Cargando…
Ability of a selfish B chromosome to evade genome elimination in the jewel wasp, Nasonia vitripennis
B chromosomes are non-essential, extra chromosomes that can exhibit transmission-enhancing behaviors, including meiotic drive, mitotic drive, and induction of genome elimination, in plants and animals. A fundamental but poorly understood question is what characteristics allow B chromosomes to exhibi...
Autores principales: | , , , , , , |
---|---|
Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Springer International Publishing
2023
|
Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10462710/ https://www.ncbi.nlm.nih.gov/pubmed/37524915 http://dx.doi.org/10.1038/s41437-023-00639-0 |
_version_ | 1785098092011323392 |
---|---|
author | Lee, Haena Seo, Pooreum Teklay, Salina Yuguchi, Emily Benetta, Elena Dalla Werren, John H. Ferree, Patrick M. |
author_facet | Lee, Haena Seo, Pooreum Teklay, Salina Yuguchi, Emily Benetta, Elena Dalla Werren, John H. Ferree, Patrick M. |
author_sort | Lee, Haena |
collection | PubMed |
description | B chromosomes are non-essential, extra chromosomes that can exhibit transmission-enhancing behaviors, including meiotic drive, mitotic drive, and induction of genome elimination, in plants and animals. A fundamental but poorly understood question is what characteristics allow B chromosomes to exhibit these extraordinary behaviors. The jewel wasp, Nasonia vitripennis, harbors a heterochromatic, paternally transmitted B chromosome known as paternal sex ratio (PSR), which causes complete elimination of the sperm-contributed half of the genome during the first mitotic division of fertilized embryos. This genome elimination event may result from specific, previously observed alterations of the paternal chromatin. Due to the haplo-diploid reproduction of the wasp, genome elimination by PSR causes female-destined embryos to develop as haploid males that transmit PSR. PSR does not undergo self-elimination despite its presence with the paternal chromatin until the elimination event. Here we performed fluorescence microscopic analyses aimed at understanding this unexplained property. Our results show that PSR, like the rest of the genome, participates in the histone-to-protamine transition, arguing that PSR does not avoid this transition to escape self-elimination. In addition, PSR partially escapes the chromatin-altering activity of the intracellular bacterium, Wolbachia, demonstrating that this ability to evade chromatin alteration is not limited to PSR’s own activity. Finally, we observed that the rDNA locus and other unidentified heterochromatic regions of the wasp’s genome also seem to evade chromatin disruption by PSR, suggesting that PSR’s genome-eliminating activity does not affect heterochromatin. Thus, PSR may target an aspect of euchromatin to cause genome elimination. |
format | Online Article Text |
id | pubmed-10462710 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Springer International Publishing |
record_format | MEDLINE/PubMed |
spelling | pubmed-104627102023-08-30 Ability of a selfish B chromosome to evade genome elimination in the jewel wasp, Nasonia vitripennis Lee, Haena Seo, Pooreum Teklay, Salina Yuguchi, Emily Benetta, Elena Dalla Werren, John H. Ferree, Patrick M. Heredity (Edinb) Article B chromosomes are non-essential, extra chromosomes that can exhibit transmission-enhancing behaviors, including meiotic drive, mitotic drive, and induction of genome elimination, in plants and animals. A fundamental but poorly understood question is what characteristics allow B chromosomes to exhibit these extraordinary behaviors. The jewel wasp, Nasonia vitripennis, harbors a heterochromatic, paternally transmitted B chromosome known as paternal sex ratio (PSR), which causes complete elimination of the sperm-contributed half of the genome during the first mitotic division of fertilized embryos. This genome elimination event may result from specific, previously observed alterations of the paternal chromatin. Due to the haplo-diploid reproduction of the wasp, genome elimination by PSR causes female-destined embryos to develop as haploid males that transmit PSR. PSR does not undergo self-elimination despite its presence with the paternal chromatin until the elimination event. Here we performed fluorescence microscopic analyses aimed at understanding this unexplained property. Our results show that PSR, like the rest of the genome, participates in the histone-to-protamine transition, arguing that PSR does not avoid this transition to escape self-elimination. In addition, PSR partially escapes the chromatin-altering activity of the intracellular bacterium, Wolbachia, demonstrating that this ability to evade chromatin alteration is not limited to PSR’s own activity. Finally, we observed that the rDNA locus and other unidentified heterochromatic regions of the wasp’s genome also seem to evade chromatin disruption by PSR, suggesting that PSR’s genome-eliminating activity does not affect heterochromatin. Thus, PSR may target an aspect of euchromatin to cause genome elimination. Springer International Publishing 2023-07-31 2023-09 /pmc/articles/PMC10462710/ /pubmed/37524915 http://dx.doi.org/10.1038/s41437-023-00639-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Lee, Haena Seo, Pooreum Teklay, Salina Yuguchi, Emily Benetta, Elena Dalla Werren, John H. Ferree, Patrick M. Ability of a selfish B chromosome to evade genome elimination in the jewel wasp, Nasonia vitripennis |
title | Ability of a selfish B chromosome to evade genome elimination in the jewel wasp, Nasonia vitripennis |
title_full | Ability of a selfish B chromosome to evade genome elimination in the jewel wasp, Nasonia vitripennis |
title_fullStr | Ability of a selfish B chromosome to evade genome elimination in the jewel wasp, Nasonia vitripennis |
title_full_unstemmed | Ability of a selfish B chromosome to evade genome elimination in the jewel wasp, Nasonia vitripennis |
title_short | Ability of a selfish B chromosome to evade genome elimination in the jewel wasp, Nasonia vitripennis |
title_sort | ability of a selfish b chromosome to evade genome elimination in the jewel wasp, nasonia vitripennis |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10462710/ https://www.ncbi.nlm.nih.gov/pubmed/37524915 http://dx.doi.org/10.1038/s41437-023-00639-0 |
work_keys_str_mv | AT leehaena abilityofaselfishbchromosometoevadegenomeeliminationinthejewelwaspnasoniavitripennis AT seopooreum abilityofaselfishbchromosometoevadegenomeeliminationinthejewelwaspnasoniavitripennis AT teklaysalina abilityofaselfishbchromosometoevadegenomeeliminationinthejewelwaspnasoniavitripennis AT yuguchiemily abilityofaselfishbchromosometoevadegenomeeliminationinthejewelwaspnasoniavitripennis AT benettaelenadalla abilityofaselfishbchromosometoevadegenomeeliminationinthejewelwaspnasoniavitripennis AT werrenjohnh abilityofaselfishbchromosometoevadegenomeeliminationinthejewelwaspnasoniavitripennis AT ferreepatrickm abilityofaselfishbchromosometoevadegenomeeliminationinthejewelwaspnasoniavitripennis |