Chromosome Dynamics Regulating Genomic Dispersion and Alteration of Nucleolus Organizer Regions (NORs)

Abstract

The nucleolus organizer regions (NORs) demonstrate differences in genomic dispersion and transcriptional activity among all organisms. I postulate that such differences stem from distinct genomic structures and their interactions from chromosome observations using fluorescence in situ hybridization and silver nitrate staining methods. Examples in primates and Australian bulldog ants indicate that chromosomal features indeed play a significant role in determining the properties of NORs. In primates, rDNA arrays that are located on the short arm of acrocentrics frequently form reciprocal associations ("affinity"), but they lack such associations ("non-affinity") with other repeat arrays-a binary molecular effect. These "rules" of affinity vs. non-affinity are extrapolated from the chromosomal configurations of meiotic prophase. In bulldog ants, genomic dispersions of rDNA loci expand much more widely following an increase in the number of acrocentric chromosomes formed by centric fission. Affinity appears to be a significantly greater force: associations likely form among rDNA and heterochromatin arrays of acrocentrics-thus, more acrocentrics bring about more rDNA loci. The specific interactions among NOR-related genome structures remain unclear and require further investigation. Here, I propose that there are limited and non-limited genomic dispersion systems that result from genomic affinity rules, inducing specific chromosomal configurations that are related to NORs.

Evolutionary insights into the genomic organization of major ribosomal DNA in ant chromosomes

“…This suggests several ribosomal gene amplification events have occurred in the different species of Myrmecia and that they have accumulated in karyotypes throughout the evolution of the genus. Only four out of 16 species from this monophyletic genus have the entire arm or intrachromosomal rDNA clusters restricted to a single pair of chromosomes (Hirai et al ., 1994, 1996; Hirai, 2020). This pattern is observed in species with small chromosome numbers, which suggests that a single NOR is plesiomorphic among Myrmecia (Hirai, 2020).…”

“…Such hypotheses are linked to the specific locations of these rDNA clusters on the chromosomes. Rearrangements, such as translocations, unequal exchange, and ectopic recombination mechanisms (i.e., between non‐homologous chromosomes), which can lead to gene dispersion or increases in number in the genome, are more likely in the terminal/subterminal regions of chromosomes and are uncommon in the intrachromosomal regions (Martins and Wasko, 2004; Mantovani et al ., 2005; Nguyen et al ., 2010; Roa and Guerra, 2012; Hirai, 2020).…”

“…Ectopic recombination is another mechanism suggested to explain the rDNA patterning in moths and butterflies (Nguyen et al ., 2010) and plants (Roa and Guerra, 2012). It is also included in the recent model proposed by Hirai (2020). In this model, two mechanisms are important: the “site effect” and the “molecular effect.” The former allows terminal region associations due to the proximity of these regions in a meiotic bouquet.…”

“…There are reports of species with multiple rDNA clusters associated with the centromeres of acrocentric chromosomes (Cazaux et al ., 2011). In the recent model proposed by Hirai (2020), the centromeric region of acrocentric chromosomes (chromosomes with a short and heterochromatic arm) that have rDNA genes associated with the centromere may behave as subterminal regions. Therefore, such an arrangement would also facilitate eventual associations of rDNA genes with other repetitive sequences and the occurrence of ectopic recombination, which leads to their dispersal in the genome (for details, see Hirai, 2020).…”

Classical and molecular cytogenetics of Belontia hasselti (Perciformes: Osphronemidae): Insights into the ZZ/ZW sex chromosome system

“…Moreover, the 18S rDNA signals were located on chromosome pair 13, which is consistent with NORs regions. The location of NORs has been confirmed by FISH using rRNA or rDNA probes in fixed chromosomes of several vertebrates, including amphibians, humans, chimpanzees (Sluisa et al 2012;Hirai 2020), and more recently, fishes (Rubert et al 2011;Milhomem et al 2013;Fernandes et al 2019). In higher eukaryotes, the moderately repetitive ribosomal RNA genes (rDNAs) are arranged in two different families: the nucleolus forming major (45S), and the non-nucleolus forming minor (5S) rDNAs.…”