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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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Phenotypic analyses of progeny from α-α unisexual and a-α bisexual reproduction.A) Top: Different phenotypic categories that were observed among the meiotic progeny from α-α unisexual and a-α bisexual reproduction. Bottom: Summary of percentage (%) of progeny that belonged to different phenotypic categories in α-α unisexual and a-α bisexual reproduction. Blue triangles highlight the phenotypes of parental strain 431α; red triangles highlight the phenotypes of the parental strains XL280αSS and XL280a. B) Phenotypic segregation of hyphal growth among the meiotic progeny from α-α unisexual and a-α bisexual reproduction. The numbers represent the percentage of progeny that belong to different phenotypic categories. Blue triangles highlight the phenotypes of parental strain 431α; red triangles highlight the phenotypes of the parental strains XL280αSS and XL280a. C) The small and large colonies of the meiotic progeny SSB309 when grown on YPD solid medium at 30°C.
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pgen-1004849-g001: Phenotypic analyses of progeny from α-α unisexual and a-α bisexual reproduction.A) Top: Different phenotypic categories that were observed among the meiotic progeny from α-α unisexual and a-α bisexual reproduction. Bottom: Summary of percentage (%) of progeny that belonged to different phenotypic categories in α-α unisexual and a-α bisexual reproduction. Blue triangles highlight the phenotypes of parental strain 431α; red triangles highlight the phenotypes of the parental strains XL280αSS and XL280a. B) Phenotypic segregation of hyphal growth among the meiotic progeny from α-α unisexual and a-α bisexual reproduction. The numbers represent the percentage of progeny that belong to different phenotypic categories. Blue triangles highlight the phenotypes of parental strain 431α; red triangles highlight the phenotypes of the parental strains XL280αSS and XL280a. C) The small and large colonies of the meiotic progeny SSB309 when grown on YPD solid medium at 30°C.

Mentions: For temperature tolerance, we tested the growth of the progeny on YPD medium at three temperatures: 37°C, 40°C, and 41°C (S1 Table and S2 Table). At each temperature we found progeny from both α-α unisexual and a-α bisexual reproduction that exhibited transgressive phenotypes compared to the two parental strains. Specifically, at 37°C none of the parental strains showed a growth defect. However, we found 7% and 22.2% of the progeny from α-α unisexual and a-α bisexual reproduction, respectively, exhibited growth defect, and thus are sensitive to high temperature (Fig. 1A). At 40°C and 41°C, the three parental strains showed little or no growth. However, there were 53.3% and 35.7% of the progeny from α-α unisexual reproduction that showed enhanced fitness at 40°C and 41°C, respectively. Similarly, from a-α unisexual reproduction, there were also 30.9% and 9.9% of the progeny that showed enhanced fitness at 40°C and 41°C, respectively (Fig. 1A).


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

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

Phenotypic analyses of progeny from α-α unisexual and a-α bisexual reproduction.A) Top: Different phenotypic categories that were observed among the meiotic progeny from α-α unisexual and a-α bisexual reproduction. Bottom: Summary of percentage (%) of progeny that belonged to different phenotypic categories in α-α unisexual and a-α bisexual reproduction. Blue triangles highlight the phenotypes of parental strain 431α; red triangles highlight the phenotypes of the parental strains XL280αSS and XL280a. B) Phenotypic segregation of hyphal growth among the meiotic progeny from α-α unisexual and a-α bisexual reproduction. The numbers represent the percentage of progeny that belong to different phenotypic categories. Blue triangles highlight the phenotypes of parental strain 431α; red triangles highlight the phenotypes of the parental strains XL280αSS and XL280a. C) The small and large colonies of the meiotic progeny SSB309 when grown on YPD solid medium at 30°C.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004849-g001: Phenotypic analyses of progeny from α-α unisexual and a-α bisexual reproduction.A) Top: Different phenotypic categories that were observed among the meiotic progeny from α-α unisexual and a-α bisexual reproduction. Bottom: Summary of percentage (%) of progeny that belonged to different phenotypic categories in α-α unisexual and a-α bisexual reproduction. Blue triangles highlight the phenotypes of parental strain 431α; red triangles highlight the phenotypes of the parental strains XL280αSS and XL280a. B) Phenotypic segregation of hyphal growth among the meiotic progeny from α-α unisexual and a-α bisexual reproduction. The numbers represent the percentage of progeny that belong to different phenotypic categories. Blue triangles highlight the phenotypes of parental strain 431α; red triangles highlight the phenotypes of the parental strains XL280αSS and XL280a. C) The small and large colonies of the meiotic progeny SSB309 when grown on YPD solid medium at 30°C.
Mentions: For temperature tolerance, we tested the growth of the progeny on YPD medium at three temperatures: 37°C, 40°C, and 41°C (S1 Table and S2 Table). At each temperature we found progeny from both α-α unisexual and a-α bisexual reproduction that exhibited transgressive phenotypes compared to the two parental strains. Specifically, at 37°C none of the parental strains showed a growth defect. However, we found 7% and 22.2% of the progeny from α-α unisexual and a-α bisexual reproduction, respectively, exhibited growth defect, and thus are sensitive to high temperature (Fig. 1A). At 40°C and 41°C, the three parental strains showed little or no growth. However, there were 53.3% and 35.7% of the progeny from α-α unisexual reproduction that showed enhanced fitness at 40°C and 41°C, respectively. Similarly, from a-α unisexual reproduction, there were also 30.9% and 9.9% of the progeny that showed enhanced fitness at 40°C and 41°C, respectively (Fig. 1A).

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