Transperons: RNA operons as effectors of coordinated gene expression in eukaryotes

Coordinated gene expression allows spatiotemporal control of cellular processes and is achieved by the cotranscription/translation of functionally related genes/proteins. Prokaryotes evolved polycistronic messages (operons) to confer expression from a single promoter to efficiently cotranslate proteins functioning on the same pathway. Yet, despite having far greater diversity (e.g., gene number, distribution, modes of expression), eukaryotic cells employ individual promoters and monocistronic messages. Although gene expression is modular, it does not account for how eukaryotes achieve coordinated localized translation. The RNA operon theory states that mRNAs derived from different chromosomes assemble into ribonucleoprotein particles (RNPs) that act as functional operons to generate protein cohorts upon cotranslation. Work in yeast has now validated this theory and shown that intergenic associations and noncanonical histone functions create pathway-specific RNA operons (transperons) that regulate cell physiology. Herein the involvement of chromatin organization in transperon formation and programmed gene coexpression is discussed. RNA operons (transperons) in eukaryotes act similarly to DNA operons in prokaryotes and regulate coordinated gene expression.Transperons are monocistronic messages containing shared cis motifs that undergo assembly in trans upon transcription to form pathway-specific ribonucleoprotein complexes.Transcription factor coalescence into phase-separated aggregates may confer intragenic and intergenic chromatin interactions leading to gene coupling and coexpression.Gene coupling allows for the formation of pathway-specific RNA operons upon transcription and requires histone H4 function.Transperons may be conserved in evolution and thus constitute a novel means for cotranslational control in eukaryotes.