Crosstalk between H2A variant-specific modifications impacts vital cell functions.

Selection of C-terminal motifs participated in evolution of distinct histone H2A variants. Hybrid types of variants combining motifs from distinct H2A classes are extremely rare. This suggests that the proximity between the motif cases interferes with their function. We studied this question in flow...

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Main Authors: Anna Schmücker, Bingkun Lei, Zdravko J Lorković, Matías Capella, Sigurd Braun, Pierre Bourguet, Olivier Mathieu, Karl Mechtler, Frédéric Berger
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-06-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1009601
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author Anna Schmücker
Bingkun Lei
Zdravko J Lorković
Matías Capella
Sigurd Braun
Pierre Bourguet
Olivier Mathieu
Karl Mechtler
Frédéric Berger
author_facet Anna Schmücker
Bingkun Lei
Zdravko J Lorković
Matías Capella
Sigurd Braun
Pierre Bourguet
Olivier Mathieu
Karl Mechtler
Frédéric Berger
author_sort Anna Schmücker
collection DOAJ
description Selection of C-terminal motifs participated in evolution of distinct histone H2A variants. Hybrid types of variants combining motifs from distinct H2A classes are extremely rare. This suggests that the proximity between the motif cases interferes with their function. We studied this question in flowering plants that evolved sporadically a hybrid H2A variant combining the SQ motif of H2A.X that participates in the DNA damage response with the KSPK motif of H2A.W that stabilizes heterochromatin. Our inventory of PTMs of H2A.W variants showed that in vivo the cell cycle-dependent kinase CDKA phosphorylates the KSPK motif of H2A.W but only in absence of an SQ motif. Phosphomimicry of KSPK prevented DNA damage response by the SQ motif of the hybrid H2A.W/X variant. In a synthetic yeast expressing the hybrid H2A.W/X variant, phosphorylation of KSPK prevented binding of the BRCT-domain protein Mdb1 to phosphorylated SQ and impaired response to DNA damage. Our findings illustrate that PTMs mediate interference between the function of H2A variant specific C-terminal motifs. Such interference could explain the mutual exclusion of motifs that led to evolution of H2A variants.
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publishDate 2021-06-01
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spelling doaj-art-4bb13fccf7bd4709836d091ade8013c82025-08-20T02:33:43ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042021-06-01176e100960110.1371/journal.pgen.1009601Crosstalk between H2A variant-specific modifications impacts vital cell functions.Anna SchmückerBingkun LeiZdravko J LorkovićMatías CapellaSigurd BraunPierre BourguetOlivier MathieuKarl MechtlerFrédéric BergerSelection of C-terminal motifs participated in evolution of distinct histone H2A variants. Hybrid types of variants combining motifs from distinct H2A classes are extremely rare. This suggests that the proximity between the motif cases interferes with their function. We studied this question in flowering plants that evolved sporadically a hybrid H2A variant combining the SQ motif of H2A.X that participates in the DNA damage response with the KSPK motif of H2A.W that stabilizes heterochromatin. Our inventory of PTMs of H2A.W variants showed that in vivo the cell cycle-dependent kinase CDKA phosphorylates the KSPK motif of H2A.W but only in absence of an SQ motif. Phosphomimicry of KSPK prevented DNA damage response by the SQ motif of the hybrid H2A.W/X variant. In a synthetic yeast expressing the hybrid H2A.W/X variant, phosphorylation of KSPK prevented binding of the BRCT-domain protein Mdb1 to phosphorylated SQ and impaired response to DNA damage. Our findings illustrate that PTMs mediate interference between the function of H2A variant specific C-terminal motifs. Such interference could explain the mutual exclusion of motifs that led to evolution of H2A variants.https://doi.org/10.1371/journal.pgen.1009601
spellingShingle Anna Schmücker
Bingkun Lei
Zdravko J Lorković
Matías Capella
Sigurd Braun
Pierre Bourguet
Olivier Mathieu
Karl Mechtler
Frédéric Berger
Crosstalk between H2A variant-specific modifications impacts vital cell functions.
PLoS Genetics
title Crosstalk between H2A variant-specific modifications impacts vital cell functions.
title_full Crosstalk between H2A variant-specific modifications impacts vital cell functions.
title_fullStr Crosstalk between H2A variant-specific modifications impacts vital cell functions.
title_full_unstemmed Crosstalk between H2A variant-specific modifications impacts vital cell functions.
title_short Crosstalk between H2A variant-specific modifications impacts vital cell functions.
title_sort crosstalk between h2a variant specific modifications impacts vital cell functions
url https://doi.org/10.1371/journal.pgen.1009601
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