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Exploring the Relationship between Spontaneous Sister Chromatid Exchange and Genome Instability in Two Cryptic Species of Non-Human Primates
SIMPLE SUMMARY: Studies on the evolution of Neotropical primates are currently based on molecular cytogenetics. Recent technological advancements have provided new capabilities and opportunities to explore novel mechanisms of evolutionary dynamics. We analyzed the genomic instability and variability...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
MDPI
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9913470/ https://www.ncbi.nlm.nih.gov/pubmed/36766399 http://dx.doi.org/10.3390/ani13030510 |
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author | Nieves, Mariela Puntieri, Fiona Bailey, Susan M. Mudry, Marta D. Maranon, David G. |
author_facet | Nieves, Mariela Puntieri, Fiona Bailey, Susan M. Mudry, Marta D. Maranon, David G. |
author_sort | Nieves, Mariela |
collection | PubMed |
description | SIMPLE SUMMARY: Studies on the evolution of Neotropical primates are currently based on molecular cytogenetics. Recent technological advancements have provided new capabilities and opportunities to explore novel mechanisms of evolutionary dynamics. We analyzed the genomic instability and variability in two species of Ateles by characterizing the spontaneous frequencies of sister chromatid exchange (SCE) along chromosomes (genomic) and specifically within telomeres. Our analyses support the hypothesis that regions of Ateles chromosomes susceptible to recombination events represent fragile sites and evolutionary hot spots. Therefore, we propose SCE analyses as a valuable indicator of genome instability in non-human primates. ABSTRACT: There are extensive studies on chromosome morphology and karyotype diversity in primates, yet we still lack insight into genomic instability as a key factor underlying the enormous interspecies chromosomal variability and its potential contribution to evolutionary dynamics. In this sense, the assessment of spontaneous sister chromatid exchange (SCE) frequencies represents a powerful tool for evaluating genome stability. Here, we employed G-banding, fluorescence plus Giemsa (FPG), and chromosome orientation fluorescence in situ hybridization (CO-FISH) methodologies to characterize both chromosome-specific frequencies of spontaneously occurring SCE throughout the genome (G-SCE) and telomere-specific SCE (T-SCE). We analyzed primary fibroblast cultures from two male species of Ateles living in captivity: Ateles paniscus (APA) and Ateles chamek (ACH). High frequencies of G-SCEs were observed in both species. Interestingly, G-SCEs clustered on evolutionary relevant chromosome pairs: ACH chromosomes 1, 2, 3, 4, and 7, and APA chromosomes 1, 2, 3, 4/12, 7, and 10. Furthermore, a statistically significant difference between the observed and expected G-SCE frequencies, not correlated with chromosome size, was also detected. CO-FISH analyses revealed the presence of telomere-specific recombination events in both species, which included T-SCE, as well as interstitial telomere signals and telomere duplications, with APA chromosomes displaying higher frequencies, compared to ACH. Our analyses support the hypothesis that regions of Ateles chromosomes susceptible to recombination events are fragile sites and evolutionary hot spots. Thus, we propose SCE analyses as a valuable indicator of genome instability in non-human primates. |
format | Online Article Text |
id | pubmed-9913470 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | MDPI |
record_format | MEDLINE/PubMed |
spelling | pubmed-99134702023-02-11 Exploring the Relationship between Spontaneous Sister Chromatid Exchange and Genome Instability in Two Cryptic Species of Non-Human Primates Nieves, Mariela Puntieri, Fiona Bailey, Susan M. Mudry, Marta D. Maranon, David G. Animals (Basel) Article SIMPLE SUMMARY: Studies on the evolution of Neotropical primates are currently based on molecular cytogenetics. Recent technological advancements have provided new capabilities and opportunities to explore novel mechanisms of evolutionary dynamics. We analyzed the genomic instability and variability in two species of Ateles by characterizing the spontaneous frequencies of sister chromatid exchange (SCE) along chromosomes (genomic) and specifically within telomeres. Our analyses support the hypothesis that regions of Ateles chromosomes susceptible to recombination events represent fragile sites and evolutionary hot spots. Therefore, we propose SCE analyses as a valuable indicator of genome instability in non-human primates. ABSTRACT: There are extensive studies on chromosome morphology and karyotype diversity in primates, yet we still lack insight into genomic instability as a key factor underlying the enormous interspecies chromosomal variability and its potential contribution to evolutionary dynamics. In this sense, the assessment of spontaneous sister chromatid exchange (SCE) frequencies represents a powerful tool for evaluating genome stability. Here, we employed G-banding, fluorescence plus Giemsa (FPG), and chromosome orientation fluorescence in situ hybridization (CO-FISH) methodologies to characterize both chromosome-specific frequencies of spontaneously occurring SCE throughout the genome (G-SCE) and telomere-specific SCE (T-SCE). We analyzed primary fibroblast cultures from two male species of Ateles living in captivity: Ateles paniscus (APA) and Ateles chamek (ACH). High frequencies of G-SCEs were observed in both species. Interestingly, G-SCEs clustered on evolutionary relevant chromosome pairs: ACH chromosomes 1, 2, 3, 4, and 7, and APA chromosomes 1, 2, 3, 4/12, 7, and 10. Furthermore, a statistically significant difference between the observed and expected G-SCE frequencies, not correlated with chromosome size, was also detected. CO-FISH analyses revealed the presence of telomere-specific recombination events in both species, which included T-SCE, as well as interstitial telomere signals and telomere duplications, with APA chromosomes displaying higher frequencies, compared to ACH. Our analyses support the hypothesis that regions of Ateles chromosomes susceptible to recombination events are fragile sites and evolutionary hot spots. Thus, we propose SCE analyses as a valuable indicator of genome instability in non-human primates. MDPI 2023-02-01 /pmc/articles/PMC9913470/ /pubmed/36766399 http://dx.doi.org/10.3390/ani13030510 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). |
spellingShingle | Article Nieves, Mariela Puntieri, Fiona Bailey, Susan M. Mudry, Marta D. Maranon, David G. Exploring the Relationship between Spontaneous Sister Chromatid Exchange and Genome Instability in Two Cryptic Species of Non-Human Primates |
title | Exploring the Relationship between Spontaneous Sister Chromatid Exchange and Genome Instability in Two Cryptic Species of Non-Human Primates |
title_full | Exploring the Relationship between Spontaneous Sister Chromatid Exchange and Genome Instability in Two Cryptic Species of Non-Human Primates |
title_fullStr | Exploring the Relationship between Spontaneous Sister Chromatid Exchange and Genome Instability in Two Cryptic Species of Non-Human Primates |
title_full_unstemmed | Exploring the Relationship between Spontaneous Sister Chromatid Exchange and Genome Instability in Two Cryptic Species of Non-Human Primates |
title_short | Exploring the Relationship between Spontaneous Sister Chromatid Exchange and Genome Instability in Two Cryptic Species of Non-Human Primates |
title_sort | exploring the relationship between spontaneous sister chromatid exchange and genome instability in two cryptic species of non-human primates |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9913470/ https://www.ncbi.nlm.nih.gov/pubmed/36766399 http://dx.doi.org/10.3390/ani13030510 |
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