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

Ingouff, Mathieu; Selles, Benjamin; Michaud, Caroline; Vu, Thiet Minh; Berger, Frédéric; Schorn, Andrea; Autran, Daphné; Durme, Matthias Van; Nowack, Moritz K.; Martienssen, Robert A.; Grimanelli, Daniel

doi:10.1101/gad.289397.116

Cited by 98 publications

(86 citation statements)

References 68 publications

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“…The targets of these processes are unknown and the epigenetic state of the MMC has not been profiled at molecular resolution. Recently, fusions between DNA methylation‐binding proteins and fluorescent reporters allowed visualization of methylation dynamics at a broad scale (Ingouff et al ., ). CG methylation remains steady but CHH methylation decreases transiently and is then restored during MMC specification.…”

Section: Meiosismentioning

confidence: 97%

“…Tansley insight New Phytologist fluorescent reporters allowed visualization of methylation dynamics at a broad scale (Ingouff et al, 2017). CG methylation remains steady but CHH methylation decreases transiently and is then restored during MMC specification.…”

Section: Reviewmentioning

confidence: 99%

“…As part of a recurring theme, AGO5 acts in a cell nonautonomous manner to promote the mitotic division of the functional megaspore (Tucker et al, 2012). Fluorescent reporters suggest that CG and CHH methylation remain fairly steady throughout female gametogenesis (Ingouff et al, 2017). The mature female gametophyte contains two gametes, a haploid egg cell and a diploid central cell.…”

Section: Female Gametogenesismentioning

confidence: 99%

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Epigenetic dynamics during flowering plant reproduction: evidence for reprogramming?

Gehring

2019

New Phytologist

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Summary Over the last 10 yr there have been major advances in documenting and understanding dynamic changes to DNA methylation, small RNAs, chromatin modifications and chromatin structure that accompany reproductive development in flowering plants, from germline specification to seed maturation. Here I highlight recent advances in the field, mostly made possible by microscopic analysis of epigenetic states or by the ability to isolate specific cell types or tissues and apply omics approaches. I consider in which contexts there is potentially reprogramming vs maintenance or reinforcement of epigenetic states.

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Section: Meiosismentioning

confidence: 97%

Section: Reviewmentioning

confidence: 99%

Section: Female Gametogenesismentioning

confidence: 99%

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Epigenetic dynamics during flowering plant reproduction: evidence for reprogramming?

Gehring

2019

New Phytologist

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“…All primers sequences are shown in Supplemental Table 1 (Ingouff et al, 2017) and pUBQ (Mehlmer et al, 2012) promoters respectively. The eGFP was cloned into the pK7WG2 (Karimi et al, 2002(Karimi et al, , 2005.…”

Section: Multisite Gateway Cloning Of Entry Clonesmentioning

confidence: 99%

Visualizing protein-protein interactions in plants by rapamycin-dependent delocalization

Winkler

Mylle

Meyer

et al. 2020

Preprint

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One-sentence summary: rapamycin-dependent delocalization allows quantifying proteinprotein interactions inside plant cells. Author contributions: DVD initiated the project and designed experiments. JW, EM, ADM and PG designed and performed experiments. BP wrote the script for quantification of the data. JM performed experiments. JW, PG and DVD wrote the paper. AbstractIdentifying protein-protein interactions (PPI) is crucial to understand any type of biological process. Many PPI tools are available, yet only some function within the context of a plant cell.Narrowing down even further, only few PPI tools allow visualizing higher order interactions.Here, we present a novel and conditional in vivo PPI tool for plant research. Knocksideways in plants (KSP) uses the ability of rapamycin to alter the localization of a bait protein and its interactors via the heterodimerization of FKBP and FRB domains. KSP is inherently free from many limitations, which other PPI systems hold. It is an in vivo tool, it is flexible concerning the orientation of protein tagging as long as this does not interfere with the interaction and it is compatible with a broad range of fluorophores. KSP is also a conditional tool and therefore does not require additional controls. The interactions can be quantified and in high throughput by the scripts that we provide. Finally, we demonstrate that KSP can visualize higher-order interactions. It is therefore a versatile tool, complementing the PPI methods field with unique characteristics and applications.

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“…In mammals, an erasure of almost all DNA methylation states is observed before fertilization (Feng et al, 2010). In plants, however, such an extreme reprogramming event does not seem to occur at fertilization (Ingouff et al, 2017;Saze et al, 2003;Jullien et al, 2012;Calarco et al, 2012). Moreover, over 85% of mammalian histones are replaced by sperm-specific protamine proteins, enabling extensive compaction of DNA in male gametes, and upon fertilization the paternal chromatin is deprived of the protamines and loaded with variant histone H3.3 provided by the female gametes (Ooi and Henikoff, 2007;Saitou and Kurimoto, 2014).…”

mentioning

confidence: 99%

SDG2-Mediated H3K4me3 Is Crucial for Chromatin Condensation and Mitotic Division during Male Gametogenesis in Arabidopsis

Pinon

Yao

et al. 2017

Plant Physiol.

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Epigenetic reprogramming occurring during reproduction is crucial for both animal and plant development. Histone H3 Lys 4 trimethylation (H3K4me3) is an evolutionarily conserved epigenetic mark of transcriptional active euchromatin. While much has been learned in somatic cells, H3K4me3 deposition and function in gametophyte is poorly studied. Here, we demonstrate that SET DOMAIN GROUP2 (SDG2)-mediated H3K4me3 deposition participates in epigenetic reprogramming during Arabidopsis male gametogenesis. We show that loss of SDG2 barely affects meiosis and cell fate establishment of haploid cells. However, we found that SDG2 is critical for postmeiotic microspore development. Mitotic cell division progression is partly impaired in the loss-of-function sdg2-1 mutant, particularly at the second mitosis setting up the two sperm cells. We demonstrate that SDG2 is involved in promoting chromatin decondensation in the pollen vegetative nucleus, likely through its role in H3K4me3 deposition, which prevents ectopic heterochromatic H3K9me2 speckle formation. Moreover, we found that derepression of the LTR retrotransposon ATLANTYS1 is compromised in the vegetative cell of the sdg2-1 mutant pollen. Consistent with chromatin condensation and compromised transcription activity, pollen germination and pollen tube elongation, representing the key function of the vegetative cell in transporting sperm cells during fertilization, are inhibited in the sdg2-1 mutant. Taken together, we conclude that SDG2-mediated H3K4me3 is an essential epigenetic mark of the gametophyte chromatin landscape, playing critical roles in gamete mitotic cell cycle progression and pollen vegetative cell function during male gametogenesis and beyond.

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

Cited by 98 publications

References 68 publications

Epigenetic dynamics during flowering plant reproduction: evidence for reprogramming?

Epigenetic dynamics during flowering plant reproduction: evidence for reprogramming?

Visualizing protein-protein interactions in plants by rapamycin-dependent delocalization

SDG2-Mediated H3K4me3 Is Crucial for Chromatin Condensation and Mitotic Division during Male Gametogenesis in Arabidopsis

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