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Current models for the folding of the human genome see a hierarchy stretchingdown from chromosome territories, through A/B compartments and TADs(topologically-associating domains), to contact domains stabilized by cohesinand CTCF. However, molecular mechanisms underlying this folding, and the wayfolding affects transcriptional activity, remain obscure. Here we reviewphysical principles driving proteins bound to long polymers into clusterssurrounded by loops, and present a parsimonious yet comprehensive model for theway the organization determines function. We argue that clusters of active RNApolymerases and their transcription factors are major architectural features;then, contact domains, TADs, and compartments just reflect one or more loopsand clusters. We suggest tethering a gene close to a cluster containingappropriate factors -- a transcription factory -- increases the firingfrequency, and offer solutions to many current puzzles concerning the actionsof enhancers, super-enhancers, boundaries, and eQTLs (expression quantitativetrait loci). As a result, the activity of any gene is directly influenced bythe activity of other transcription units around it in 3D space, and this issupported by Brownian-dynamics simulations of transcription factors binding tocognate sites on long polymers.

Transcription-driven genome organization: a model for chromosome structure and the regulation of gene expression tested through simulations