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

Autores
Lei, Bingkun; Capella, Matias; Montgomery, Sean A.; Borg, Michael; Osakabe, Akihisa; Goiser, Malgorzata; Muhammad, Abubakar; Braun, Sigurd; Berger, Frédéric
Año de publicación
2021
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Diversification of histone variants is marked by the acquisition of distinct motifs and functional properties through convergent evolution.1–4 H2A variants are distinguished by specific C-terminal motifs and tend to be segregated within defined domains of the genome.5,6 Whether evolution of these motifs pre-dated the evolution of segregation mechanisms or vice versa has remained unclear. A suitable model to address this question is the variant H2A.W, which evolved in plants through acquisition of a KSPK motif7 and is tightly associated with heterochromatin.4 We used fission yeast, where chromatin is naturally devoid of H2A.W, to study the impact of engineered chimeras combining yeast H2A with the KSPK motif. Biochemical assays showed that the KSPK motif conferred nucleosomes with specific properties. Despite uniform incorporation of the engineered H2A chimeras in the yeast genome, the KSPK motif specifically affected heterochromatin composition and function. We conclude that the KSPK motif promotes chromatin properties in yeast that are comparable to the properties and function of H2A.W in plant heterochromatin. We propose that the selection of functional motifs confer histone variants with properties that impact primarily a specific chromatin state. The association between a new histone variant and a preferred chromatin state can thus provide a setting for the evolution of mechanisms that segregate the new variant to this state, thereby enhancing the impact of the selected properties of the variant on genome activity.
Fil: Lei, Bingkun. Gregor Mendel Institute; Austria
Fil: Capella, Matias. 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: Montgomery, Sean A.. Gregor Mendel Institute; Austria
Fil: Borg, Michael. Gregor Mendel Institute; Austria
Fil: Osakabe, Akihisa. Gregor Mendel Institute; Austria
Fil: Goiser, Malgorzata. Gregor Mendel Institute; Austria
Fil: Muhammad, Abubakar. Universitat Technical Zu Munich; Alemania
Fil: Braun, Sigurd. Universitat Technical Zu Munich; Alemania
Fil: Berger, Frédéric. Gregor Mendel Institute; Austria
Materia
CHROMATIN
EVOLUTION
H2A.M
H2A.W
HETEROCHROMATIN
HISTONE
HISTONE VARIANT
STREPTOPHYTES
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/185011
Acceder
id CONICETDig_1fc18b06b4cc48e8bce9f69a15245387
oai_identifier_str oai:ri.conicet.gov.ar:11336/185011
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.WLei, BingkunCapella, MatiasMontgomery, Sean A.Borg, MichaelOsakabe, AkihisaGoiser, MalgorzataMuhammad, AbubakarBraun, SigurdBerger, FrédéricCHROMATINEVOLUTIONH2A.MH2A.WHETEROCHROMATINHISTONEHISTONE VARIANTSTREPTOPHYTEShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Diversification of histone variants is marked by the acquisition of distinct motifs and functional properties through convergent evolution.1–4 H2A variants are distinguished by specific C-terminal motifs and tend to be segregated within defined domains of the genome.5,6 Whether evolution of these motifs pre-dated the evolution of segregation mechanisms or vice versa has remained unclear. A suitable model to address this question is the variant H2A.W, which evolved in plants through acquisition of a KSPK motif7 and is tightly associated with heterochromatin.4 We used fission yeast, where chromatin is naturally devoid of H2A.W, to study the impact of engineered chimeras combining yeast H2A with the KSPK motif. Biochemical assays showed that the KSPK motif conferred nucleosomes with specific properties. Despite uniform incorporation of the engineered H2A chimeras in the yeast genome, the KSPK motif specifically affected heterochromatin composition and function. We conclude that the KSPK motif promotes chromatin properties in yeast that are comparable to the properties and function of H2A.W in plant heterochromatin. We propose that the selection of functional motifs confer histone variants with properties that impact primarily a specific chromatin state. The association between a new histone variant and a preferred chromatin state can thus provide a setting for the evolution of mechanisms that segregate the new variant to this state, thereby enhancing the impact of the selected properties of the variant on genome activity.Fil: Lei, Bingkun. Gregor Mendel Institute; AustriaFil: Capella, Matias. 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: Montgomery, Sean A.. Gregor Mendel Institute; AustriaFil: Borg, Michael. Gregor Mendel Institute; AustriaFil: Osakabe, Akihisa. Gregor Mendel Institute; AustriaFil: Goiser, Malgorzata. Gregor Mendel Institute; AustriaFil: Muhammad, Abubakar. Universitat Technical Zu Munich; AlemaniaFil: Braun, Sigurd. Universitat Technical Zu Munich; AlemaniaFil: Berger, Frédéric. Gregor Mendel Institute; AustriaCell Press2021-01info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/185011Lei, Bingkun; Capella, Matias; Montgomery, Sean A.; Borg, Michael; Osakabe, Akihisa; et al.; A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W; Cell Press; Current Biology; 31; 1; 1-2021; 182-191.e50960-9822CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://linkinghub.elsevier.com/retrieve/pii/S0960982220314913info:eu-repo/semantics/altIdentifier/doi/10.1016/j.cub.2020.09.080info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-nd/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T09:53:49Zoai:ri.conicet.gov.ar:11336/185011instacron: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 09:53:49.592CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W
title A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W
spellingShingle A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W
Lei, Bingkun
CHROMATIN
EVOLUTION
H2A.M
H2A.W
HETEROCHROMATIN
HISTONE
HISTONE VARIANT
STREPTOPHYTES
title_short A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W
title_full A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W
title_fullStr A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W
title_full_unstemmed A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W
title_sort A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W
dc.creator.none.fl_str_mv Lei, Bingkun
Capella, Matias
Montgomery, Sean A.
Borg, Michael
Osakabe, Akihisa
Goiser, Malgorzata
Muhammad, Abubakar
Braun, Sigurd
Berger, Frédéric
author Lei, Bingkun
author_facet Lei, Bingkun
Capella, Matias
Montgomery, Sean A.
Borg, Michael
Osakabe, Akihisa
Goiser, Malgorzata
Muhammad, Abubakar
Braun, Sigurd
Berger, Frédéric
author_role author
author2 Capella, Matias
Montgomery, Sean A.
Borg, Michael
Osakabe, Akihisa
Goiser, Malgorzata
Muhammad, Abubakar
Braun, Sigurd
Berger, Frédéric
author2_role author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv CHROMATIN
EVOLUTION
H2A.M
H2A.W
HETEROCHROMATIN
HISTONE
HISTONE VARIANT
STREPTOPHYTES
topic CHROMATIN
EVOLUTION
H2A.M
H2A.W
HETEROCHROMATIN
HISTONE
HISTONE VARIANT
STREPTOPHYTES
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Diversification of histone variants is marked by the acquisition of distinct motifs and functional properties through convergent evolution.1–4 H2A variants are distinguished by specific C-terminal motifs and tend to be segregated within defined domains of the genome.5,6 Whether evolution of these motifs pre-dated the evolution of segregation mechanisms or vice versa has remained unclear. A suitable model to address this question is the variant H2A.W, which evolved in plants through acquisition of a KSPK motif7 and is tightly associated with heterochromatin.4 We used fission yeast, where chromatin is naturally devoid of H2A.W, to study the impact of engineered chimeras combining yeast H2A with the KSPK motif. Biochemical assays showed that the KSPK motif conferred nucleosomes with specific properties. Despite uniform incorporation of the engineered H2A chimeras in the yeast genome, the KSPK motif specifically affected heterochromatin composition and function. We conclude that the KSPK motif promotes chromatin properties in yeast that are comparable to the properties and function of H2A.W in plant heterochromatin. We propose that the selection of functional motifs confer histone variants with properties that impact primarily a specific chromatin state. The association between a new histone variant and a preferred chromatin state can thus provide a setting for the evolution of mechanisms that segregate the new variant to this state, thereby enhancing the impact of the selected properties of the variant on genome activity.
Fil: Lei, Bingkun. Gregor Mendel Institute; Austria
Fil: Capella, Matias. 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: Montgomery, Sean A.. Gregor Mendel Institute; Austria
Fil: Borg, Michael. Gregor Mendel Institute; Austria
Fil: Osakabe, Akihisa. Gregor Mendel Institute; Austria
Fil: Goiser, Malgorzata. Gregor Mendel Institute; Austria
Fil: Muhammad, Abubakar. Universitat Technical Zu Munich; Alemania
Fil: Braun, Sigurd. Universitat Technical Zu Munich; Alemania
Fil: Berger, Frédéric. Gregor Mendel Institute; Austria
description Diversification of histone variants is marked by the acquisition of distinct motifs and functional properties through convergent evolution.1–4 H2A variants are distinguished by specific C-terminal motifs and tend to be segregated within defined domains of the genome.5,6 Whether evolution of these motifs pre-dated the evolution of segregation mechanisms or vice versa has remained unclear. A suitable model to address this question is the variant H2A.W, which evolved in plants through acquisition of a KSPK motif7 and is tightly associated with heterochromatin.4 We used fission yeast, where chromatin is naturally devoid of H2A.W, to study the impact of engineered chimeras combining yeast H2A with the KSPK motif. Biochemical assays showed that the KSPK motif conferred nucleosomes with specific properties. Despite uniform incorporation of the engineered H2A chimeras in the yeast genome, the KSPK motif specifically affected heterochromatin composition and function. We conclude that the KSPK motif promotes chromatin properties in yeast that are comparable to the properties and function of H2A.W in plant heterochromatin. We propose that the selection of functional motifs confer histone variants with properties that impact primarily a specific chromatin state. The association between a new histone variant and a preferred chromatin state can thus provide a setting for the evolution of mechanisms that segregate the new variant to this state, thereby enhancing the impact of the selected properties of the variant on genome activity.
publishDate 2021
dc.date.none.fl_str_mv 2021-01
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/11336/185011
Lei, Bingkun; Capella, Matias; Montgomery, Sean A.; Borg, Michael; Osakabe, Akihisa; et al.; A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W; Cell Press; Current Biology; 31; 1; 1-2021; 182-191.e5
0960-9822
CONICET Digital
CONICET
url http://hdl.handle.net/11336/185011
identifier_str_mv Lei, Bingkun; Capella, Matias; Montgomery, Sean A.; Borg, Michael; Osakabe, Akihisa; et al.; A Synthetic Approach to Reconstruct the Evolutionary and Functional Innovations of the Plant Histone Variant H2A.W; Cell Press; Current Biology; 31; 1; 1-2021; 182-191.e5
0960-9822
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://linkinghub.elsevier.com/retrieve/pii/S0960982220314913
info:eu-repo/semantics/altIdentifier/doi/10.1016/j.cub.2020.09.080
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-nd/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Cell Press
publisher.none.fl_str_mv Cell Press
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
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score 13.13397

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