Brave new RNA world(s): from prebiotic chemistry to gene regulation and RNA technology

RNA has long provided a plausible route by which heredity and catalysis could become linked in early evolution, and the same chemical versatility helps explain why RNA remains central to origin-of-life research, modern cell biology, and biotechnology. This review adopts a plural framing of RNA worlds to connect three regimes: a primordial RNA world constrained by geochemistry, a contemporary RNA world in which RNAs contribute to catalysis and regulation in cells, and an applied RNA world in which RNA is engineered as a programmable tool. Across these regimes, a common logic emerges from the mapping of sequence to structure to function under explicit constraints. In early evolution, cycling, interfaces, and confinement can generate heterogeneous oligomer pools and bias their persistence, whereas the transition toward Darwinian dynamics depends on copying fidelity, strand dynamics, and compartment coupled population structure. In cells and applications, noncoding RNA networks, RNA modifications, and RNA-guided targeting implement specificity in chemically complex environments, while laboratory selection and design must also confront constraints imposed by stability, delivery, and immune sensing. Across contexts, fitness landscapes and tradeoffs between peak performance and robustness provide experimental benchmarks and practical design principles for RNA function.