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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

Genetic markers and genotyping of the meiotic progeny.Shown here are results of genotyping of meiotic progeny from α-α unisexual reproduction strains 431α and XL280αSS. The marker on the left is “Inter-CND00400–CND00410” and the marker on the right is “Inter-CND05360–CND05370” (Please see Table 2 for detailed marker information). Dashed-lined rectangles highlight the controls included during genotyping, which are (from left to right): 431α, XL280αSS, and artificial heterozygote (i.e. mixed DNA sample; please see Materials and Methods for detailed information). “L” indicates DNA ladder. The progeny that are heterozygous at these two markers are highlighted with red stars.
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pgen-1004849-g002: Genetic markers and genotyping of the meiotic progeny.Shown here are results of genotyping of meiotic progeny from α-α unisexual reproduction strains 431α and XL280αSS. The marker on the left is “Inter-CND00400–CND00410” and the marker on the right is “Inter-CND05360–CND05370” (Please see Table 2 for detailed marker information). Dashed-lined rectangles highlight the controls included during genotyping, which are (from left to right): 431α, XL280αSS, and artificial heterozygote (i.e. mixed DNA sample; please see Materials and Methods for detailed information). “L” indicates DNA ladder. The progeny that are heterozygous at these two markers are highlighted with red stars.

Mentions: To study meiotic recombination during α-α unisexual and a-α bisexual reproduction, we focused on chromosome 4 where the MAT locus is located. We developed 44 co-dominant genetic markers that are located along chromosome 4, including eight markers that are located within the MAT locus, as well as two markers that flank the centromere of chromosome 4 (Table 2; Fig. 2).


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

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

Genetic markers and genotyping of the meiotic progeny.Shown here are results of genotyping of meiotic progeny from α-α unisexual reproduction strains 431α and XL280αSS. The marker on the left is “Inter-CND00400–CND00410” and the marker on the right is “Inter-CND05360–CND05370” (Please see Table 2 for detailed marker information). Dashed-lined rectangles highlight the controls included during genotyping, which are (from left to right): 431α, XL280αSS, and artificial heterozygote (i.e. mixed DNA sample; please see Materials and Methods for detailed information). “L” indicates DNA ladder. The progeny that are heterozygous at these two markers are highlighted with red stars.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004849-g002: Genetic markers and genotyping of the meiotic progeny.Shown here are results of genotyping of meiotic progeny from α-α unisexual reproduction strains 431α and XL280αSS. The marker on the left is “Inter-CND00400–CND00410” and the marker on the right is “Inter-CND05360–CND05370” (Please see Table 2 for detailed marker information). Dashed-lined rectangles highlight the controls included during genotyping, which are (from left to right): 431α, XL280αSS, and artificial heterozygote (i.e. mixed DNA sample; please see Materials and Methods for detailed information). “L” indicates DNA ladder. The progeny that are heterozygous at these two markers are highlighted with red stars.
Mentions: To study meiotic recombination during α-α unisexual and a-α bisexual reproduction, we focused on chromosome 4 where the MAT locus is located. We developed 44 co-dominant genetic markers that are located along chromosome 4, including eight markers that are located within the MAT locus, as well as two markers that flank the centromere of chromosome 4 (Table 2; Fig. 2).

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