Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species

Recombination has an evident impact on virus evolution and emergence of new pathotypes, and has generated an immense literature. However, the distribution of phenotypic effects caused by genome-wide random homologous recombination has never been formally investigated. Previous data on the subject ha...

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Main Authors:	Vuillaume, Florence, Thébaud, Gaël, Urbino, Cica, Forfert, Nadège, Granier, Martine, Froissart, Rémy, Blanc, Stéphane, Peterschmitt, Michel
Format:	Online
Language:	English
Published:	Public Library of Science 2011
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3088723/

id	pubmed-3088723
recordtype	oai_dc
spelling	pubmed-30887232011-05-13 Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species Vuillaume, Florence Thébaud, Gaël Urbino, Cica Forfert, Nadège Granier, Martine Froissart, Rémy Blanc, Stéphane Peterschmitt, Michel Research Article Recombination has an evident impact on virus evolution and emergence of new pathotypes, and has generated an immense literature. However, the distribution of phenotypic effects caused by genome-wide random homologous recombination has never been formally investigated. Previous data on the subject have promoted the implicit view that most viral recombinant genomes are likely to be deleterious or lethal if the nucleotide identity of parental sequences is below 90%. We decided to challenge this view by creating a bank of near-random recombinants between two viral species of the genus Begomovirus (Family Geminiviridae) exhibiting 82% nucleotide identity, and by testing infectivity and in planta accumulation of recombinant clones randomly extracted from this bank. The bank was created by DNA-shuffling—a technology initially applied to the random shuffling of individual genes, and here implemented for the first time to shuffle full-length viral genomes. Together with our previously described system allowing the direct cloning of full-length infectious geminivirus genomes, it provided a unique opportunity to generate hundreds of “mosaic” virus genomes, directly testable for infectivity. A subset of 47 randomly chosen recombinants was sequenced, individually inoculated into tomato plants, and compared with the parental viruses. Surprisingly, our results showed that all recombinants were infectious and accumulated at levels comparable or intermediate to that of the parental clones. This indicates that, in our experimental system, despite the fact that the parental genomes differ by nearly 20%, lethal and/or large deleterious effects of recombination are very rare, in striking contrast to the common view that has emerged from previous studies published on other viruses. Public Library of Science 2011-05-05 /pmc/articles/PMC3088723/ /pubmed/21573141 http://dx.doi.org/10.1371/journal.ppat.1002028 Text en Vuillaume et al. http://creativecommons.org/licenses/by/4.0/ 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 properly credited.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Vuillaume, Florence Thébaud, Gaël Urbino, Cica Forfert, Nadège Granier, Martine Froissart, Rémy Blanc, Stéphane Peterschmitt, Michel
spellingShingle	Vuillaume, Florence Thébaud, Gaël Urbino, Cica Forfert, Nadège Granier, Martine Froissart, Rémy Blanc, Stéphane Peterschmitt, Michel Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species
author_facet	Vuillaume, Florence Thébaud, Gaël Urbino, Cica Forfert, Nadège Granier, Martine Froissart, Rémy Blanc, Stéphane Peterschmitt, Michel
author_sort	Vuillaume, Florence
title	Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species
title_short	Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species
title_full	Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species
title_fullStr	Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species
title_full_unstemmed	Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species
title_sort	distribution of the phenotypic effects of random homologous recombination between two virus species
description	Recombination has an evident impact on virus evolution and emergence of new pathotypes, and has generated an immense literature. However, the distribution of phenotypic effects caused by genome-wide random homologous recombination has never been formally investigated. Previous data on the subject have promoted the implicit view that most viral recombinant genomes are likely to be deleterious or lethal if the nucleotide identity of parental sequences is below 90%. We decided to challenge this view by creating a bank of near-random recombinants between two viral species of the genus Begomovirus (Family Geminiviridae) exhibiting 82% nucleotide identity, and by testing infectivity and in planta accumulation of recombinant clones randomly extracted from this bank. The bank was created by DNA-shuffling—a technology initially applied to the random shuffling of individual genes, and here implemented for the first time to shuffle full-length viral genomes. Together with our previously described system allowing the direct cloning of full-length infectious geminivirus genomes, it provided a unique opportunity to generate hundreds of “mosaic” virus genomes, directly testable for infectivity. A subset of 47 randomly chosen recombinants was sequenced, individually inoculated into tomato plants, and compared with the parental viruses. Surprisingly, our results showed that all recombinants were infectious and accumulated at levels comparable or intermediate to that of the parental clones. This indicates that, in our experimental system, despite the fact that the parental genomes differ by nearly 20%, lethal and/or large deleterious effects of recombination are very rare, in striking contrast to the common view that has emerged from previous studies published on other viruses.
publisher	Public Library of Science
publishDate	2011
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3088723/
_version_	1611452125478387712

Distribution of the Phenotypic Effects of Random Homologous Recombination between Two Virus Species

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