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Adaptive evolution by recombination is not associated with increased mutation rates in Maize streak virus

BACKGROUND: Single-stranded (ss) DNA viruses in the family Geminiviridae are proving to be very useful in real-time evolution studies. The high mutation rate of geminiviruses and other ssDNA viruses is somewhat mysterious in that their DNA genomes are replicated in host nuclei by high fidelity host...

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Autores principales: Monjane, Adérito L, Pande, Daniel, Lakay, Francisco, Shepherd, Dionne N, van der Walt, Eric, Lefeuvre, Pierre, Lett, Jean-Michel, Varsani, Arvind, Rybicki, Edward P, Martin, Darren P
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3556111/
https://www.ncbi.nlm.nih.gov/pubmed/23268599
http://dx.doi.org/10.1186/1471-2148-12-252
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author Monjane, Adérito L
Pande, Daniel
Lakay, Francisco
Shepherd, Dionne N
van der Walt, Eric
Lefeuvre, Pierre
Lett, Jean-Michel
Varsani, Arvind
Rybicki, Edward P
Martin, Darren P
author_facet Monjane, Adérito L
Pande, Daniel
Lakay, Francisco
Shepherd, Dionne N
van der Walt, Eric
Lefeuvre, Pierre
Lett, Jean-Michel
Varsani, Arvind
Rybicki, Edward P
Martin, Darren P
author_sort Monjane, Adérito L
collection PubMed
description BACKGROUND: Single-stranded (ss) DNA viruses in the family Geminiviridae are proving to be very useful in real-time evolution studies. The high mutation rate of geminiviruses and other ssDNA viruses is somewhat mysterious in that their DNA genomes are replicated in host nuclei by high fidelity host polymerases. Although strand specific mutation biases observed in virus species from the geminivirus genus Mastrevirus indicate that the high mutation rates in viruses in this genus may be due to mutational processes that operate specifically on ssDNA, it is currently unknown whether viruses from other genera display similar strand specific mutation biases. Also, geminivirus genomes frequently recombine with one another and an alternative cause of their high mutation rates could be that the recombination process is either directly mutagenic or produces a selective environment in which the survival of mutants is favoured. To investigate whether there is an association between recombination and increased basal mutation rates or increased degrees of selection favoring the survival of mutations, we compared the mutation dynamics of the MSV-MatA and MSV-VW field isolates of Maize streak virus (MSV; Mastrevirus), with both a laboratory constructed MSV recombinant, and MSV recombinants closely resembling MSV-MatA. To determine whether strand specific mutation biases are a general characteristic of geminivirus evolution we compared mutation spectra arising during these MSV experiments with those arising during similar experiments involving the geminivirus Tomato yellow leaf curl virus (Begomovirus genus). RESULTS: Although both the genomic distribution of mutations and the occurrence of various convergent mutations at specific genomic sites indicated that either mutation hotspots or selection for adaptive mutations might elevate observed mutation rates in MSV, we found no association between recombination and mutation rates. Importantly, when comparing the mutation spectra of MSV and TYLCV we observed similar strand specific mutation biases arising predominantly from imbalances in the complementary mutations G → T: C → A. CONCLUSIONS: While our results suggest that recombination does not strongly influence mutation rates in MSV, they indicate that high geminivirus mutation rates are at least partially attributable to increased susceptibility of all geminivirus genomes to oxidative damage while in a single stranded state.
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spelling pubmed-35561112013-01-31 Adaptive evolution by recombination is not associated with increased mutation rates in Maize streak virus Monjane, Adérito L Pande, Daniel Lakay, Francisco Shepherd, Dionne N van der Walt, Eric Lefeuvre, Pierre Lett, Jean-Michel Varsani, Arvind Rybicki, Edward P Martin, Darren P BMC Evol Biol Research Article BACKGROUND: Single-stranded (ss) DNA viruses in the family Geminiviridae are proving to be very useful in real-time evolution studies. The high mutation rate of geminiviruses and other ssDNA viruses is somewhat mysterious in that their DNA genomes are replicated in host nuclei by high fidelity host polymerases. Although strand specific mutation biases observed in virus species from the geminivirus genus Mastrevirus indicate that the high mutation rates in viruses in this genus may be due to mutational processes that operate specifically on ssDNA, it is currently unknown whether viruses from other genera display similar strand specific mutation biases. Also, geminivirus genomes frequently recombine with one another and an alternative cause of their high mutation rates could be that the recombination process is either directly mutagenic or produces a selective environment in which the survival of mutants is favoured. To investigate whether there is an association between recombination and increased basal mutation rates or increased degrees of selection favoring the survival of mutations, we compared the mutation dynamics of the MSV-MatA and MSV-VW field isolates of Maize streak virus (MSV; Mastrevirus), with both a laboratory constructed MSV recombinant, and MSV recombinants closely resembling MSV-MatA. To determine whether strand specific mutation biases are a general characteristic of geminivirus evolution we compared mutation spectra arising during these MSV experiments with those arising during similar experiments involving the geminivirus Tomato yellow leaf curl virus (Begomovirus genus). RESULTS: Although both the genomic distribution of mutations and the occurrence of various convergent mutations at specific genomic sites indicated that either mutation hotspots or selection for adaptive mutations might elevate observed mutation rates in MSV, we found no association between recombination and mutation rates. Importantly, when comparing the mutation spectra of MSV and TYLCV we observed similar strand specific mutation biases arising predominantly from imbalances in the complementary mutations G → T: C → A. CONCLUSIONS: While our results suggest that recombination does not strongly influence mutation rates in MSV, they indicate that high geminivirus mutation rates are at least partially attributable to increased susceptibility of all geminivirus genomes to oxidative damage while in a single stranded state. BioMed Central 2012-12-27 /pmc/articles/PMC3556111/ /pubmed/23268599 http://dx.doi.org/10.1186/1471-2148-12-252 Text en Copyright ©2012 Monjane et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Monjane, Adérito L
Pande, Daniel
Lakay, Francisco
Shepherd, Dionne N
van der Walt, Eric
Lefeuvre, Pierre
Lett, Jean-Michel
Varsani, Arvind
Rybicki, Edward P
Martin, Darren P
Adaptive evolution by recombination is not associated with increased mutation rates in Maize streak virus
title Adaptive evolution by recombination is not associated with increased mutation rates in Maize streak virus
title_full Adaptive evolution by recombination is not associated with increased mutation rates in Maize streak virus
title_fullStr Adaptive evolution by recombination is not associated with increased mutation rates in Maize streak virus
title_full_unstemmed Adaptive evolution by recombination is not associated with increased mutation rates in Maize streak virus
title_short Adaptive evolution by recombination is not associated with increased mutation rates in Maize streak virus
title_sort adaptive evolution by recombination is not associated with increased mutation rates in maize streak virus
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3556111/
https://www.ncbi.nlm.nih.gov/pubmed/23268599
http://dx.doi.org/10.1186/1471-2148-12-252
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