Nucleolar Dominance

Abstract

Nucleolar dominance is an epigenetic phenomenon that describes the formation of nucleoli, the sites of ribosome synthesis, at specific loci of chromosomes inherited from only one progenitor of a genetic hybrid. These loci, known as nucleolus organiser regions (NORs), consist of ribosomal RNA (rRNA) genes that are repeated in hundreds of copies. The molecular basis for nucleolar dominance is the silencing of rRNA genes at some NORs, but not others, a manifestation of a dosage control system that regulates the number of active rRNA genes depending on the cellular demand for ribosomes and protein synthesis. rRNA gene silencing involves cytosine methylation, histone postā€translational modifications and noncoding RNAs, but the precise mechanisms by which specific sets of rRNA genes are chosen for silencing are unclear.

Key Concepts:

  • In genetic hybrids, genes inherited from the different parents, or progenitors, can be differentially expressed.

  • Nucleolar dominance in genetic hybrids involves the selective silencing of ribosomal RNA gene loci that span millions of base pairs on eukaryotic chromosomes.

  • Ribosomal RNA gene silencing involves epigenetic modifications of chromosomal chromatin, including cytosine methylation and repressive histone postā€translational modifications.

  • Nucleolar dominance is not a regulatory phenomenon unique to hybrids but a manifestation of a dosage control system that operates in all eukaryotes to control the number of active rRNA genes.

  • Nucleolar dominance may result from inactivation of entire nucleolus organiser regions (NORs) rather than silencing decisions made one rRNA gene at a time.

Keywords: chromatin modification; DNA methylation; epigenetic phenomena; gene silencing; nucleolus organiser region; ribosomal RNA ; RNA polymerase I

Figure 1.

Cartoon depicting the discovery of nucleolar dominance based on observations of metaphase chromosomes in pure species and interspecific hybrids. Haploid chromosome sets of two progenitor species, each with three chromosomes, and their diploid hybrid are depicted. Species A and B each have a chromosome with an NOR that forms a secondary constriction at metaphase as a consequence of rRNA gene transcription during the preceding interphase and persistent binding of transcription factors that interfere with chromosome condensation. In hybrids, secondary constrictions observed only on the NOR‐bearing chromosome(s) of one progenitor reflect the differential expression of rRNA genes at different NORs.

Figure 2.

Relationship between the nucleolus, NOR and rRNA gene repeats. The nucleolus fully forms during interphase, but its remnant persists in association with secondary constrictions at NORs during metaphase. NORs are the chromosomal loci where the rRNA genes transcribed by DNA‐dependent RNA polymerase I (Pol I) are tandemly repeated in hundreds of copies. Each Pol I transcription unit includes the 18S, 5.8S and 25–28S rRNA sequences assembled within the ribosomes, and is separated from the next gene by an intergenic spacer that includes the promoter and other regulatory elements important for transcriptional regulation.

Figure 3.

Molecular attributes of the rRNA gene ‘on’ and ‘off’ states in the plant genus, Arabidopsis. Silencing in the allotetraploid A. suecica involves components of the RNA‐directed DNA methylation pathway and repressive histone post‐translational modifications typical of condensed heterochromatin. By contrast, the active state is characterised by histone post‐translational modifications typical of decondensed euchromatin and cytosine hypomethylation.

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Further Reading

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Pikaard, Craig S(Jan 2014) Nucleolar Dominance. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0005976.pub2]