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Unisexual reproduction drives meiotic recombination and phenotypic and karyotypic plasticity in Cryptococcus neoformans.

Sun S, Billmyre RB, Mieczkowski PA, Heitman J - PLoS Genet. (2014)

Bottom Line: We found that meiotic recombination operates in a similar fashion during both modes of sexual reproduction.Additionally, we found diploid meiotic progeny were also produced at similar frequencies in the two modes of sexual reproduction, and transient chromosomal loss and duplication likely occurs frequently and results in aneuploidy and loss of heterozygosity that can span entire chromosomes.Our results provide definitive evidence that α-α unisexual reproduction is a meiotic process similar to a-α bisexual reproduction.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, United States of America.

ABSTRACT
In fungi, unisexual reproduction, where sexual development is initiated without the presence of two compatible mating type alleles, has been observed in several species that can also undergo traditional bisexual reproduction, including the important human fungal pathogens Cryptococcus neoformans and Candida albicans. While unisexual reproduction has been well characterized qualitatively, detailed quantifications are still lacking for aspects of this process, such as the frequency of recombination during unisexual reproduction, and how this compares with bisexual reproduction. Here, we analyzed meiotic recombination during α-α unisexual and a-α bisexual reproduction of C. neoformans. We found that meiotic recombination operates in a similar fashion during both modes of sexual reproduction. Specifically, we observed that in α-α unisexual reproduction, the numbers of crossovers along the chromosomes during meiosis, recombination frequencies at specific chromosomal regions, as well as meiotic recombination hot and cold spots, are all similar to those observed during a-α bisexual reproduction. The similarity in meiosis is also reflected by the fact that phenotypic segregation among progeny collected from the two modes of sexual reproduction is also similar, with transgressive segregation being observed in both. Additionally, we found diploid meiotic progeny were also produced at similar frequencies in the two modes of sexual reproduction, and transient chromosomal loss and duplication likely occurs frequently and results in aneuploidy and loss of heterozygosity that can span entire chromosomes. Furthermore, in both α-α unisexual and a-α bisexual reproduction, we observed biased allele inheritance in regions on chromosome 4, suggesting the presence of fragile chromosomal regions that might be vulnerable to mitotic recombination. Interestingly, we also observed a crossover event that occurred within the MAT locus during α-α unisexual reproduction. Our results provide definitive evidence that α-α unisexual reproduction is a meiotic process similar to a-α bisexual reproduction.

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Related in: MedlinePlus

Crossovers are distributed along chromosome 4 during α-α unisexual and a-α bisexual reproduction.Blue bars represent the number of progeny from α-α unisexual reproduction between strains 431α and XL280αSS, while the red bars represent the number of genotypes from a-α bisexual reproduction between strains 431α and XL280a. The 12 progeny from α-α unisexual reproduction, as well as the 2 genotypes from a-α bisexual reproduction that were disomic for chromosome 4 were excluded.
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pgen-1004849-g003: Crossovers are distributed along chromosome 4 during α-α unisexual and a-α bisexual reproduction.Blue bars represent the number of progeny from α-α unisexual reproduction between strains 431α and XL280αSS, while the red bars represent the number of genotypes from a-α bisexual reproduction between strains 431α and XL280a. The 12 progeny from α-α unisexual reproduction, as well as the 2 genotypes from a-α bisexual reproduction that were disomic for chromosome 4 were excluded.

Mentions: We applied 42 of the 44 genetic markers to genotype the 156 mating products collected from α-α unisexual reproduction. Based on these 42 markers, we identified a total of 74 different genotypes among the 156 mating products recovered from α-α unisexual reproduction. Eleven of the 74 genotypes that were represented by 12 progeny had loci that were heterozygous, suggesting the chromosome 4 in these progeny might be disomic (see below). The number of progeny representing each genotype ranged from 1 to 17, with the majority of the genotypes (66, 89%) being represented by 1 to 3 progeny each. There were two genotypes, No. 52 and No. 60, which were represented by 13 and 17 progeny, respectively (S3 Table). The numbers of detected crossovers along chromosome 4 also varied among the progeny. Of the 144 progeny that were not heterozygous at any of the 42 markers, the majority (126, 87.5%) had 1 to 4 crossovers along chromosome 4 (S4 Table; Fig. 3). The maximum number of crossovers along chromosome 4 was 8, which occurred in one progeny, SSB385 (genotype 23; S3 Table).


Unisexual reproduction drives meiotic recombination and phenotypic and karyotypic plasticity in Cryptococcus neoformans.

Sun S, Billmyre RB, Mieczkowski PA, Heitman J - PLoS Genet. (2014)

Crossovers are distributed along chromosome 4 during α-α unisexual and a-α bisexual reproduction.Blue bars represent the number of progeny from α-α unisexual reproduction between strains 431α and XL280αSS, while the red bars represent the number of genotypes from a-α bisexual reproduction between strains 431α and XL280a. The 12 progeny from α-α unisexual reproduction, as well as the 2 genotypes from a-α bisexual reproduction that were disomic for chromosome 4 were excluded.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4263396&req=5

pgen-1004849-g003: Crossovers are distributed along chromosome 4 during α-α unisexual and a-α bisexual reproduction.Blue bars represent the number of progeny from α-α unisexual reproduction between strains 431α and XL280αSS, while the red bars represent the number of genotypes from a-α bisexual reproduction between strains 431α and XL280a. The 12 progeny from α-α unisexual reproduction, as well as the 2 genotypes from a-α bisexual reproduction that were disomic for chromosome 4 were excluded.
Mentions: We applied 42 of the 44 genetic markers to genotype the 156 mating products collected from α-α unisexual reproduction. Based on these 42 markers, we identified a total of 74 different genotypes among the 156 mating products recovered from α-α unisexual reproduction. Eleven of the 74 genotypes that were represented by 12 progeny had loci that were heterozygous, suggesting the chromosome 4 in these progeny might be disomic (see below). The number of progeny representing each genotype ranged from 1 to 17, with the majority of the genotypes (66, 89%) being represented by 1 to 3 progeny each. There were two genotypes, No. 52 and No. 60, which were represented by 13 and 17 progeny, respectively (S3 Table). The numbers of detected crossovers along chromosome 4 also varied among the progeny. Of the 144 progeny that were not heterozygous at any of the 42 markers, the majority (126, 87.5%) had 1 to 4 crossovers along chromosome 4 (S4 Table; Fig. 3). The maximum number of crossovers along chromosome 4 was 8, which occurred in one progeny, SSB385 (genotype 23; S3 Table).

Bottom Line: We found that meiotic recombination operates in a similar fashion during both modes of sexual reproduction.Additionally, we found diploid meiotic progeny were also produced at similar frequencies in the two modes of sexual reproduction, and transient chromosomal loss and duplication likely occurs frequently and results in aneuploidy and loss of heterozygosity that can span entire chromosomes.Our results provide definitive evidence that α-α unisexual reproduction is a meiotic process similar to a-α bisexual reproduction.

View Article: PubMed Central - PubMed

Affiliation: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, North Carolina, United States of America.

ABSTRACT
In fungi, unisexual reproduction, where sexual development is initiated without the presence of two compatible mating type alleles, has been observed in several species that can also undergo traditional bisexual reproduction, including the important human fungal pathogens Cryptococcus neoformans and Candida albicans. While unisexual reproduction has been well characterized qualitatively, detailed quantifications are still lacking for aspects of this process, such as the frequency of recombination during unisexual reproduction, and how this compares with bisexual reproduction. Here, we analyzed meiotic recombination during α-α unisexual and a-α bisexual reproduction of C. neoformans. We found that meiotic recombination operates in a similar fashion during both modes of sexual reproduction. Specifically, we observed that in α-α unisexual reproduction, the numbers of crossovers along the chromosomes during meiosis, recombination frequencies at specific chromosomal regions, as well as meiotic recombination hot and cold spots, are all similar to those observed during a-α bisexual reproduction. The similarity in meiosis is also reflected by the fact that phenotypic segregation among progeny collected from the two modes of sexual reproduction is also similar, with transgressive segregation being observed in both. Additionally, we found diploid meiotic progeny were also produced at similar frequencies in the two modes of sexual reproduction, and transient chromosomal loss and duplication likely occurs frequently and results in aneuploidy and loss of heterozygosity that can span entire chromosomes. Furthermore, in both α-α unisexual and a-α bisexual reproduction, we observed biased allele inheritance in regions on chromosome 4, suggesting the presence of fragile chromosomal regions that might be vulnerable to mitotic recombination. Interestingly, we also observed a crossover event that occurred within the MAT locus during α-α unisexual reproduction. Our results provide definitive evidence that α-α unisexual reproduction is a meiotic process similar to a-α bisexual reproduction.

Show MeSH
Related in: MedlinePlus