In diverse bacteria, RNA chaperones play a key role in the post-transcriptional control of gene expression. The RNA-binding protein Hfq and other RNA chaperones facilitate the action of small regulatory RNAs in post-transcriptional control processes of many bacterial species. A model will be described proposing how Hfq works in conjunction with some regulatory RNAs to guide ribonuclease machinery for action on targeted transcripts. Hfq can also form regulatory assemblies directly on mRNAs, and in the pathogen Pseudomonas aeruginosa, the chaperone forms higher-order assemblies on control regions of different target mRNAs with its partner protein Crc. Our results show that these assemblies have mRNA-specific quaternary architectures resulting from the combination of multivalent protein-protein interfaces and recognition of patterns in the RNA sequence. The structural polymorphism of the ribonucleoprotein assemblies enables selective translational repression of hundreds of different target mRNAs. This system suggests how highly complex regulatory pathways can evolve and be rewired with a simple economy of protein components.