The Relationship between the (In-)Stability of NORs and Their Chromosomal Location: The Example of Cercopithecidae and a Short Review of Other Primates

Abstract

Amongst Cercopithecidae, the species of the Cercopithecini tribe underwent a very active chromosome evolution, principally by fissions, which increased their chromosome number up to 72. In contrast, all the species of Papionini have fairly similar karyotypes with 42 chromosomes. In animals, nucleolus organizer regions (NORs) are generally considered as instable structures, which frequently vary in size, number, and location at both infra- and interspecific levels. Although in Cercopithecinae the NORs, involved in breaks, exchanges, and translocations, behave like fragile sites in somatic cells, their number and location appear to be very stable between species. Fluorescence in situ hybridization of a 28S rDNA probe on metaphase chromosomes displayed a unique interstitial location in either an acrocentric pair (in 12 species of Cercopithecini) or a metacentric pair (in 6 species of Papionini). A non-exhaustive survey of literature data on NOR location in other primates shows that numerical variations of the NORs principally depend on their location: most multiple NORs are in terminal positions, while almost all unique NORs are in interstitial positions. We propose that this correlation is the consequence of the selection against gametic imbalances involving the chromosomal material distal to the NORs, which is effective when they are interstitially, but not terminally, located. Thus, the consequences of the interstitial NOR instability for reproduction are essentially limited to their size variations, as observed in Cercopithecidae.

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

“…Based on rDNA mapping data in fish karyotypes, Martins and Wasko (2004) proposed that translocations are more likely to occur in telomeric regions because of their proximity within the interphase nucleus, which originates from the ordering of chromosomes according to Rabl's model. Effects due to the location of ribosomal genes in relation to their dispersion in the karyotype were also observed in Coleoptera (Dutrillaux et al ., 2016) and primates (Gerbault‐Seureau et al ., 2017). These authors argued that translocations in the interstitial position could result in abnormal meiosis and, therefore, unbalanced gametes.…”

The Case of X and Y Localization of Nucleolus Organizer Regions (NORs) in Tragulus javanicus (Cetartiodactyla, Mammalia)

“…The clustered NOR structure also might contribute to its instability, facilitated by an illegitimate recombination between non-homologous chromosomes. It results in variation of the number of sequences per NOR and the localization on various chromosomes even in closely related species [ 7 ].…”

“…These ribosomal DNA sequences exhibit a high degree of conservation across animals. In contrast with sequence conservation, rDNA clusters are characterized by variation in copy-number [ 3 ], rDNA content of NORs between individuals [ 4 ], between the cells of one individual [ 5 ], and variable localization in different animal species [ 6 , 7 ]. The variation in the number of transcriptionally active NORs can occur even between the cells and tissues of one individual [ 8 ].…”

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

“…By comparison, the Old World monkeys have interstitial (INTRA) rDNA arrays, and these can be located either in metacentric (m) chromosomes or acrocentric (a) chromosomes (INTRAm or INTRAa) ( Figure 1). Interestingly, the monkey species examined to date do not show the genomic dispersion of rDNA arrays [45]. The interstitial rDNA regions that were observed in INTRAm and INTRAa hardly make association between each other because proximal regions of chromosome arms cannot easily make contact with other regions (unlike the telomere-telomere associations in terminal regions), though self-duplication at the locus seems to arise [46].…”