Section: Evolutionary Biology
Topic: Evolution, Microbiology, Plant biology

How to survive the mutational meltdown: lessons from plant RNA viruses

10.24072/pcjournal.379 - Peer Community Journal, Volume 4 (2024), article no. e22.

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Muller's ratchet refers to the irreversible accumulation of deleterious mutations in small populations, resulting in a decline in overall fitness. This phenomenon has been extensively observed in experiments involving microorganisms, including bacteriophages and yeast. While the impact of Muller’s ratchet on viruses has been largely studied in bacteriophages and animal RNA viruses, its effects on plant RNA viruses remain poorly documented. Plant RNA viruses give rise to large and diverse populations that undergo significant bottlenecks during the colonization of distant tissues or through vector-mediated horizontal transmission. In this study, we aim to investigate the role of bottleneck size, the maximum population size between consecutive bottlenecks, and the generation of genetic diversity in countering the effects of Muller’s ratchet. We observed three distinct evolutionary outcomes for tobacco etch virus under three different demographic conditions: (i) a decline in fitness following periodic severe bottlenecks in Chenopodium quinoa, (ii) a consistent fitness level with moderate bottlenecks in C. quinoa, and (iii) a net increase in fitness when severe bottlenecks in C. quinoa were alternated with large population expansions in Nicotiana tabacum. By fitting empirical data to an in silico simulation model, we found that initiating a lesion in C. quinoa required only 1-5 virions, and approximately 40 new virions were produced per lesion. These findings demonstrate that Muller's ratchet can be halted not only by increasing the number of founder viruses but also by incorporating phases of exponential growth to large populations between bottlenecks. Such population expansions generate genetic diversity, serving as a buffer against, and potentially even leveraging, the effects of genetic drift.

Published online:
DOI: 10.24072/pcjournal.379
Type: Research article
Lafforgue, Guillaume 1; Lefebvre, Marie 1; Michon, Thierry 1; Elena, Santiago F. 2, 3

1 UMR Biologie du Fruit et Pathologie, INRAE, Université de Bordeaux, Villenave d’Ornon, France
2 Instituto de Biología Integrativa de Sistemas (I2SysBio), Consejo Superior de Investigaciones Científicas – Universitat de València, Paterna, 46980 València, Spain
3 The Santa Fe Institute, Santa Fe, NM 87501, USA
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
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Lafforgue, Guillaume; Lefebvre, Marie; Michon, Thierry; Elena, Santiago F. How to survive the mutational meltdown: lessons from plant RNA viruses. Peer Community Journal, Volume 4 (2024), article  no. e22. doi : 10.24072/pcjournal.379.

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100702

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

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