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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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Biased allele inheritance among progeny from a-α bisexual reproduction.Numbers in the top row indicate the loci/genetic markers used for genotyping progeny from a-α bisexual reproduction, with the markers flanking the centromere are highlighted in red and the markers within the MAT locus are highlighted in green (see Table 2 for detailed information). For simplicity, only the unique genotypes are shown for each of the eight basidia that showed biased allele inheritance. The markers that exhibited biased allele inheritance are highlighted by rectangles, with red color indicating a bias toward the “a” allele and green color indicating a bias toward the “b” allele.
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pgen-1004849-g009: Biased allele inheritance among progeny from a-α bisexual reproduction.Numbers in the top row indicate the loci/genetic markers used for genotyping progeny from a-α bisexual reproduction, with the markers flanking the centromere are highlighted in red and the markers within the MAT locus are highlighted in green (see Table 2 for detailed information). For simplicity, only the unique genotypes are shown for each of the eight basidia that showed biased allele inheritance. The markers that exhibited biased allele inheritance are highlighted by rectangles, with red color indicating a bias toward the “a” allele and green color indicating a bias toward the “b” allele.

Mentions: Similarly, we also found evidence of biased allele inheritance among progeny that were dissected from a-α bisexual reproduction. Specifically, of the 26 basidia from which viable spores were recovered (basidium No. 15 was excluded because only one viable spore was recovered), for 8 basidia (30.8%) there was at least one (and up to 10) genetic marker(s) for which the allele from one of the two parental strains was absent among all viable spores (Fig. 9). All eight basidia generated spores that belonged to four different genotypes, and the germination rates of the spores from these eight basidia were higher than 80% except for two basidia, No. 3 and No. 20, that had spore germination rates of 50% and 46%, respectively. Among these eight basidia, the absence of an allele from one of the two parental strains occurred in 13 of the 17 loci analyzed. Interestingly, of the four loci for which no biased allele inheritance has been observed during a-α bisexual reproduction, one locus, SXI1Dα/SXI2Da, is located within the MAT locus, while the other three, Inter-BSP3-IKS1, Inter-CND06020–CND06030 and Inter-CND06030–CN06040, are located within regions that flank the MAT locus (Table 2; Fig. 9).


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

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

Biased allele inheritance among progeny from a-α bisexual reproduction.Numbers in the top row indicate the loci/genetic markers used for genotyping progeny from a-α bisexual reproduction, with the markers flanking the centromere are highlighted in red and the markers within the MAT locus are highlighted in green (see Table 2 for detailed information). For simplicity, only the unique genotypes are shown for each of the eight basidia that showed biased allele inheritance. The markers that exhibited biased allele inheritance are highlighted by rectangles, with red color indicating a bias toward the “a” allele and green color indicating a bias toward the “b” allele.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004849-g009: Biased allele inheritance among progeny from a-α bisexual reproduction.Numbers in the top row indicate the loci/genetic markers used for genotyping progeny from a-α bisexual reproduction, with the markers flanking the centromere are highlighted in red and the markers within the MAT locus are highlighted in green (see Table 2 for detailed information). For simplicity, only the unique genotypes are shown for each of the eight basidia that showed biased allele inheritance. The markers that exhibited biased allele inheritance are highlighted by rectangles, with red color indicating a bias toward the “a” allele and green color indicating a bias toward the “b” allele.
Mentions: Similarly, we also found evidence of biased allele inheritance among progeny that were dissected from a-α bisexual reproduction. Specifically, of the 26 basidia from which viable spores were recovered (basidium No. 15 was excluded because only one viable spore was recovered), for 8 basidia (30.8%) there was at least one (and up to 10) genetic marker(s) for which the allele from one of the two parental strains was absent among all viable spores (Fig. 9). All eight basidia generated spores that belonged to four different genotypes, and the germination rates of the spores from these eight basidia were higher than 80% except for two basidia, No. 3 and No. 20, that had spore germination rates of 50% and 46%, respectively. Among these eight basidia, the absence of an allele from one of the two parental strains occurred in 13 of the 17 loci analyzed. Interestingly, of the four loci for which no biased allele inheritance has been observed during a-α bisexual reproduction, one locus, SXI1Dα/SXI2Da, is located within the MAT locus, while the other three, Inter-BSP3-IKS1, Inter-CND06020–CND06030 and Inter-CND06030–CN06040, are located within regions that flank the MAT locus (Table 2; Fig. 9).

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