Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants

She, Wenjing; Grimanelli, Daniel; Rutowicz, Kinga; Whitehead, Marek W. J.; Puzio, Marcin; Kotliński, Maciej; Jerzmanowski, Andrzej; Baroux, Célia

doi:10.1242/dev.095034

Cited by 158 publications

(229 citation statements)

References 105 publications

(122 reference statements)

Supporting

Mentioning

206

Contrasting

Unclassified

Order By: Relevance

“…Formation and maintenance of condensed heterochromatin states most notably involve high levels of DNA cytosine methylation, histone posttranslational modifications such as dimethylation of histone H3 at lysine 9 (H3K9me2), the regulation of linker histone H1 density, and the replacement of canonical histones by histone variants, such as H2A.W (23)(24)(25)(26). Notwithstanding these observations, the mechanisms dynamically controlling spatial chromatin rearrangements and their functional impact on nuclear activity, and in particular on gene expression during development or in response to external cues, are only poorly understood in plants and other systems (reviewed in refs.…”

Section: Significancementioning

confidence: 99%

Light signaling controls nuclear architecture reorganization during seedling establishment

Bourbousse

Mestiri

Zabulon

et al. 2015

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

108

View full text Add to dashboard Cite

The spatial organization of chromatin can be subject to extensive remodeling in plant somatic cells in response to developmental and environmental signals. However, the mechanisms controlling these dynamic changes and their functional impact on nuclear activity are poorly understood. Here, we determined that light perception triggers a switch between two different nuclear architectural schemes during Arabidopsis postembryonic development. Whereas progressive nucleus expansion and heterochromatin rearrangements in cotyledon cells are achieved similarly under light and dark conditions during germination, the later steps that lead to mature nuclear phenotypes are intimately associated with the photomorphogenic transition in an organ-specific manner. The light signaling integrators DE-ETIOLATED 1 and CONSTITUTIVE PHOTOMORPHOGENIC 1 maintain heterochromatin in a decondensed state in etiolated cotyledons. In contrast, under light conditions cryptochrome-mediated photoperception releases nuclear expansion and heterochromatin compaction within conspicuous chromocenters. For all tested loci, chromatin condensation during photomorphogenesis does not detectably rely on DNA methylation-based processes. Notwithstanding, the efficiency of transcriptional gene silencing may be impacted during the transition, as based on the reactivation of transposable element-driven reporter genes. Finally, we report that global engagement of RNA polymerase II in transcription is highly increased under light conditions, suggesting that cotyledon photomorphogenesis involves a transition from globally quiescent to more active transcriptional states. Given these findings, we propose that light-triggered changes in nuclear architecture underlie interplays between heterochromatin reorganization and transcriptional reprogramming associated with the establishment of photosynthesis. plant development | photomorphogenesis | light signaling | nuclear organization | heterochromatin C hromatin allows dense packaging of chromosomal DNA into a small and constrained nuclear space. It also serves as a structural framework for regulatory processes that control the functional status of genome domains with variable sizes, notably by dynamically influencing the subnuclear partitioning of generich and repeat-rich domains within euchromatic and heterochromatic regions, respectively (reviewed in refs. 1-3). These chromatin-based processes impact plasticity in the regulation of nuclear programs during both vegetative and reproductive phases of the plant life cycle (recently reviewed in refs. 4-8). In many cases, such events combine local chromatin variations with prominent changes in nuclear architecture and higher-order chromatin organization.Spatial chromatin organization is well exemplified by the extreme cases of transcriptionally silent chromocenters that contain the majority of ribosomal DNA repeats, such as the (peri)centromeric domains of mice and several plant species that include transposable elements (TE) and non-TE repeated sequences (9,

show abstract

Section: Significancementioning

confidence: 99%

Light signaling controls nuclear architecture reorganization during seedling establishment

Bourbousse

Mestiri

Zabulon

et al. 2015

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

108

View full text Add to dashboard Cite

show abstract

“…While there are some reports proposing a tissue-specific distribution of these marks in plants (Costa and Shaw, 2006;Caro et al, 2007), the majority of studies have focused on germ cells (Hsieh et al, 2009;Slotkin et al, 2009;She et al, 2013). Currently, little is known about how different epigenetic marks influence tissue-specific gene expression patterns in sporophytic tissues.…”

mentioning

confidence: 99%

HISTONE DEACETYLASE6 Controls Gene Expression Patterning and DNA Methylation-Independent Euchromatic Silencing

et al. 2015

View full text Add to dashboard Cite

To investigate the role of chromatin regulators in patterning gene expression, we employed a unique epigenetically controlled and highly tissue-specific green fluorescent protein reporter line in Arabidopsis (Arabidopsis thaliana). Using a combination of forward and reverse genetic approaches on this line, we show here that distinct epigenetic regulators are involved in silencing the transgene in different tissues. The forward genetic screen led to the identification of a novel HISTONE DEACETYLASE6 (HDA6) mutant allele (epigenetic control1, hda6-8). This allele differs from the previously reported alleles, as it did not affect DNA methylation and only had a very modest effect on the release of transposable elements and other heterochromatic transcripts. Overall, our data shows that HDA6 has at least two clearly separable activities in different genomic regions. In addition, we present an unexpected role for HDA6 in the control of DNA methylation at CG dinucleotides.

show abstract

“…1). The female meiosis also occurs normally in the sdg2-1 mutant, albeit reduced H3K4me3 in megaspore mother cells (She et al, 2013). It seems that Arabidopsis meiosis is rather tolerant to H3K4me3 reduction.…”

Section: Discussionmentioning

confidence: 96%

“…In wild-type Arabidopsis, as compared to surrounding somatic cells, both megaspore and microspore mother cells display more decondensed chromatin with higher levels of H3K4me2 and H3K4me3 (She et al, 2013;She and Baroux, 2015). The MALE MEIOCYTE DEATH1 (MMD1, also known as DUET) gene encodes a PHDfinger protein essential for male meiosis (Reddy et al, 2003;Yang et al, 2003).…”

Section: Discussionmentioning

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.

View full text Add to dashboard Cite

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.

show abstract

Chromatin reprogramming during the somatic-to-reproductive cell fate transition in plants

Cited by 158 publications

References 105 publications

Light signaling controls nuclear architecture reorganization during seedling establishment

Light signaling controls nuclear architecture reorganization during seedling establishment

HISTONE DEACETYLASE6 Controls Gene Expression Patterning and DNA Methylation-Independent Euchromatic Silencing

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

Contact Info

Product

Resources

About