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The human fungal pathogen Aspergillus fumigatus can produce the highest known number of meiotic crossovers

Sexual reproduction involving meiosis is essential in most eukaryotes. This produces offspring with novel genotypes, both by segregation of parental chromosomes as well as crossovers between homologous chromosomes. A sexual cycle for the opportunistic human pathogenic fungus Aspergillus fumigatus is...

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Autores principales: Auxier, Ben, Debets, Alfons J. M., Stanford, Felicia Adelina, Rhodes, Johanna, Becker, Frank M., Reyes Marquez, Francisca, Nijland, Reindert, Dyer, Paul S., Fisher, Matthew C., van den Heuvel, Joost, Snelders, Eveline
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10501685/
https://www.ncbi.nlm.nih.gov/pubmed/37708139
http://dx.doi.org/10.1371/journal.pbio.3002278
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author Auxier, Ben
Debets, Alfons J. M.
Stanford, Felicia Adelina
Rhodes, Johanna
Becker, Frank M.
Reyes Marquez, Francisca
Nijland, Reindert
Dyer, Paul S.
Fisher, Matthew C.
van den Heuvel, Joost
Snelders, Eveline
author_facet Auxier, Ben
Debets, Alfons J. M.
Stanford, Felicia Adelina
Rhodes, Johanna
Becker, Frank M.
Reyes Marquez, Francisca
Nijland, Reindert
Dyer, Paul S.
Fisher, Matthew C.
van den Heuvel, Joost
Snelders, Eveline
author_sort Auxier, Ben
collection PubMed
description Sexual reproduction involving meiosis is essential in most eukaryotes. This produces offspring with novel genotypes, both by segregation of parental chromosomes as well as crossovers between homologous chromosomes. A sexual cycle for the opportunistic human pathogenic fungus Aspergillus fumigatus is known, but the genetic consequences of meiosis have remained unknown. Among other Aspergilli, it is known that A. flavus has a moderately high recombination rate with an average of 4.2 crossovers per chromosome pair, whereas A. nidulans has in contrast a higher rate with 9.3 crossovers per chromosome pair. Here, we show in a cross between A. fumigatus strains that they produce an average of 29.9 crossovers per chromosome pair and large variation in total map length across additional strain crosses. This rate of crossovers per chromosome is more than twice that seen for any known organism, which we discuss in relation to other genetic model systems. We validate this high rate of crossovers through mapping of resistance to the laboratory antifungal acriflavine by using standing variation in an undescribed ABC efflux transporter. We then demonstrate that this rate of crossovers is sufficient to produce one of the common multidrug resistant haplotypes found in the cyp51A gene (TR(34)/L98H) in crosses among parents harboring either of 2 nearby genetic variants, possibly explaining the early spread of such haplotypes. Our results suggest that genomic studies in this species should reassess common assumptions about linkage between genetic regions. The finding of an unparalleled crossover rate in A. fumigatus provides opportunities to understand why these rates are not generally higher in other eukaryotes.
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spelling pubmed-105016852023-09-15 The human fungal pathogen Aspergillus fumigatus can produce the highest known number of meiotic crossovers Auxier, Ben Debets, Alfons J. M. Stanford, Felicia Adelina Rhodes, Johanna Becker, Frank M. Reyes Marquez, Francisca Nijland, Reindert Dyer, Paul S. Fisher, Matthew C. van den Heuvel, Joost Snelders, Eveline PLoS Biol Short Reports Sexual reproduction involving meiosis is essential in most eukaryotes. This produces offspring with novel genotypes, both by segregation of parental chromosomes as well as crossovers between homologous chromosomes. A sexual cycle for the opportunistic human pathogenic fungus Aspergillus fumigatus is known, but the genetic consequences of meiosis have remained unknown. Among other Aspergilli, it is known that A. flavus has a moderately high recombination rate with an average of 4.2 crossovers per chromosome pair, whereas A. nidulans has in contrast a higher rate with 9.3 crossovers per chromosome pair. Here, we show in a cross between A. fumigatus strains that they produce an average of 29.9 crossovers per chromosome pair and large variation in total map length across additional strain crosses. This rate of crossovers per chromosome is more than twice that seen for any known organism, which we discuss in relation to other genetic model systems. We validate this high rate of crossovers through mapping of resistance to the laboratory antifungal acriflavine by using standing variation in an undescribed ABC efflux transporter. We then demonstrate that this rate of crossovers is sufficient to produce one of the common multidrug resistant haplotypes found in the cyp51A gene (TR(34)/L98H) in crosses among parents harboring either of 2 nearby genetic variants, possibly explaining the early spread of such haplotypes. Our results suggest that genomic studies in this species should reassess common assumptions about linkage between genetic regions. The finding of an unparalleled crossover rate in A. fumigatus provides opportunities to understand why these rates are not generally higher in other eukaryotes. Public Library of Science 2023-09-14 /pmc/articles/PMC10501685/ /pubmed/37708139 http://dx.doi.org/10.1371/journal.pbio.3002278 Text en © 2023 Auxier et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Short Reports
Auxier, Ben
Debets, Alfons J. M.
Stanford, Felicia Adelina
Rhodes, Johanna
Becker, Frank M.
Reyes Marquez, Francisca
Nijland, Reindert
Dyer, Paul S.
Fisher, Matthew C.
van den Heuvel, Joost
Snelders, Eveline
The human fungal pathogen Aspergillus fumigatus can produce the highest known number of meiotic crossovers
title The human fungal pathogen Aspergillus fumigatus can produce the highest known number of meiotic crossovers
title_full The human fungal pathogen Aspergillus fumigatus can produce the highest known number of meiotic crossovers
title_fullStr The human fungal pathogen Aspergillus fumigatus can produce the highest known number of meiotic crossovers
title_full_unstemmed The human fungal pathogen Aspergillus fumigatus can produce the highest known number of meiotic crossovers
title_short The human fungal pathogen Aspergillus fumigatus can produce the highest known number of meiotic crossovers
title_sort human fungal pathogen aspergillus fumigatus can produce the highest known number of meiotic crossovers
topic Short Reports
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10501685/
https://www.ncbi.nlm.nih.gov/pubmed/37708139
http://dx.doi.org/10.1371/journal.pbio.3002278
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