H2A Variants in Arabidopsis: Versatile Regulators of Genome Activity

Lei, Bingkun; Berger, Frédéric

doi:10.1016/j.xplc.2019.100015

Cited by 55 publications

(41 citation statements)

References 153 publications

(159 reference statements)

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“…9 It has been proposed that the diversification of histone variants that accompanies evolution of multicellular eukaryotes enabled more complex modes of regulation of these chromatin activities. [1][2][3]5,6 Neofunctionalization of histone variants from the H2A family is marked by the acquisition of specific amino acid motifs in their C-terminal tails as well as occupation of very defined chromatin states. 5,6 For example, variants H2A.W in plants and macroH2A in animals are associated with transcriptional repression.…”

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“…[1][2][3]5,6 Neofunctionalization of histone variants from the H2A family is marked by the acquisition of specific amino acid motifs in their C-terminal tails as well as occupation of very defined chromatin states. 5,6 For example, variants H2A.W in plants and macroH2A in animals are associated with transcriptional repression. 4,10 The mechanisms responsible for segregation of macroH2A and H2A.W to heterochromatin are unknown.…”

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A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W

et al. 2021

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A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W

et al. 2021

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“…Both lines showed significant enrichments of H2A.Z throughout the LUC gene bodies, while there were almost no H2A.Z signals in the corresponding regions in the WT genome (Figure 3d and e). Although H2A.Z is a marker histone for the promoter region, it also appears in the gene bodies of genes with low expression (Lashgari et al, 2017; Gómez-Zambrano, Merini and Calonje, 2019; Lei and Frederic, 2020). In addition, mC and H3K36me3 were reportedly deposited within a gene body in a transcription-coupled manner (Teissandier and Bourc’his, 2017), which would be undetectable in the low-expressed genes (Cermakova et al, 2019).…”

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De novoactivated transcription of inserted foreign coding sequences is inheritable in the plant genome

Hata

Takada

Hayakawa

et al. 2020

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The manner in which newborn genes become transcriptionally activated and fixed in the plant genome is poorly understood. To examine such processes of gene evolution, we performed an artificial evolutionary experiment in Arabidopsis thaliana. As a model of gene-birth events, we introduced a promoterless coding sequence of the firefly luciferase (LUC) gene and established 386 T2-generation transgenic lines. Among them, we determined the individual LUC insertion loci in 76 lines and found that one-third of them were transcribed de novo even in the intergenic or inherently unexpressed regions. In the transcribed lines, transcription-related epigenetic marks were detected across the newly activated transcribed regions. These results agreed with our previous findings in A. thaliana cultured cells under a similar experimental scheme. The comparison of the results of the T2-plant and cultured cell experiments revealed that the de novo-activated transcription caused by local chromatin remodelling was inheritable. During one-generation inheritance, it seems likely that the transcription activities of the LUC inserts trapped by the endogenous genes/transcripts became stronger, while those of de novo transcription in the intergenic/untranscribed regions became weaker. These findings may offer a clue for the elucidation of the mechanism via which newborn genes become transcriptionally activated and fixed in the plant genome.

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“…Distinct C-terminal motifs present in specific classes of H2A variants do not usually cooccur. The KSPK is present exclusively in plant H2A.W and mammalian macroH2A, while the SQ[E/D]Φ motif is present primarily on H2A.X variants in eukaryotes [5,9,33,35]. There are notable exceptions to this rule in animals and plants.…”

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Crosstalk between H2A variant-specific modifications impacts vital cell functions

Schmuecker

Lei

Lorković

et al. 2021

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Histone variants are distinguished by specific substitutions and motifs that might be subject to post-translational modifications (PTMs). Compared with the high conservation of H3 variants, the N- and C-terminal tails of H2A variants are more divergent and are potential substrates for a more complex array of PTMs, which have remained largely unexplored. We used mass spectrometry to inventory the PTMs of the two heterochromatin-enriched variants H2A.W.6 and H2A.W.7 of Arabidopsis, which harbor the C-terminal motif KSPK. This motif is also found in macroH2A variants in animals and confers specific properties to the nucleosome. We showed that H2A.W.6 is phosphorylated by the cell cycle-dependent kinase CDKA specifically at KSPK. In contrast, this modification is absent on H2A.W.7, which also harbors the SQ motif associated with the variant H2A.X. Phosphorylation of the SQ motif is critical for the DNA damage response but is suppressed in H2A.W.7 by phosphorylation of KSPK. To identify factors involved in this suppression mechanism, we performed a synthetic screen in fission yeast expressing a mimic of the Arabidopsis H2A.W.7. Among those factors was the BRCT-domain protein Mdb1. We showed that phosphorylation of KSPK prevents binding of the BRCT-domain protein Mdb1 to phosphorylated SQ and as a result hampers response to DNA damage. Hence, cross-talks between motif-specific PTMs interfere with the vital functions of H2A variants. Such interference could be responsible for the mutual exclusion of specific motifs between distinct H2A variants. We conclude that sequence innovations in H2A variants have potentiated the acquisition of many specific PTMs with still unknown functions. These add a layer of complexity to the nucleosome properties and their impact in chromatin regulation.

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H2A Variants in Arabidopsis: Versatile Regulators of Genome Activity

Cited by 55 publications

References 153 publications

A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W

A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W

De novoactivated transcription of inserted foreign coding sequences is inheritable in the plant genome

Crosstalk between H2A variant-specific modifications impacts vital cell functions

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