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It Is Just a Matter of Time: Balancing Homologous Recombination and Non-homologous End Joining at the rDNA Locus During Meiosis

Ribosomal RNA genes (rDNAs) are located in large domains of hundreds of rDNA units organized in a head-to-tail manner. The proper and stable inheritance of rDNA clusters is of paramount importance for survival. Yet, these highly repetitive elements pose a potential risk to the genome since they can...

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Autores principales: Sims, Jason, Rabanal, Fernando A., Elgert, Christiane, von Haeseler, Arndt, Schlögelhofer, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8580885/
https://www.ncbi.nlm.nih.gov/pubmed/34777453
http://dx.doi.org/10.3389/fpls.2021.773052
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author Sims, Jason
Rabanal, Fernando A.
Elgert, Christiane
von Haeseler, Arndt
Schlögelhofer, Peter
author_facet Sims, Jason
Rabanal, Fernando A.
Elgert, Christiane
von Haeseler, Arndt
Schlögelhofer, Peter
author_sort Sims, Jason
collection PubMed
description Ribosomal RNA genes (rDNAs) are located in large domains of hundreds of rDNA units organized in a head-to-tail manner. The proper and stable inheritance of rDNA clusters is of paramount importance for survival. Yet, these highly repetitive elements pose a potential risk to the genome since they can undergo non-allelic exchanges. Here, we review the current knowledge of the organization of the rDNA clusters in Arabidopsis thaliana and their stability during meiosis. Recent findings suggest that during meiosis, all rDNA loci are embedded within the nucleolus favoring non-homologous end joining (NHEJ) as a repair mechanism, while DNA repair via homologous recombination (HR) appears to be a rare event. We propose a model where (1) frequent meiotic NHEJ events generate abundant single nucleotide polymorphisms and insertions/deletions within the rDNA, resulting in a heterogeneous population of rDNA units and (2) rare HR events dynamically change rDNA unit numbers, only to be observed in large populations over many generations. Based on the latest efforts to delineate the entire rDNA sequence in A. thaliana, we discuss evidence supporting this model. The results compiled so far draw a surprising picture of rDNA sequence heterogeneity between individual units. Furthermore, rDNA cluster sizes have been recognized as relatively stable when observing less than 10 generations, yet emerged as major determinant of genome size variation between different A. thaliana ecotypes. The sequencing efforts also revealed that transcripts from the diverse rDNA units yield heterogenous ribosome populations with potential functional implications. These findings strongly motivate further research to understand the mechanisms that maintain the metastable state of rDNA loci.
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spelling pubmed-85808852021-11-12 It Is Just a Matter of Time: Balancing Homologous Recombination and Non-homologous End Joining at the rDNA Locus During Meiosis Sims, Jason Rabanal, Fernando A. Elgert, Christiane von Haeseler, Arndt Schlögelhofer, Peter Front Plant Sci Plant Science Ribosomal RNA genes (rDNAs) are located in large domains of hundreds of rDNA units organized in a head-to-tail manner. The proper and stable inheritance of rDNA clusters is of paramount importance for survival. Yet, these highly repetitive elements pose a potential risk to the genome since they can undergo non-allelic exchanges. Here, we review the current knowledge of the organization of the rDNA clusters in Arabidopsis thaliana and their stability during meiosis. Recent findings suggest that during meiosis, all rDNA loci are embedded within the nucleolus favoring non-homologous end joining (NHEJ) as a repair mechanism, while DNA repair via homologous recombination (HR) appears to be a rare event. We propose a model where (1) frequent meiotic NHEJ events generate abundant single nucleotide polymorphisms and insertions/deletions within the rDNA, resulting in a heterogeneous population of rDNA units and (2) rare HR events dynamically change rDNA unit numbers, only to be observed in large populations over many generations. Based on the latest efforts to delineate the entire rDNA sequence in A. thaliana, we discuss evidence supporting this model. The results compiled so far draw a surprising picture of rDNA sequence heterogeneity between individual units. Furthermore, rDNA cluster sizes have been recognized as relatively stable when observing less than 10 generations, yet emerged as major determinant of genome size variation between different A. thaliana ecotypes. The sequencing efforts also revealed that transcripts from the diverse rDNA units yield heterogenous ribosome populations with potential functional implications. These findings strongly motivate further research to understand the mechanisms that maintain the metastable state of rDNA loci. Frontiers Media S.A. 2021-10-28 /pmc/articles/PMC8580885/ /pubmed/34777453 http://dx.doi.org/10.3389/fpls.2021.773052 Text en Copyright © 2021 Sims, Rabanal, Elgert, von Haeseler and Schlögelhofer. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Sims, Jason
Rabanal, Fernando A.
Elgert, Christiane
von Haeseler, Arndt
Schlögelhofer, Peter
It Is Just a Matter of Time: Balancing Homologous Recombination and Non-homologous End Joining at the rDNA Locus During Meiosis
title It Is Just a Matter of Time: Balancing Homologous Recombination and Non-homologous End Joining at the rDNA Locus During Meiosis
title_full It Is Just a Matter of Time: Balancing Homologous Recombination and Non-homologous End Joining at the rDNA Locus During Meiosis
title_fullStr It Is Just a Matter of Time: Balancing Homologous Recombination and Non-homologous End Joining at the rDNA Locus During Meiosis
title_full_unstemmed It Is Just a Matter of Time: Balancing Homologous Recombination and Non-homologous End Joining at the rDNA Locus During Meiosis
title_short It Is Just a Matter of Time: Balancing Homologous Recombination and Non-homologous End Joining at the rDNA Locus During Meiosis
title_sort it is just a matter of time: balancing homologous recombination and non-homologous end joining at the rdna locus during meiosis
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8580885/
https://www.ncbi.nlm.nih.gov/pubmed/34777453
http://dx.doi.org/10.3389/fpls.2021.773052
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