Cargando…
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...
Autores principales: | , , , , , , , , , , |
---|---|
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 |
_version_ | 1785106165497069568 |
---|---|
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. |
format | Online Article Text |
id | pubmed-10501685 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT auxierben thehumanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT debetsalfonsjm thehumanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT stanfordfeliciaadelina thehumanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT rhodesjohanna thehumanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT beckerfrankm thehumanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT reyesmarquezfrancisca thehumanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT nijlandreindert thehumanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT dyerpauls thehumanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT fishermatthewc thehumanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT vandenheuveljoost thehumanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT snelderseveline thehumanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT auxierben humanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT debetsalfonsjm humanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT stanfordfeliciaadelina humanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT rhodesjohanna humanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT beckerfrankm humanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT reyesmarquezfrancisca humanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT nijlandreindert humanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT dyerpauls humanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT fishermatthewc humanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT vandenheuveljoost humanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers AT snelderseveline humanfungalpathogenaspergillusfumigatuscanproducethehighestknownnumberofmeioticcrossovers |