Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in Heteroptera

Autores
Toscani, María Ayelén; Pigozzi, Maria Ines; Papeschi, Alba Graciela; Bressa, Maria Jose
Año de publicación
2022
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
Heteropteran insects exhibit a remarkable diversity of meiotic processes, including coexistence of different chromosomes types with different behavior during the first meiotic division, non-chiasmatic segregation, and inverted meiosis. Because of this diversity they represent suitable models to study fundamental questions about the mechanisms of chromosome behavior during cell division. All heteropteran species possess holokinetic chromosomes and in most of them the autosomal chromosomes synapse, recombine, and undergoe pre-reductional meiosis. In contrast, the sex chromosomes are achiasmatic, behave as univalents at metaphase I and present an inverted or post-reductional meiosis. An exception to this typical behavior is found in Pachylis argentinus, where both the autosomes and the X-chromosome divide reductionally at anaphase I and then divide equationally at anaphase II. In the present report, we analyzed the distribution of histones H3K9me2 and H3K9me3 in P. argentinus and in five species that have simple and multiple sex chromosome systems with typical chromosome segregation, Belostoma elegans, B. oxyurum, Holhymenia rubiginosa, Phthia picta, and Oncopeltus unifasciatellus. We found that H3K9me3 is a marker for sex-chromosomes from early prophase I to the end of the first division in all the species. H3K9me2 also marks the sex chromosomes since early prophase but shows different dynamics at metaphase I depending on the sex-chromosome segregation: it is lost in species with equationally dividing sex chromosomes but remains on one end of the X chromosome of P. argentinus, where chromatids migrate together at anaphase I. It is proposed that the loss of H3K9me2 from the sex chromosomes observed at metaphase I may be part of a set of epigenetic signals that lead to the reductional or equational division of autosomes and sex chromosomes observed in most Heteroptera. The present observations suggest that the histone modifications analyzed here evolved in Heteroptera as markers for asynaptic and achiasmatic sex chromosomes during meiosis to allow the distinction from the chiasmatic autosomal chromosomes.
Fil: Toscani, María Ayelén. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Investigaciones Biomédicas. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Investigaciones Biomédicas; Argentina
Fil: Pigozzi, Maria Ines. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Investigaciones Biomédicas. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Investigaciones Biomédicas; Argentina
Fil: Papeschi, Alba Graciela. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Bressa, Maria Jose. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Materia
AUTOSOMES
HETEROPTERA
HISTONE MODIFICATIONS
HOLOKINETIC CHROMOSOMES
M CHROMOSOMES
MEIOSIS
SEX CHROMOSOMES
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:11336/202950
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/202950
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in HeteropteraToscani, María AyelénPigozzi, Maria InesPapeschi, Alba GracielaBressa, Maria JoseAUTOSOMESHETEROPTERAHISTONE MODIFICATIONSHOLOKINETIC CHROMOSOMESM CHROMOSOMESMEIOSISSEX CHROMOSOMEShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1Heteropteran insects exhibit a remarkable diversity of meiotic processes, including coexistence of different chromosomes types with different behavior during the first meiotic division, non-chiasmatic segregation, and inverted meiosis. Because of this diversity they represent suitable models to study fundamental questions about the mechanisms of chromosome behavior during cell division. All heteropteran species possess holokinetic chromosomes and in most of them the autosomal chromosomes synapse, recombine, and undergoe pre-reductional meiosis. In contrast, the sex chromosomes are achiasmatic, behave as univalents at metaphase I and present an inverted or post-reductional meiosis. An exception to this typical behavior is found in Pachylis argentinus, where both the autosomes and the X-chromosome divide reductionally at anaphase I and then divide equationally at anaphase II. In the present report, we analyzed the distribution of histones H3K9me2 and H3K9me3 in P. argentinus and in five species that have simple and multiple sex chromosome systems with typical chromosome segregation, Belostoma elegans, B. oxyurum, Holhymenia rubiginosa, Phthia picta, and Oncopeltus unifasciatellus. We found that H3K9me3 is a marker for sex-chromosomes from early prophase I to the end of the first division in all the species. H3K9me2 also marks the sex chromosomes since early prophase but shows different dynamics at metaphase I depending on the sex-chromosome segregation: it is lost in species with equationally dividing sex chromosomes but remains on one end of the X chromosome of P. argentinus, where chromatids migrate together at anaphase I. It is proposed that the loss of H3K9me2 from the sex chromosomes observed at metaphase I may be part of a set of epigenetic signals that lead to the reductional or equational division of autosomes and sex chromosomes observed in most Heteroptera. The present observations suggest that the histone modifications analyzed here evolved in Heteroptera as markers for asynaptic and achiasmatic sex chromosomes during meiosis to allow the distinction from the chiasmatic autosomal chromosomes.Fil: Toscani, María Ayelén. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Investigaciones Biomédicas. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Investigaciones Biomédicas; ArgentinaFil: Pigozzi, Maria Ines. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Investigaciones Biomédicas. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Investigaciones Biomédicas; ArgentinaFil: Papeschi, Alba Graciela. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Bressa, Maria Jose. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFrontiers Media2022-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/202950Toscani, María Ayelén; Pigozzi, Maria Ines; Papeschi, Alba Graciela; Bressa, Maria Jose; Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in Heteroptera; Frontiers Media; Frontiers in Ecology and Evolution; 10; 3-2022; 1-172296-701XCONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://www.frontiersin.org/articles/10.3389/fevo.2022.836786/fullinfo:eu-repo/semantics/altIdentifier/doi/10.3389/fevo.2022.836786info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-03T10:10:53Zoai:ri.conicet.gov.ar:11336/202950instacron: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 10:10:53.441CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in Heteroptera
title Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in Heteroptera
spellingShingle Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in Heteroptera
Toscani, María Ayelén
AUTOSOMES
HETEROPTERA
HISTONE MODIFICATIONS
HOLOKINETIC CHROMOSOMES
M CHROMOSOMES
MEIOSIS
SEX CHROMOSOMES
title_short Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in Heteroptera
title_full Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in Heteroptera
title_fullStr Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in Heteroptera
title_full_unstemmed Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in Heteroptera
title_sort Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in Heteroptera
dc.creator.none.fl_str_mv Toscani, María Ayelén
Pigozzi, Maria Ines
Papeschi, Alba Graciela
Bressa, Maria Jose
author Toscani, María Ayelén
author_facet Toscani, María Ayelén
Pigozzi, Maria Ines
Papeschi, Alba Graciela
Bressa, Maria Jose
author_role author
author2 Pigozzi, Maria Ines
Papeschi, Alba Graciela
Bressa, Maria Jose
author2_role author
author
author
dc.subject.none.fl_str_mv AUTOSOMES
HETEROPTERA
HISTONE MODIFICATIONS
HOLOKINETIC CHROMOSOMES
M CHROMOSOMES
MEIOSIS
SEX CHROMOSOMES
topic AUTOSOMES
HETEROPTERA
HISTONE MODIFICATIONS
HOLOKINETIC CHROMOSOMES
M CHROMOSOMES
MEIOSIS
SEX CHROMOSOMES
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv Heteropteran insects exhibit a remarkable diversity of meiotic processes, including coexistence of different chromosomes types with different behavior during the first meiotic division, non-chiasmatic segregation, and inverted meiosis. Because of this diversity they represent suitable models to study fundamental questions about the mechanisms of chromosome behavior during cell division. All heteropteran species possess holokinetic chromosomes and in most of them the autosomal chromosomes synapse, recombine, and undergoe pre-reductional meiosis. In contrast, the sex chromosomes are achiasmatic, behave as univalents at metaphase I and present an inverted or post-reductional meiosis. An exception to this typical behavior is found in Pachylis argentinus, where both the autosomes and the X-chromosome divide reductionally at anaphase I and then divide equationally at anaphase II. In the present report, we analyzed the distribution of histones H3K9me2 and H3K9me3 in P. argentinus and in five species that have simple and multiple sex chromosome systems with typical chromosome segregation, Belostoma elegans, B. oxyurum, Holhymenia rubiginosa, Phthia picta, and Oncopeltus unifasciatellus. We found that H3K9me3 is a marker for sex-chromosomes from early prophase I to the end of the first division in all the species. H3K9me2 also marks the sex chromosomes since early prophase but shows different dynamics at metaphase I depending on the sex-chromosome segregation: it is lost in species with equationally dividing sex chromosomes but remains on one end of the X chromosome of P. argentinus, where chromatids migrate together at anaphase I. It is proposed that the loss of H3K9me2 from the sex chromosomes observed at metaphase I may be part of a set of epigenetic signals that lead to the reductional or equational division of autosomes and sex chromosomes observed in most Heteroptera. The present observations suggest that the histone modifications analyzed here evolved in Heteroptera as markers for asynaptic and achiasmatic sex chromosomes during meiosis to allow the distinction from the chiasmatic autosomal chromosomes.
Fil: Toscani, María Ayelén. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Investigaciones Biomédicas. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Investigaciones Biomédicas; Argentina
Fil: Pigozzi, Maria Ines. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Houssay. Instituto de Investigaciones Biomédicas. Universidad de Buenos Aires. Facultad de Medicina. Instituto de Investigaciones Biomédicas; Argentina
Fil: Papeschi, Alba Graciela. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Bressa, Maria Jose. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Ecología, Genética y Evolución; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
description Heteropteran insects exhibit a remarkable diversity of meiotic processes, including coexistence of different chromosomes types with different behavior during the first meiotic division, non-chiasmatic segregation, and inverted meiosis. Because of this diversity they represent suitable models to study fundamental questions about the mechanisms of chromosome behavior during cell division. All heteropteran species possess holokinetic chromosomes and in most of them the autosomal chromosomes synapse, recombine, and undergoe pre-reductional meiosis. In contrast, the sex chromosomes are achiasmatic, behave as univalents at metaphase I and present an inverted or post-reductional meiosis. An exception to this typical behavior is found in Pachylis argentinus, where both the autosomes and the X-chromosome divide reductionally at anaphase I and then divide equationally at anaphase II. In the present report, we analyzed the distribution of histones H3K9me2 and H3K9me3 in P. argentinus and in five species that have simple and multiple sex chromosome systems with typical chromosome segregation, Belostoma elegans, B. oxyurum, Holhymenia rubiginosa, Phthia picta, and Oncopeltus unifasciatellus. We found that H3K9me3 is a marker for sex-chromosomes from early prophase I to the end of the first division in all the species. H3K9me2 also marks the sex chromosomes since early prophase but shows different dynamics at metaphase I depending on the sex-chromosome segregation: it is lost in species with equationally dividing sex chromosomes but remains on one end of the X chromosome of P. argentinus, where chromatids migrate together at anaphase I. It is proposed that the loss of H3K9me2 from the sex chromosomes observed at metaphase I may be part of a set of epigenetic signals that lead to the reductional or equational division of autosomes and sex chromosomes observed in most Heteroptera. The present observations suggest that the histone modifications analyzed here evolved in Heteroptera as markers for asynaptic and achiasmatic sex chromosomes during meiosis to allow the distinction from the chiasmatic autosomal chromosomes.
publishDate 2022
dc.date.none.fl_str_mv 2022-03
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/11336/202950
Toscani, María Ayelén; Pigozzi, Maria Ines; Papeschi, Alba Graciela; Bressa, Maria Jose; Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in Heteroptera; Frontiers Media; Frontiers in Ecology and Evolution; 10; 3-2022; 1-17
2296-701X
CONICET Digital
CONICET
url http://hdl.handle.net/11336/202950
identifier_str_mv Toscani, María Ayelén; Pigozzi, Maria Ines; Papeschi, Alba Graciela; Bressa, Maria Jose; Histone H3 Methylation and Autosomal vs. Sex Chromosome Segregation During Male Meiosis in Heteroptera; Frontiers Media; Frontiers in Ecology and Evolution; 10; 3-2022; 1-17
2296-701X
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://www.frontiersin.org/articles/10.3389/fevo.2022.836786/full
info:eu-repo/semantics/altIdentifier/doi/10.3389/fevo.2022.836786
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
application/pdf
dc.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
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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