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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

ABSTRACT: 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.

SUBMITTER: Sims J

PROVIDER: S-EPMC8580885 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:An important objective in genome research is to relate genome structure to gene function. Sequence comparisons among orthologous and paralogous genes and their allelic variants can reveal sequences of functional significance. Here, we describe a 379-kb region on chromosome 1 of maize that enables us to reconstruct chromosome breakage, transposition, non-homologous end-joining, and homologous recombination events. Such a high-density composition of various mechanisms in a small chromosomal interval exemplifies the evolution of gene regulation and allelic diversity in general. It also illustrates the evolutionary pace of changes in plants, where many of the above mechanisms are of somatic origin. In contrast to animals, somatic alterations can easily be transmitted through meiosis because the germline in plants is contiguous to somatic tissue, permitting the recovery of such chromosomal rearrangements. The analyzed region contains the P1-wr allele, a variant of the genetically well-defined p1 gene, which encodes a Myb-like transcriptional activator in maize. The P1-wr allele consists of eleven nearly perfect P1-wr 12-kb repeats that are arranged in a tandem head-to-tail array. Although a technical challenge to sequence such a structure by shotgun sequencing, we overcame this problem by subcloning each repeat and ordering them based on nucleotide variations. These polymorphisms were also critical for recombination and expression analysis in presence and absence of the trans-acting epigenetic factor Ufo1. Interestingly, chimeras of the p1 and p2 genes, p2/p1 and p1/p2, are framing the P1-wr cluster. Reconstruction of sequence amplification steps at the p locus showed the evolution from a single Myb-homolog to the multi-gene P1-wr cluster. It also demonstrates how non-homologous end-joining can create novel gene fusions. Comparisons to orthologous regions in sorghum and rice also indicate a greater instability of the maize genome, probably due to diploidization following allotetraploidization.

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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

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