The driving force for molecular evolution of translation

Abstract

It is widely argued that protein synthesis evolved out of an RNA world, in which catalytic and other biological functions now carried out by proteins were performed by RNAs. However, it is not clear what selective advantage would have provided the driving force for evolution of a primitive translation apparatus, because of the unlikelihood that rudimentary polypeptides would have contributed sufficiently useful biological functions. Here, I suggest that the availability of even simple peptides could have significantly enlarged the otherwise limited structure space of RNA. In other words, translation initially evolved not to create a protein world, but to extend the structural, and therefore the functional, capabilities of the RNA world. Observed examples of substantial structural rearrangements in RNA that are induced by binding of peptides and other small molecules support this possibility.

FIGURE 1.

The 5.5 Å crystal structure of the Thermus thermophilus 70S ribosome (Yusupov et al. 2001). The 30S subunit (left) contains 16S rRNA (cyan) and 19 different ribosomal proteins (dark blue). The 50S subunit (right) contains 23S rRNA (gray), 5S rRNA (gray-blue), and more than 30 different proteins (magenta).

FIGURE 2.

The Tat–TAR interaction: An example of ligand-induced structural rearrangement of RNA. (A) Secondary structure and NMR solution structures of (B) free TAR RNA and (C) a complex of argininamide bound to TAR RNA (Puglisi et al. 1992), rendered as space-filling van der Waals surfaces. The UCU bulge loop is shown in dark blue, and the bound argininamide ligand in orange. The structure of TAR RNA in the argininamide complex is the same as in the TAR–peptide complex (Puglisi et al. 1992), but the K_d for the latter is five to six orders of magnitude lower (Tao and Frankel 1992).