Recombination hotspots and host susceptibility modulate the adaptive value of recombination during maize streak virus evolution

<p>Abstract</p> <p>Background</p> <p><it>Maize streak virus </it>-strain A (MSV-A; Genus <it>Mastrevirus</it>, Family <it>Geminiviridae</it>), the maize-adapted strain of MSV that causes maize streak disease throughout sub-Saharan Afr...

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Main Authors: Monjane Adérito L, van der Walt Eric, Varsani Arvind, Rybicki Edward P, Martin Darren P
Format: Article
Language:English
Published: BMC 2011-12-01
Series:BMC Evolutionary Biology
Online Access:http://www.biomedcentral.com/1471-2148/11/350
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author Monjane Adérito L
van der Walt Eric
Varsani Arvind
Rybicki Edward P
Martin Darren P
author_facet Monjane Adérito L
van der Walt Eric
Varsani Arvind
Rybicki Edward P
Martin Darren P
author_sort Monjane Adérito L
collection DOAJ
description <p>Abstract</p> <p>Background</p> <p><it>Maize streak virus </it>-strain A (MSV-A; Genus <it>Mastrevirus</it>, Family <it>Geminiviridae</it>), the maize-adapted strain of MSV that causes maize streak disease throughout sub-Saharan Africa, probably arose between 100 and 200 years ago via homologous recombination between two MSV strains adapted to wild grasses. MSV recombination experiments and analyses of natural MSV recombination patterns have revealed that this recombination event entailed the exchange of the movement protein - coat protein gene cassette, bounded by the two genomic regions most prone to recombination in mastrevirus genomes; the first surrounding the virion-strand origin of replication, and the second around the interface between the coat protein gene and the short intergenic region. Therefore, aside from the likely adaptive advantages presented by a modular exchange of this cassette, these specific breakpoints may have been largely predetermined by the underlying mechanisms of mastrevirus recombination. To investigate this hypothesis, we constructed artificial, low-fitness, reciprocal chimaeric MSV genomes using alternating genomic segments from two MSV strains; a grass-adapted MSV-B, and a maize-adapted MSV-A. Between them, each pair of reciprocal chimaeric genomes represented all of the genetic material required to reconstruct - via recombination - the highly maize-adapted MSV-A genotype, MSV-MatA. We then co-infected a selection of differentially MSV-resistant maize genotypes with pairs of reciprocal chimaeras to determine the efficiency with which recombination would give rise to high-fitness progeny genomes resembling MSV-MatA.</p> <p>Results</p> <p>Recombinants resembling MSV-MatA invariably arose in all of our experiments. However, the accuracy and efficiency with which the MSV-MatA genotype was recovered across all replicates of each experiment depended on the MSV susceptibility of the maize genotypes used and the precise positions - in relation to known recombination hotspots - of the breakpoints required to re-create MSV-MatA. Although the MSV-sensitive maize genotype gave rise to the greatest variety of recombinants, the measured fitness of each of these recombinants correlated with their similarity to MSV-MatA.</p> <p>Conclusions</p> <p>The mechanistic predispositions of different MSV genomic regions to recombination can strongly influence the accessibility of high-fitness MSV recombinants. The frequency with which the fittest recombinant MSV genomes arise also correlates directly with the escalating selection pressures imposed by increasingly MSV-resistant maize hosts.</p>
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spelling doaj.art-45a269f8de9d4e4faee696897acc99102022-12-21T21:05:07ZengBMCBMC Evolutionary Biology1471-21482011-12-0111135010.1186/1471-2148-11-350Recombination hotspots and host susceptibility modulate the adaptive value of recombination during maize streak virus evolutionMonjane Adérito Lvan der Walt EricVarsani ArvindRybicki Edward PMartin Darren P<p>Abstract</p> <p>Background</p> <p><it>Maize streak virus </it>-strain A (MSV-A; Genus <it>Mastrevirus</it>, Family <it>Geminiviridae</it>), the maize-adapted strain of MSV that causes maize streak disease throughout sub-Saharan Africa, probably arose between 100 and 200 years ago via homologous recombination between two MSV strains adapted to wild grasses. MSV recombination experiments and analyses of natural MSV recombination patterns have revealed that this recombination event entailed the exchange of the movement protein - coat protein gene cassette, bounded by the two genomic regions most prone to recombination in mastrevirus genomes; the first surrounding the virion-strand origin of replication, and the second around the interface between the coat protein gene and the short intergenic region. Therefore, aside from the likely adaptive advantages presented by a modular exchange of this cassette, these specific breakpoints may have been largely predetermined by the underlying mechanisms of mastrevirus recombination. To investigate this hypothesis, we constructed artificial, low-fitness, reciprocal chimaeric MSV genomes using alternating genomic segments from two MSV strains; a grass-adapted MSV-B, and a maize-adapted MSV-A. Between them, each pair of reciprocal chimaeric genomes represented all of the genetic material required to reconstruct - via recombination - the highly maize-adapted MSV-A genotype, MSV-MatA. We then co-infected a selection of differentially MSV-resistant maize genotypes with pairs of reciprocal chimaeras to determine the efficiency with which recombination would give rise to high-fitness progeny genomes resembling MSV-MatA.</p> <p>Results</p> <p>Recombinants resembling MSV-MatA invariably arose in all of our experiments. However, the accuracy and efficiency with which the MSV-MatA genotype was recovered across all replicates of each experiment depended on the MSV susceptibility of the maize genotypes used and the precise positions - in relation to known recombination hotspots - of the breakpoints required to re-create MSV-MatA. Although the MSV-sensitive maize genotype gave rise to the greatest variety of recombinants, the measured fitness of each of these recombinants correlated with their similarity to MSV-MatA.</p> <p>Conclusions</p> <p>The mechanistic predispositions of different MSV genomic regions to recombination can strongly influence the accessibility of high-fitness MSV recombinants. The frequency with which the fittest recombinant MSV genomes arise also correlates directly with the escalating selection pressures imposed by increasingly MSV-resistant maize hosts.</p>http://www.biomedcentral.com/1471-2148/11/350
spellingShingle Monjane Adérito L
van der Walt Eric
Varsani Arvind
Rybicki Edward P
Martin Darren P
Recombination hotspots and host susceptibility modulate the adaptive value of recombination during maize streak virus evolution
BMC Evolutionary Biology
title Recombination hotspots and host susceptibility modulate the adaptive value of recombination during maize streak virus evolution
title_full Recombination hotspots and host susceptibility modulate the adaptive value of recombination during maize streak virus evolution
title_fullStr Recombination hotspots and host susceptibility modulate the adaptive value of recombination during maize streak virus evolution
title_full_unstemmed Recombination hotspots and host susceptibility modulate the adaptive value of recombination during maize streak virus evolution
title_short Recombination hotspots and host susceptibility modulate the adaptive value of recombination during maize streak virus evolution
title_sort recombination hotspots and host susceptibility modulate the adaptive value of recombination during maize streak virus evolution
url http://www.biomedcentral.com/1471-2148/11/350
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