Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin

Borg, Michael; Jacob, Yannick; Susaki, Daichi; LeBlanc, Chantal; Buendía, Daniel; Axelsson, Elin; Kawashima, Tomokazu; Voigt, Philipp; Boavida, Leonor C.; Becker, Jörg; Higashiyama, Tetsuya; Martienssen, Robert A.; Berger, Frédéric

doi:10.1038/s41556-020-0515-y

Cited by 156 publications

(123 citation statements)

References 97 publications

(124 reference statements)

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“…There is accumulating evidence for the active role of histone demethylases in resetting H3K27me3 at specific loci during sexual reproduction (Crevillén et al, 2014;Noh et al, 2004) and for a global depletion of H3K27me3 during spermatogenesis (Borg et al, 2020). While the precise mechanism(s) governing this phenomenon remain poorly understood, our finding that the failure to reset H3K27me3 during sexual reproduction resulted in its trans-generational inheritance in euchromatin, even when functional demethylase activity was restored, might suggest that some of the H3K27me3 imprints that are ectopically deposited in histone demethylase mutants cannot be reset if they are distal to the target sequences recognized by the demethylases.…”

Section: Discussionmentioning

confidence: 99%

A new role for histone demethylases in the maintenance of plant genome integrity

Antunez-Sanchez

Naish

Ramirez-Prado

et al. 2020

eLife

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Histone modifications deposited by the Polycomb repressive complex 2 (PRC2) play a critical role in the control of growth, development, and adaptation to environmental fluctuations of most multicellular eukaryotes. The catalytic activity of PRC2 is counteracted by Jumonji-type (JMJ) histone demethylases, which shapes the genomic distribution of H3K27me3. Here, we show that two JMJ histone demethylases in Arabidopsis, EARLY FLOWERING 6 (ELF6) and RELATIVE OF EARLY FLOWERING 6 (REF6), play distinct roles in H3K27me3 and H3K27me1 homeostasis. We show that failure to reset these chromatin marks during sexual reproduction results in the transgenerational inheritance of histone marks, which cause a loss of DNA methylation at heterochromatic loci and transposon activation. Thus, Jumonji-type histone demethylases play a dual role in plants by helping to maintain transcriptional states through development and safeguard genome integrity during sexual reproduction.

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Section: Discussionmentioning

confidence: 99%

A new role for histone demethylases in the maintenance of plant genome integrity

Antunez-Sanchez

Naish

Ramirez-Prado

et al. 2020

eLife

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“…Similar to the MMC, HTR13 is absent in mature Arabidopsis female and male germ cells [ 17 , 22 ], suggesting that HTR13 turnover is indeed necessary to establish germline identity. Limited global availability of H3.1 replicative histones might be associated with the specific cell cycle regulation of reproductive cells, as suggested for the egg cell where no or low signal for all H3.1 genes was detected [ 17 ].…”

Section: Discussionmentioning

confidence: 99%

H3.1 Eviction Marks Female Germline Precursors in Arabidopsis

Hernandez-Lagana

Autran

2020

Plants

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In flowering plants, germline precursors are differentiated from somatic cells. The female germline precursor of Arabidopsis thaliana is located in the internal (nucellar) tissue of the ovule, and is known as the Megaspore Mother Cell (MMC). MMC differentiation in Arabidopsis occurs when a cell in the subepidermal layer of the nucellar apex enters the meiotic program. Increasing evidence has demonstrated that MMC specification is a plastic process where the number and developmental outcome of MMCs are variable. During its differentiation, the MMC displays specific chromatin hallmarks that distinguish it from other cells within the primordium. To date, these signatures have been only analyzed at developmental stages where the MMC is morphologically conspicuous, and their role in reproductive fate acquisition remains to be elucidated. Here, we show that the histone 3 variant H3.1 HISTONE THREE RELATED 13 (HTR13) can be evicted in multiple subepidermal cells of the nucellus, but that H3.1 eviction persists only in the MMC. This pattern is established very early in ovule development and is reminiscent of the specific eviction of H3.1 that marks cell cycle exit in other somatic cell types, such as the root quiescent center (QC) of Arabidopsis. Our findings suggest that cell cycle progression in the subepidermal region of the ovule apex is modified very early in development and is associated with plasticity of reproductive fate acquisition.

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“…PCR amplification was performed using the primers listed in S2 Data. Expression profiles of H2B genes in rice, tomato and maize were extracted from Genevestigator data [49].RNA-seq data from various Arabidopsis tissues was analysed and described previously [19].…”

Section: Expression Analysismentioning

confidence: 99%

The evolution and functional divergence of the histone H2B family in plants

et al. 2020

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Chromatin regulation of eukaryotic genomes depends on the formation of nucleosome complexes between histone proteins and DNA. Histone variants, which are diversified by sequence or expression pattern, can profoundly alter chromatin properties. While variants in histone H2A and H3 families are well characterized, the extent of diversification of histone H2B proteins is less understood. Here, we report a systematic analysis of the histone H2B family in plants, which have undergone substantial divergence during the evolution of each major group in the plant kingdom. By characterising Arabidopsis H2Bs, we substantiate this diversification and reveal potential functional specialization that parallels the phylogenetic structure of emergent clades in eudicots. In addition, we identify a new class of highly divergent H2B variants, H2B.S, that specifically accumulate during chromatin compaction of dry seed embryos in multiple species of flowering plants. Our findings thus identify unsuspected diverse properties among histone H2B proteins in plants that has manifested into potentially novel groups of histone variants.

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Targeted reprogramming of H3K27me3 resets epigenetic memory in plant paternal chromatin

Cited by 156 publications

References 97 publications

A new role for histone demethylases in the maintenance of plant genome integrity

A new role for histone demethylases in the maintenance of plant genome integrity

H3.1 Eviction Marks Female Germline Precursors in Arabidopsis

The evolution and functional divergence of the histone H2B family in plants

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