Ultrastructural analysis of polytene chromatin of Drosophila melanogaster reveals clusters of tightly linked co-expressed genes

Abstract

Patterns of gene activity on individual chromatids of polytene chromosomes of Drosophila melanogaster white prepupae were ultrastructurally characterized by electron microscopy. The band-interband structure of salivary gland polytene chromosomes is lost when they are dispersed in a low ionic strength detergent solution. Morphologically similar, active genes in close proximity to one another were seen in dispersed white prepupal chromatin. The arrays of genes almost certainly represent sister copies of the same locus. Although lateral register between gene copies on multiple strands was not maintained, analysis of sister transcriptional units of unknown identity was achieved at the periphery of the chromatin arrays. Juxtaposed genes with divergent transcriptional polarity were prevalent. The morphology, size and transcriptional polarity of multiple copies of short, tandemly organized, RNA polymerase dense, co-expressed gene clusters is reported. One highly transcriptionally active region, designated the white prepupal locus (WPP locus), composed of a co-expressed tandem cluster of ten genes within an approximately 50 kb region was analyzed on six separate chromatids. The transcriptional map suggests that the pattern of gene activity for at least one gene within the cluster may not be identical on all homologous strands. The survey of active polytene genes provides ultrastructural correlation with previous molecular data that demonstrate tight linkage of certain developmentally co-regulated Drosophila genes. Our findings are discussed in relation to Drosophila gene organization, clustering, and regulation of gene expression.