Silencing in sperm cells is directed by RNA movement from the surrounding nurse cell

Martínez, Gabriel García; Panda, Kaushik; Köhler, Claudia; Slotkin, R. Keith

doi:10.1038/nplants.2016.30

Cited by 197 publications

(156 citation statements)

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“…While there could have been maternal contributions to heterotic phenotypes observed in our study, these effects cannot account for the variation in heterotic phenotypes seen between the 19 different epiHybrid lines, as the maternal parental line was invariant. It is plausible, nonetheless, that paternal effects could have contributed to between-cross variation in hybrid performance, for example via the cytoplasmic transmission of differential small RNAs in the pollen (Martínez et al, 2016). However, these paternally inherited effects, if they occurred, cannot explain the epigenetic QTL associations detected in our study.…”

Section: Discussionmentioning

confidence: 69%

Parental DNA Methylation States Are Associated with Heterosis in Epigenetic Hybrids

et al. 2017

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Despite the importance and wide exploitation of heterosis in commercial crop breeding, the molecular mechanisms behind this phenomenon are not completely understood. Recent studies have implicated changes in DNA methylation and small RNAs in hybrid performance; however, it remains unclear whether epigenetic changes are a cause or a consequence of heterosis. Here, we analyze a large panel of over 500 Arabidopsis (Arabidopsis thaliana) epigenetic hybrid plants (epiHybrids), which we derived from near-isogenic but epigenetically divergent parents. This proof-of-principle experimental system allowed us to quantify the contribution of parental methylation differences to heterosis. We measured traits such as leaf area, growth rate, flowering time, main stem branching, rosette branching, and final plant height and observed several strong positive and negative heterotic phenotypes among the epiHybrids. Using an epigenetic quantitative trait locus mapping approach, we were able to identify specific differentially methylated regions in the parental genomes that are associated with hybrid performance. Sequencing of methylomes, transcriptomes, and genomes of selected parent-epiHybrid combinations further showed that these parental differentially methylated regions most likely mediate the remodeling of methylation and transcriptional states at specific loci in the hybrids. Taken together, our data suggest that locus-specific epigenetic divergence between the parental lines can directly or indirectly trigger heterosis in Arabidopsis hybrids independent of genetic changes. These results add to a growing body of evidence that points to epigenetic factors as one of the key determinants of hybrid performance.

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Section: Discussionmentioning

confidence: 69%

Parental DNA Methylation States Are Associated with Heterosis in Epigenetic Hybrids

et al. 2017

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“…One possibility is that RNA Pol II substitutes for Pol IV as a source of small RNAs to induce DRM-dependent methylation (Matzke et al 2015;Cuerda-Gil and Slotkin 2016), acting either cell-autonomously or non-cell-autonomously. Such Pol IV-independent small RNAs could originate from surrounding cells of the maternal sporophyte or accessory cells of the female gametophyte and be transported to the egg cell, as shown between accessory cells and target sperm cells (Martinez et al 2016). Alternatively, as yet unknown actors might be required, and identifying components of such a pathway will be of major interest.…”

Section: Discussionmentioning

confidence: 99%

Live-cell analysis of DNA methylation during sexual reproduction in Arabidopsis reveals context and sex-specific dynamics controlled by noncanonical RdDM

et al. 2017

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Cytosine methylation is a key epigenetic mark in many organisms, important for both transcriptional control and genome integrity. While relatively stable during somatic growth, DNA methylation is reprogrammed genome-wide during mammalian reproduction. Reprogramming is essential for zygotic totipotency and to prevent transgenerational inheritance of epimutations. However, the extent of DNA methylation reprogramming in plants remains unclear. Here, we developed sensors reporting with single-cell resolution CG and non-CG methylation in Arabidopsis. Live imaging during reproduction revealed distinct and sex-specific dynamics for both contexts. We found that CHH methylation in the egg cell depends on DOMAINS REARRANGED METHYLASE 2 (DRM2) and RNA polymerase V (Pol V), two main actors of RNA-directed DNA methylation, but does not depend on Pol IV. Our sensors provide insight into global DNA methylation dynamics at the single-cell level with high temporal resolution and offer a powerful tool to track CG and non-CG methylation both during development and in response to environmental cues in all organisms with methylated DNA, as we illustrate in mouse embryonic stem cells.

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“…Demethylated companion cells do not pass on their genome to the next generation; therefore, the genomic instability resulting from transposon transcription is not deleterious to the species as a whole. Rather, there is evidence to suggest that the RdDM pathway then promotes corresponding TE methylation in the egg and sperm cells, respectively (3,11,12). In this way, the companion cell acts sacrificially, reinforcing and protecting the genomic integrity of egg and sperm, which will be inherited by the next generation.…”

Section: Discussionmentioning

confidence: 99%

“…DME-mediated DNA demethylation in companion cells is preferentially targeted to small, AT-rich, and nucleosome-depleted euchromatic transposable elements (TEs) (3). Evidence suggests that TE hypomethylation in the companion cells promotes transcription of mobile siRNA at the TEs, mediating RNA-directed DNA methylation (RdDM) in the gametes, so that the same TE sequences become hypermethylated, safeguarding the genomic integrity of the gametes (3,11,12). The large overlap between sites demethylated in the central cell, inferred from hypomethylated sites in the maternal endosperm genome (13) and sites demethylated in the vegetative cell, despite their different cell fates, provides evidence toward this common basal function of DME expression in gamete companion cells.…”

Section: Significancementioning

confidence: 99%

Control of DEMETER DNA demethylase gene transcription in male and female gamete companion cells inArabidopsis thaliana

Park

Frost

Park

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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The DEMETER (DME) DNA glycosylase initiates active DNA demethylation via the base-excision repair pathway and is vital for reproduction in Arabidopsis thaliana. DME-mediated DNA demethylation is preferentially targeted to small, AT-rich, and nucleosome-depleted euchromatic transposable elements, influencing expression of adjacent genes and leading to imprinting in the endosperm. In the female gametophyte, DME expression and subsequent genome-wide DNA demethylation are confined to the companion cell of the egg, the central cell. Here, we show that, in the male gametophyte, DME expression is limited to the companion cell of sperm, the vegetative cell, and to a narrow window of time: immediately after separation of the companion cell lineage from the germline. We define transcriptional regulatory elements of DME using reporter genes, showing that a small region, which surprisingly lies within the DME gene, controls its expression in male and female companion cells. DME expression from this minimal promoter is sufficient to rescue seed abortion and the aberrant DNA methylome associated with the null dme-2 mutation. Within this minimal promoter, we found short, conserved enhancer sequences necessary for the transcriptional activities of DME and combined predicted binding motifs with published transcription factor binding coordinates to produce a list of candidate upstream pathway members in the genetic circuitry controlling DNA demethylation in gamete companion cells. These data show how DNA demethylation is regulated to facilitate endosperm gene imprinting and potential transgenerational epigenetic regulation, without subjecting the germline to potentially deleterious transposable element demethylation.S exual reproduction is characterized by fertilization of an egg by a sperm cell, generating the embryo. Uniquely in angiosperms, a second sperm cell fertilizes the companion cell of the egg, the central cell, to generate the endosperm, which supports development of the embryo. During reproduction in angiosperm Arabidopsis thaliana, the DEMETER (DME) DNA glycosylase exhibits a striking expression pattern. Within the ovule, the female gametophyte is generated by mitosis of the haploid megaspore, forming a mature gametophyte of seven cells. During this process, the egg and central cell lineages are separated, and, at this point, DME expression and DNA demethylation is initiated solely in the central cell (1, 2). DME expression is switched off after fertilization (2). This precise pattern of expression initiated in the central cell, and not in the egg cell, is responsible for hypomethylation specifically in the maternal endosperm genome and not in the maternal embryo genome (3). DME expression in the central cell is essential for plant reproduction and genomic imprinting, whereby its absence results in loss of genomic imprinting, aberrant endosperm development, and early seed abortion (2, 4, 5).In the male gametophyte, indirect evidence suggests that DME is expressed during development of the mature three-cell pollen gra...

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Silencing in sperm cells is directed by RNA movement from the surrounding nurse cell

Cited by 197 publications

References 50 publications

Parental DNA Methylation States Are Associated with Heterosis in Epigenetic Hybrids

Parental DNA Methylation States Are Associated with Heterosis in Epigenetic Hybrids

Live-cell analysis of DNA methylation during sexual reproduction in Arabidopsis reveals context and sex-specific dynamics controlled by noncanonical RdDM

Control of DEMETER DNA demethylase gene transcription in male and female gamete companion cells inArabidopsis thaliana

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