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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Published inPLoS biology Vol. 21; no. 9; p. e3002278
Main Authors 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
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 14.09.2023
Public Library of Science (PLoS)
Subjects
Acriflavine
Antifungal Agents
Aspergillus fumigatus
Aspergillus fumigatus - genetics
ATP-Binding Cassette Transporters
Biological Transport
Biology and Life Sciences
Cell division
Chromosomes
Efflux
Eukaryota
Eukaryotes
Fungicides
Genetic crosses
Genetic diversity
Genetic variance
Genomes
Genotypes
Haplotypes
Humans
Medicine and Health Sciences
Meiosis
Meiosis - genetics
Multidrug resistance
Mutation
Offspring
Parents & parenting
Research and Analysis Methods
Sexual reproduction
Short Reports
Yeast
United Kingdom > UK
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Abstract 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 (TR34/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.
AbstractList 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 (TR34/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.
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. Aspergillus fumigatus is a saprotrophic fungus that can cause serious life-threatening invasive infections in immunocompromised individuals. By constructing a recombination map, this study shows that A. fumigatus produces the highest number of crossovers per chromosome ever described.
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.
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 (TR34/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.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 (TR34/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.
Author Snelders, Eveline
Reyes Marquez, Francisca
Fisher, Matthew C
van den Heuvel, Joost
Rhodes, Johanna
Dyer, Paul S
Nijland, Reindert
Debets, Alfons J M
Stanford, Felicia Adelina
Auxier, Ben
Becker, Frank M
AuthorAffiliation Duke University Medical Center, UNITED STATES
4 Marine Animal Ecology, Wageningen University, Wageningen, the Netherlands
2 School of Life Sciences, University of Nottingham, Nottingham, United Kingdom
1 Laboratory of Genetics, Wageningen University; Wageningen, the Netherlands
3 MRC Centre for Global Infectious Disease Analysis, Imperial College London, London, United Kingdom
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/37708139$$D View this record in MEDLINE/PubMed
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Snippet Sexual reproduction involving meiosis is essential in most eukaryotes. This produces offspring with novel genotypes, both by segregation of parental...
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StartPage e3002278
SubjectTerms Acriflavine
Antifungal Agents
Aspergillus fumigatus
Aspergillus fumigatus - genetics
ATP-Binding Cassette Transporters
Biological Transport
Biology and Life Sciences
Cell division
Chromosomes
Efflux
Eukaryota
Eukaryotes
Fungicides
Genetic crosses
Genetic diversity
Genetic variance
Genomes
Genotypes
Haplotypes
Humans
Medicine and Health Sciences
Meiosis
Meiosis - genetics
Multidrug resistance
Mutation
Offspring
Parents & parenting
Research and Analysis Methods
Sexual reproduction
Short Reports
Yeast
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Title The human fungal pathogen Aspergillus fumigatus can produce the highest known number of meiotic crossovers
URI https://www.ncbi.nlm.nih.gov/pubmed/37708139
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http://dx.doi.org/10.1371/journal.pbio.3002278
Volume 21
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