Within-host Evolution of Segments Ratio for the Tripartite Genome of Alfalfa Mosaic Virus

Abstract The existence of multipartite viruses is an intriguing mystery in evolutionary virology. Several hypotheses suggest benefits that should outweigh the costs of a reduced transmission efficiency and of segregation of coadapted genes associated with encapsidating each segment into a different...

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Main Authors: Beilei Wu, Mark P. Zwart, Jesús A. Sánchez-Navarro, Santiago F. Elena
Format: Article
Language:English
Published: Nature Portfolio 2017-07-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-017-05335-8
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author Beilei Wu
Mark P. Zwart
Jesús A. Sánchez-Navarro
Santiago F. Elena
author_facet Beilei Wu
Mark P. Zwart
Jesús A. Sánchez-Navarro
Santiago F. Elena
author_sort Beilei Wu
collection DOAJ
description Abstract The existence of multipartite viruses is an intriguing mystery in evolutionary virology. Several hypotheses suggest benefits that should outweigh the costs of a reduced transmission efficiency and of segregation of coadapted genes associated with encapsidating each segment into a different particle. Advantages range from increasing genome size despite high mutation rates, faster replication, more efficient selection resulting from reassortment during mixed infections, better regulation of gene expression, or enhanced virion stability and cell-to-cell movement. However, support for these hypotheses is scarce. Here we report experiments testing whether an evolutionary stable equilibrium exists for the three genomic RNAs of Alfalfa mosaic virus (AMV). Starting infections with different segment combinations, we found that the relative abundance of each segment evolves towards a constant ratio. Population genetic analyses show that the segment ratio at this equilibrium is determined by frequency-dependent selection. Replication of RNAs 1 and 2 was coupled and collaborative, whereas the replication of RNA 3 interfered with the replication of the other two. We found that the equilibrium solution is slightly different for the total amounts of RNA produced and encapsidated, suggesting that competition exists between all RNAs during encapsidation. Finally, we found that the observed equilibrium appears to be host-species dependent.
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spelling doaj.art-8815b20fcfeb4208bfe3860488a520ac2022-12-21T20:31:25ZengNature PortfolioScientific Reports2045-23222017-07-017111510.1038/s41598-017-05335-8Within-host Evolution of Segments Ratio for the Tripartite Genome of Alfalfa Mosaic VirusBeilei Wu0Mark P. Zwart1Jesús A. Sánchez-Navarro2Santiago F. Elena3Instituto de Biología Molecular y Celular de Plantas (IBMCP), Consejo Superior de Investigaciones Científicas-Universidad Politécnica de ValenciaInstituto de Biología Molecular y Celular de Plantas (IBMCP), Consejo Superior de Investigaciones Científicas-Universidad Politécnica de ValenciaInstituto de Biología Molecular y Celular de Plantas (IBMCP), Consejo Superior de Investigaciones Científicas-Universidad Politécnica de ValenciaInstituto de Biología Molecular y Celular de Plantas (IBMCP), Consejo Superior de Investigaciones Científicas-Universidad Politécnica de ValenciaAbstract The existence of multipartite viruses is an intriguing mystery in evolutionary virology. Several hypotheses suggest benefits that should outweigh the costs of a reduced transmission efficiency and of segregation of coadapted genes associated with encapsidating each segment into a different particle. Advantages range from increasing genome size despite high mutation rates, faster replication, more efficient selection resulting from reassortment during mixed infections, better regulation of gene expression, or enhanced virion stability and cell-to-cell movement. However, support for these hypotheses is scarce. Here we report experiments testing whether an evolutionary stable equilibrium exists for the three genomic RNAs of Alfalfa mosaic virus (AMV). Starting infections with different segment combinations, we found that the relative abundance of each segment evolves towards a constant ratio. Population genetic analyses show that the segment ratio at this equilibrium is determined by frequency-dependent selection. Replication of RNAs 1 and 2 was coupled and collaborative, whereas the replication of RNA 3 interfered with the replication of the other two. We found that the equilibrium solution is slightly different for the total amounts of RNA produced and encapsidated, suggesting that competition exists between all RNAs during encapsidation. Finally, we found that the observed equilibrium appears to be host-species dependent.https://doi.org/10.1038/s41598-017-05335-8
spellingShingle Beilei Wu
Mark P. Zwart
Jesús A. Sánchez-Navarro
Santiago F. Elena
Within-host Evolution of Segments Ratio for the Tripartite Genome of Alfalfa Mosaic Virus
Scientific Reports
title Within-host Evolution of Segments Ratio for the Tripartite Genome of Alfalfa Mosaic Virus
title_full Within-host Evolution of Segments Ratio for the Tripartite Genome of Alfalfa Mosaic Virus
title_fullStr Within-host Evolution of Segments Ratio for the Tripartite Genome of Alfalfa Mosaic Virus
title_full_unstemmed Within-host Evolution of Segments Ratio for the Tripartite Genome of Alfalfa Mosaic Virus
title_short Within-host Evolution of Segments Ratio for the Tripartite Genome of Alfalfa Mosaic Virus
title_sort within host evolution of segments ratio for the tripartite genome of alfalfa mosaic virus
url https://doi.org/10.1038/s41598-017-05335-8
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