Crosstalk between H2A variant-specific modifications impacts vital cell functions

Autores
Schmücker, Anna; Lei, Bingkun; Lorkovic, Zdravko J.; Capella, Matias; Braun, Sigurd; Bourguet, Pierre; Mathieu, Olivier; Mechtler, Karl; Berger, Frédéric
Año de publicación
2021
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
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.
Fil: Schmücker, Anna. Austrian Academy Of Sciences (oaw);
Fil: Lei, Bingkun. Austrian Academy Of Sciences (oaw);
Fil: Lorkovic, Zdravko J.. Ludwig Maximilians Universitat; Alemania
Fil: Capella, Matias. Ludwig Maximilians Universitat; Alemania. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; Argentina
Fil: Braun, Sigurd. Ludwig Maximilians Universitat; Alemania
Fil: Bourguet, Pierre. Gregor Mendel Institute Of Molecular Plant Biology; Austria. Université Clermont Auvergne; Francia
Fil: Mathieu, Olivier. Université Clermont Auvergne; Francia
Fil: Mechtler, Karl. Gregor Mendel Institute Of Molecular Plant Biology; Austria
Fil: Berger, Frédéric. Gregor Mendel Institute Of Molecular Plant Biology; Austria
Materia
Histone variants
Post-translational modifications
Arabidopsis thaliana
BRCT domain
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/185013
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/185013
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Crosstalk between H2A variant-specific modifications impacts vital cell functionsSchmücker, AnnaLei, BingkunLorkovic, Zdravko J.Capella, MatiasBraun, SigurdBourguet, PierreMathieu, OlivierMechtler, KarlBerger, FrédéricHistone variantsPost-translational modificationsArabidopsis thalianaBRCT domainhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Selection 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.Fil: Schmücker, Anna. Austrian Academy Of Sciences (oaw);Fil: Lei, Bingkun. Austrian Academy Of Sciences (oaw);Fil: Lorkovic, Zdravko J.. Ludwig Maximilians Universitat; AlemaniaFil: Capella, Matias. Ludwig Maximilians Universitat; Alemania. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; ArgentinaFil: Braun, Sigurd. Ludwig Maximilians Universitat; AlemaniaFil: Bourguet, Pierre. Gregor Mendel Institute Of Molecular Plant Biology; Austria. Université Clermont Auvergne; FranciaFil: Mathieu, Olivier. Université Clermont Auvergne; FranciaFil: Mechtler, Karl. Gregor Mendel Institute Of Molecular Plant Biology; AustriaFil: Berger, Frédéric. Gregor Mendel Institute Of Molecular Plant Biology; AustriaPublic Library of Science2021-06info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/185013Schmücker, Anna; Lei, Bingkun; Lorkovic, Zdravko J.; Capella, Matias; Braun, Sigurd; et al.; Crosstalk between H2A variant-specific modifications impacts vital cell functions; Public Library of Science; Plos Genetics; 17; 6; 6-2021; 1-271553-7390CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pgen.1009601info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:47:40Zoai:ri.conicet.gov.ar:11336/185013instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-03 09:47:41.275CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Crosstalk between H2A variant-specific modifications impacts vital cell functions
title Crosstalk between H2A variant-specific modifications impacts vital cell functions
spellingShingle Crosstalk between H2A variant-specific modifications impacts vital cell functions
Schmücker, Anna
Histone variants
Post-translational modifications
Arabidopsis thaliana
BRCT domain
title_short 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_sort Crosstalk between H2A variant-specific modifications impacts vital cell functions
dc.creator.none.fl_str_mv Schmücker, Anna
Lei, Bingkun
Lorkovic, Zdravko J.
Capella, Matias
Braun, Sigurd
Bourguet, Pierre
Mathieu, Olivier
Mechtler, Karl
Berger, Frédéric
author Schmücker, Anna
author_facet Schmücker, Anna
Lei, Bingkun
Lorkovic, Zdravko J.
Capella, Matias
Braun, Sigurd
Bourguet, Pierre
Mathieu, Olivier
Mechtler, Karl
Berger, Frédéric
author_role author
author2 Lei, Bingkun
Lorkovic, Zdravko J.
Capella, Matias
Braun, Sigurd
Bourguet, Pierre
Mathieu, Olivier
Mechtler, Karl
Berger, Frédéric
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Histone variants
Post-translational modifications
Arabidopsis thaliana
BRCT domain
topic Histone variants
Post-translational modifications
Arabidopsis thaliana
BRCT domain
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv 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.
Fil: Schmücker, Anna. Austrian Academy Of Sciences (oaw);
Fil: Lei, Bingkun. Austrian Academy Of Sciences (oaw);
Fil: Lorkovic, Zdravko J.. Ludwig Maximilians Universitat; Alemania
Fil: Capella, Matias. Ludwig Maximilians Universitat; Alemania. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; Argentina
Fil: Braun, Sigurd. Ludwig Maximilians Universitat; Alemania
Fil: Bourguet, Pierre. Gregor Mendel Institute Of Molecular Plant Biology; Austria. Université Clermont Auvergne; Francia
Fil: Mathieu, Olivier. Université Clermont Auvergne; Francia
Fil: Mechtler, Karl. Gregor Mendel Institute Of Molecular Plant Biology; Austria
Fil: Berger, Frédéric. Gregor Mendel Institute Of Molecular Plant Biology; Austria
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.
publishDate 2021
dc.date.none.fl_str_mv 2021-06
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/185013
Schmücker, Anna; Lei, Bingkun; Lorkovic, Zdravko J.; Capella, Matias; Braun, Sigurd; et al.; Crosstalk between H2A variant-specific modifications impacts vital cell functions; Public Library of Science; Plos Genetics; 17; 6; 6-2021; 1-27
1553-7390
CONICET Digital
CONICET
url http://hdl.handle.net/11336/185013
identifier_str_mv Schmücker, Anna; Lei, Bingkun; Lorkovic, Zdravko J.; Capella, Matias; Braun, Sigurd; et al.; Crosstalk between H2A variant-specific modifications impacts vital cell functions; Public Library of Science; Plos Genetics; 17; 6; 6-2021; 1-27
1553-7390
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pgen.1009601
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
_version_ 1842268873577988096
score 13.13397

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