The differential expression of ribosomal RNA genes

Abstract

Ribosomal RNA genes are localized at chromosomal sites termed nucleolus organizers because nucleoli form around transcribed ribosomal RNA genes. The relative activities of arrays of ribosomal RNA genes can be estimated cytologically by comparing the sizes of nucleoli in the same cell. Also, active nucleolus organizers give rise to visible constrictions in metaphase chromosomes whereas inactive nucleolus organizers do not. With these assays the differential expression of nucleolus organizers and ribosomal RNA genes has been observed frequently, especially in interspecies hybrids. Studies on wheat have revealed that differences in gene expression are associated with differences in chromatin structure and cytosine methylation. Active loci have higher proportions of their genes decondensed and accessible to proteins and also higher proportions with a non-methylated cytosine residue at a CCGG site in the region of the promoter. Short, related sequences with dyad symmetry have been noted between —140 and —70 base pairs from where transcription is initiated in a wheat ribosomal RNA gene. Similar sequences are reiterated upstream of the promoter over 2000 base pairs. From comparison of this gene structure with that ofXenopusribosomal RNA genes it can be concluded that these short sequences are likely to act as enhancers of transcription by binding to specific regulatory proteins that function to stimulate the attachment of polymerase I complexes. Differential expression of arrays of ribosomal RNA genes results when genes have different numbers of enhancer repeats or a higher affinity for the regulatory protein(s). This model to explain differential gene expression and the origins of genetic variation affecting ribosomal RNA gene expression are discussed.