Genet. 13, 97–109 (2011).
Becker, C. & Weigel, D. Epigenetic variation: origin and transgenerational inheritance. Curr. Opin. Plant Biol. 15, 562–567 (2012).
Woo, H. R., Dittmer, T. A. & Richards, E. J. Three SRA-domain methylcytosine-binding proteins cooperate to maintain global CpG methylation and epigenetic silencing in Arabidopsis. PLoS Genet. 4, e1000156 (2008).
Woo, H. R., Pontes, O., Pikaard, C. S. & Richards, E. J. VIM1, a methylcytosine-binding protein required for centromeric heterochromatinization. Genes Dev. 21, 267–277 (2007).
Jackson, J. P., Lindroth, A. M., Cao, X. & Jacobsen, S. E. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416, 556–560 (2002).
Malagnac, F., Bartee, L. & Bender, J. An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J. 21, 6842–6852 (2002).
Law, J. A. et al. Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature 498, 385–389 (2013).
Tadros, W. & Lipshitz, H. D. The maternal-to-zygotic transition: a play in two acts. Development 136, 3033–3042 (2009).
Kawashima, T. & Goldberg, R. B. The suspensor: not just suspending the embryo. Trends Plant Sci. 15, 23–30 (2010).
Lau, S., Slane, D., Herud, O., Kong, J. & Jurgens, G. Early embryogenesis in flowering plants: setting up the basic body pattern. Annu. Rev. Plant Biol. 63, 483–506 (2012).
Muralla, R., Lloyd, J. & Meinke, D. Molecular foundations of reproductive lethality in Arabidopsis thaliana. PLoS ONE 6, e28398 (2011).
Ingouff, M., Hamamura, Y., Gourgues, M., Higashiyama, T. & Berger, F. Distinct dynamics of HISTONE3 variants between the two fertilization products in plants. Curr. Biol. 17, 1032–1037 (2007).
Meyer, S. & Scholten, S. Equivalent parental contribution to early plant zygotic development. Curr. Biol. 17, 1686–1691 (2007).
Scholten, S., Lorz, H. & Kranz, E. Paternal mRNA and protein synthesis coincides with male chromatin decondensation in maize zygotes. Plant J. 32, 221–231 (2002).
Xin, H. P., Zhao, J. & Sun, M. X. The maternal-to-zygotic transition in higher plants. J. Integr. Plant. Biol. 54, 610–615 (2012).
Autran, D. et al. Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis. Cell 145, 707–719 (2011).
Nodine, M. D. & Bartel, D. P. Maternal and paternal genomes contribute equally to the transcriptome of early plant embryos. Nature 482, 94–97 (2012).
Chen, Z. J. Genomic and epigenetic insights into the molecular bases of heterosis. Nature Rev. Genet. 14, 471–482 (2013).
The authors thank B. H. Le and R. Feil for critical reading of the manuscript. F.B. and T.K. were supported by Temasek Life Sciences Laboratory. They apologize to colleagues whose publications are not cited owing to space limitations.
The authors declare no competing financial interests.
- Epigenetic marks
Modifications of the chromatin that are inherited through cell division.
Haploid cells that are derived from meiosis of meiocytes and that undergo several rounds of mitosis to give rise to gametophytes. The male and female spores are also known as microspores and megaspores, respectively.
Haploid life forms that define the germ line and that are produced by the development of spores. Each gametophyte generally comprises a small number of cells, such as the embryo sac (female gametophyte) and the pollen (male gametophyte) in flowering plants. However, in mosses, the gametophyte constitutes the major part of the life cycle.
The product of the fertilized central cell. It protects the embryo, controls the transfer of nutrients from the mother and, in some species, stores seed nutrient reserves. The role of the endosperm can be compared to that of the placenta in mammals.
- RNA-directed DNA methylation
(RdDM). A plant-specific pathway that regulates de novo DNA methylation in all sequence contexts (CG, CHG and CHH). Small RNAs establish DNA methylation by guiding protein components required for DNA methylation to genomic loci that are homologous to the small RNAs.
The cell differentiated from the somatic cell in a position- dependent manner to undergo meiosis. Male and female meiocytes are also known as pollen mother cells and megaspore mother cells, respectively.
- Asymmetrical division
Cell division that results in two cells with dissimilar morphologies and/or fates.
- Pollen vegetative cell
The male companion cell generated during male gametogenesis. It germinates to give rise to the pollen tube, through which sperm cells are transferred to the female gamete.
- Generative cell
The male germline cell, which undergoes one round of cell division to generate two sperm cells in the vegetative cell.
- Sperm cells
Male gametes produced in the pollen.
- Embryo sac
The female gametophyte that contains four cell types: the egg cell (female gamete), the central cell (female companion cell) and accessory cells (three antipodal cells and two synergid cells).
- Egg cell
The female gamete, which produces the embryo. As the product of the fertilized egg cell reinitiates the plant life cycle, the egg cell can be considered the true female gamete.
- Central cell
The female companion cell generated from female gametogenesis. It is fertilized by the sperm cell to give rise to the endosperm and can be considered the somatic part of the female gametophyte, which reinitiates its development following fertilization.
A family of effector proteins involved in small-RNA-directed gene silencing. Small RNAs bind to Argonaute proteins and guide the complex to their RNA targets.
- Functional unreduced gametes
Gametes produced in the absence of the reduction meiotic division. They are diploid and result in triploid progeny after fertilization.
- Imprinted genes
Genes in which one allele is silenced, whereas the other allele is expressed in a parent-of-origin-specific manner.
Alleles that cause changes in gene expression and that are produced by epigenetic marks (generally DNA methylation in a CG context) but not by mutations in the DNA sequence
The diploid life form in which meiosis takes place to produce the haploid spores.
- Hybrid vigour
A phenomenon that causes the hybrid progeny to differ from the predicted average of the parental traits.
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Kawashima, T., Berger, F. Epigenetic reprogramming in plant sexual reproduction. Nat Rev Genet 15, 613–624 (2014). https://doi.org/10.1038/nrg3685
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