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Parsimonious Scenario for the Emergence of Viroid-Like Replicons De Novo

1
Biosciences, College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4QD, UK
2
Grupo Interdisciplinar de Sistemas Complejos (GISC), Madrid, Spain
3
Instituto de Biología Integrativa de Sistemas (I2SysBio), CSIC-Universitat de València, Paterna, 46980 València, Spain
4
The Santa Fe Institute, Santa Fe, NM 87501, USA
5
Departamento de Matemáticas, Universidad Carlos III de Madrid, 28911 Leganés, Spain
6
Instituto de Biocomputación y Física de Sistemas Complejos (BiFi), Universidad de Zaragoza, 50018 Zaragoza, Spain
7
Institute of Financial Big Data (IFiBiD), Universidad Carlos III de Madrid–Banco de Santander, 28903 Getafe, Spain
8
National Biotechnology Centre (CSIC), 28049 Madrid, Spain
*
Author to whom correspondence should be addressed.
Viruses 2019, 11(5), 425; https://doi.org/10.3390/v11050425
Received: 29 March 2019 / Revised: 30 April 2019 / Accepted: 2 May 2019 / Published: 9 May 2019
(This article belongs to the Special Issue Viroid-2018: International Conference on Viroids and Viroid-Like RNAs)
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Abstract

Viroids are small, non-coding, circular RNA molecules that infect plants. Different hypotheses for their evolutionary origin have been put forward, such as an early emergence in a precellular RNA World or several de novo independent evolutionary origins in plants. Here, we discuss the plausibility of de novo emergence of viroid-like replicons by giving theoretical support to the likelihood of different steps along a parsimonious evolutionary pathway. While Avsunviroidae-like structures are relatively easy to obtain through evolution of a population of random RNA sequences of fixed length, rod-like structures typical of Pospiviroidae are difficult to fix. Using different quantitative approaches, we evaluated the likelihood that RNA sequences fold into a rod-like structure and bear specific sequence motifs facilitating interactions with other molecules, e.g., RNA polymerases, RNases, and ligases. By means of numerical simulations, we show that circular RNA replicons analogous to Pospiviroidae emerge if evolution is seeded with minimal circular RNAs that grow through the gradual addition of nucleotides. Further, these rod-like replicons often maintain their structure if independent functional modules are acquired that impose selective constraints. The evolutionary scenario we propose here is consistent with the structural and biochemical properties of viroids described to date. View Full-Text
Keywords: viroid; RNA secondary structure; population dynamics; computational simulations; structure enumeration; simple replicators; modular evolution viroid; RNA secondary structure; population dynamics; computational simulations; structure enumeration; simple replicators; modular evolution
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Catalán, P.; Elena, S.F.; Cuesta, J.A.; Manrubia, S. Parsimonious Scenario for the Emergence of Viroid-Like Replicons De Novo. Viruses 2019, 11, 425.

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