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Accurate knowledge of RNA hybridization is essential for understanding RNAstructure and function. Here we mechanically unzip and rezip a 2-kbp RNAhairpin and derive the 10 nearest-neighbor base pair (NNBP) RNA free energiesin sodium and magnesium with 0.1 kcal/mol precision using optical tweezers.Notably, force-distance curves (FDCs) exhibit strong irreversible effects withhysteresis and several intermediates, precluding the extraction of the NNBPenergies with currently available methods. The combination of a suitable RNAsynthesis with a tailored pulling protocol allowed us to obtain the fullyreversible FDCs necessary to derive the NNBP energies. We demonstrate theequivalence of sodium and magnesium free-energy salt corrections at the levelof individual NNBP. To characterize the irreversibility of theunzipping-rezipping process, we introduce a barrier energy landscape of thestem-loop structures forming along the complementary strands, which competeagainst the formation of the native hairpin. This landscape correlates with thehysteresis observed along the FDCs. RNA sequence analysis shows that basestacking and base pairing stabilize the stem-loops that kinetically trap thelong-lived intermediates observed in the FDC. Stem-loops formation appears as ageneral mechanism to explain a wide range of behaviors observed in RNA folding.

Stem-loop formation drives RNA folding in mechanical unzipping experiments