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DNA methylation is a major epigenetic mark involved in the silencing of genes and transposable elements (TEs). DNA methylation varies significantly across the plant life cycle, but is efficiently reinforced during reproduction, ensuring stable silencing of TEs. Plants are remarkably flexible in their mode of reproduction and numerous species, including crops, can propagate asexually, skipping one or more of these critical reinforcement steps. In this review, we summarize recent advances in the characterization of DNA methylation inheritance in sexual and asexual plants. We argue that because most epigenetic reinforcement appears to occur during seed formation, methylomes of asexual seeds should resemble that of their sexual counterparts. Conversely, clonally propagated plants are expected to be hypomethylated and undergo frequent stochastic epigenetic changes. Last, we provide insights on how the use of nonmodel organisms will advance our understanding of epigenetic inheritance in plants.

Introduction

DNA methylation is a major epigenetic mark found in higher eukaryotes, including plants and mammals, that is involved in the silencing of genes and transposable elements (TEs). Heritable changes of DNA methylation, known as epialleles, can have phenotypic impacts, opening the interesting possibility that epialleles may underlie at least part of the phenotypic diversity observed in natural plant population [1]. Although very rare in mammals, phenotypically relevant epiallelic variation has been recurrently observed in plants, likely because DNA methylation is not fully reset across generations [2]. In turn, plants undergo a DNA methylation reinforcement during sexual reproduction, a mechanism that plays an important role in the correction of accidental epigenetic defects. Although sexual reproduction is predominant in model plant species, such as Arabidopsis, rice, maize, and tomato, transitions to asexual reproduction have occurred multiple times during the diversification of flowering plants [3]. Indeed, several major crops, such as potato, citrus, strawberry, and grape vine, typically propagate asexually, providing unique opportunities to investigate how distinct reproductive strategies shape the extent and mode of epigenetic inheritance. In this review, we will summarize recent advances in the characterization of the mechanisms controlling DNA methylation dynamics in sexual and asexual organisms, as well as propose plausible dynamics in asexually propagated species. Last, we provide insights on how the use of nonmodel organisms has the potential to significantly advance our understanding of epigenetic inheritance in plants.

Section snippetsEstablishment and maintenance of DNA methylation

Plant DNA methylation can occur in any possible sequence context: CG, CHG, and CHH (where H is any nucleotide but G), which are faithfully maintained across cell divisions by the activity of context-specific DNA methyltransferases. In the model plant Arabidopsis thaliana, methylation at the symmetrical CG sites is maintained by the DNA methyltransferase 1 (MET1) during DNA replication. Indeed, symmetric CG methylation is lost during DNA replication but rapidly restored in late S/G2 phase [4].

DNA methylation dynamics during plant growth

DNA methylation can vary significantly between some tissues and developmental stages. For instance, Arabidopsis roots are globally hypomethylated compared with shoots [11]. Notably, cell-type-specific methylome analysis of Arabidopsis roots shows specific CHH hypermethylation in columella root cap cells, likely due to enhanced production of 24-nt siRNAs in this tissue [12]. More recently, transcriptome and methylome analysis of shoot apical meristem (SAM) revealed upregulation of genes encoding

DNA methylation reinforcement during sexual reproduction

In angiosperms, female and male sexual lineages are initiated through meiotic division of the diploid megaspore mother cell (MMC) and microspore mother cell (MiMC), respectively [15]. In Arabidopsis, these two types of mother cells have low CHH methylation levels 14, 16, which in the case of MiMC affects pericentromeric TEs preferentially. Nonetheless, few TEs become hypermethylated in MiMCs and this hypermethylation was shown to be directed by siRNAs produced in surrounding Nourse cells

Asexual reproduction through apomixis

Plants are remarkably diverse in their mode of reproduction, ranging from the archetypal sexual reproduction, to many different flavors of asexual propagation (i.e. lack meiosis and fertilization). In particular, some plants may produce so-called apomictic seeds by a modified sexual cycle in which the MMC (diplospory apomixis), a surrounding cell (apospory apomixis), or a nucellar cell (adventitious apomixis), skips meiosis and double fertilization (reviewed in [30]).

Despite their similar

Clonal propagation

Vegetative propagation is an extreme case of asexual reproduction. Unlike apomixis, the parental organs that give rise to the vegetative offspring are somatic [38], initiated from meristems of differentiated and specialized organs. The lack of sexual reproduction and embryogenesis is expected to affect the stability of DNA methylation. Nonetheless, it is reasonable to speculate that some degree of DNA methylation reinforcement may take place during vegetative propagation, as SAM stem cells have

Conclusions

How DNA methylation is maintained across generations has been a major focus of research for the last two decades, yielding an impressive level of detail of the dynamics and mechanisms involved. Despite these advances, very little is known about how asexual reproduction shapes DNA methylation memory in plants. Here, we reviewed recent findings obtained using model plant species, particularly Arabidopsis, rice, and maize, to propose plausible DNA methylation dynamics in asexually propagated

Conflict of interest statement

Nothing declared.

Acknowledgements

We thank members of the Quadrana laboratory for discussion. This work was supported by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (Grant agreement No. 948674) and Agence National de la Recherche (ANR epiTOM).

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