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Published March 2011 | Published + Supplemental Material
Journal Article Open

Viral Genome Segmentation Can Result from a Trade-Off between Genetic Content and Particle Stability

Abstract

The evolutionary benefit of viral genome segmentation is a classical, yet unsolved question in evolutionary biology and RNA genetics. Theoretical studies anticipated that replication of shorter RNA segments could provide a replicative advantage over standard size genomes. However, this question has remained elusive to experimentalists because of the lack of a proper viral model system. Here we present a study with a stable segmented bipartite RNA virus and its ancestor non-segmented counterpart, in an identical genomic nucleotide sequence context. Results of RNA replication, protein expression, competition experiments, and inactivation of infectious particles point to a non-replicative trait, the particle stability, as the main driver of fitness gain of segmented genomes. Accordingly, measurements of the volume occupation of the genome inside viral capsids indicate that packaging shorter genomes involves a relaxation of the packaging density that is energetically favourable. The empirical observations are used to design a computational model that predicts the existence of a critical multiplicity of infection for domination of segmented over standard types. Our experiments suggest that viral segmented genomes may have arisen as a molecular solution for the trade-off between genome length and particle stability. Genome segmentation allows maximizing the genetic content without the detrimental effect in stability derived from incresing genome length.

Additional Information

© 2011 Ojosnegros et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received September 3, 2010; Accepted February 16, 2011; Published March 17, 2011. Editor: Harmit S. Malik, Fred Hutchinson Cancer Research Center, United States of America. Funding: Work at Centro de Biologia Molecular Severo Ochoa was supported by grants BFU2006-00863 from MEC, BFU2008-02816/BMC from MCI, 36558/06 from FIPSE, and Fundacion R. Areces. CIBERehd is funded by Instituto de Salud Carlos III. SO was supported by a predoctoral fellowship from the MEC. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank David Baltimore for the critical reading of the manuscript. We also thank M. Dávila and A. I. de Avila for technical assistance. Author Contributions: Conceived and designed the experiments: SO CE SCM ED. Performed the experiments: SO CP MGM. Analyzed the data: SO JGA CE SCM CP MGM ED. Contributed reagents/materials/analysis tools: JGA AA. Wrote the paper: SO SCM MGM ED.

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Published - Ojosnegros2011p13716Plos_Genet.pdf

Supplemental Material - FigureS1.eps

Supplemental Material - FigureS2.eps

Supplemental Material - TextS1.doc

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August 19, 2023
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