Nuclear speckle-associated perispeckle networks partition active chromatin into gene expression niches

A subset of genes, reproducibly positioned adjacent to nuclear speckles (NS), amplify their expression only with NS contact. However, genome-wide gene expression differences inversely correlate with differences in NS distance. To resolve this paradox, we hypothesized the existence of additional "niches" away from, but spatially correlated with NS, that would enhance gene expression of adjacent genes. Analyzing NS-related proteins led us to identify two dynamic multi-protein perispeckle patterns extending outwards from NS. Highly active chromosome regions weakly associated with NS show close, NS-independent association with these perispeckle patterns. These perispeckle patterns persist after NS are eliminated. Whereas NS-associated genes are downregulated upon NS depletion, perispeckle-pattern associated genes are upregulated. Transcripts expressed from model intron-containing versus intronless genes associate differentially with these two patterns. We suggest that the interchromatin space is partitioned into additional gene expression "niches", surrounding and extending from NS, that may be involved in mRNA and gene dynamics.