Parsimonious scenario for the emergence of viroid-like repliconsde novo

Abstract

Viroids are small, non-coding, circular RNA molecules that infect plants. Different 1 hypotheses for their evolutionary origin have been put forward, such as an early emergence in a 2 precellular RNA World or several de novo independent evolutionary origins in plants. Here we discuss 3 the plausibility of de novo emergence of viroid-like replicons by giving theoretical support to the 4 likelihood of different steps along a parsimonious evolutionary pathway. While Avsunviroidae-like 5 structures are relatively easy to obtain through evolution of a population of random RNA sequences of 6 fixed length, rod-like structures typical of Pospiviroidae are difficult to fix. Using different quantitative 7 approaches, we evaluate the likelihood that RNA sequences fold into a rod-like structure and bear 8 specific sequence motifs facilitating interactions with other molecules, e.g. RNA polymerases, RNases 9 and ligases. By means of numerical simulations, we show that circular RNA replicons analogous 10 to Pospiviroidae emerge if evolution is seeded with minimal circular RNAs that grow through the 11 gradual addition of nucleotides. Further, these rod-like replicons often maintain their structure if 12 independent functional modules are acquired that impose selective constraints. The evolutionary 13 scenario we propose here is consistent with the structural and biochemical properties of viroids 14 described to date. 15