Tertiary folding of the 160-nt P4-P6 domain of the
Tetrahymena group I intron RNA involves burying of
substantial surface area, providing a model for the folding
of other large RNA domains involved in catalysis. Stopped-flow
fluorescence was used to monitor the Mg2+-induced
tertiary folding of pyrene-labeled P4-P6. At 35 °C with
[Mg2+] ≈ 10 mM, P4-P6 folds on the tens
of milliseconds timescale with kobs
= 15–31 s−1. From these values, an
activation free energy ΔG[Dagger] of
∼8–16 kcal/mol is calculated, where the large
range for ΔG[Dagger] arises from uncertainty
in the pre-exponential factor relating kobs
and ΔG[Dagger]. The folding rates of six mutant
P4-P6 RNAs were measured and found to be similar to that of the
wild-type RNA, in spite of significant thermodynamic destabilization or
stabilization. The ratios of the kinetic and thermodynamic free energy
changes Φ = ΔΔG[Dagger]/ΔΔG°′
are ≈0, implying a folding transition state in which most of the
native-state tertiary contacts are not yet formed (an early folding
transition state). The kobs depends on
the Mg2+ concentration, and the initial slope of
kobs versus [Mg2+]
suggests that only ∼1 Mg2+ ion is bound in the
rate-limiting folding step. This is consistent with an early folding
transition state, because folded P4-P6 binds many Mg2+ ions.
The observation of a substantial ΔG[Dagger] despite an
early folding transition state suggests that a simple two-state folding
diagram for Mg2+-induced P4-P6 folding is incomplete.
Our kinetic data are some of the first to provide quantitative
values for an activation barrier and location of a transition
state for tertiary folding of an RNA domain.