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Epigenetic reprogramming in plant sexual reproduction

Key Points

  • 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.

Abstract

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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Figure 1: Sexual reproduction in Arabidopsis thaliana.
Figure 2: Epigenetic reprogramming during male gametogenesis.
Figure 3: Epigenetic reprogramming during embryogenesis.

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Acknowledgements

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.

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Correspondence to Frédéric Berger.

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Glossary

Epigenetic marks

Modifications of the chromatin that are inherited through cell division.

Spores

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.

Gametophytes

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.

Endosperm

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.

Meiocyte

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.

Argonaute

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.

Epialleles

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

Sporophyte

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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