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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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Genetic maps based on analysis of α-α unisexual and a-α bisexual reproduction meiotic progeny.Top and bottom panels: Genetic maps were constructed for a-α bisexual and α-α unisexual reproduction, respectively. The genetic map from a-α bisexual reproduction contains four linkage groups (LG) and three genetic markers that are not linked to any other markers (Top), while the genetic map from α-α unisexual reproduction contains three linkage groups (Bottom). Numbers at the bottom of linkage groups indicate the serial numbers of the genetic markers analyzed in this study (see Table 2). Numbers at the top of the linkage groups indicate the genetic distance of the markers from the beginning of their respective linkage groups. Middle panel: A schematic illustration of the genetic markers employed to genotype mating products from α-α unisexual reproduction and a-α bisexual reproduction. The black bar represents chromosome 4, the vertical lines indicate physical positions of the genetic markers along chromosome 4, and the red and green bars indicate locations of the centromere and MAT locus, respectively.
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pgen-1004849-g004: Genetic maps based on analysis of α-α unisexual and a-α bisexual reproduction meiotic progeny.Top and bottom panels: Genetic maps were constructed for a-α bisexual and α-α unisexual reproduction, respectively. The genetic map from a-α bisexual reproduction contains four linkage groups (LG) and three genetic markers that are not linked to any other markers (Top), while the genetic map from α-α unisexual reproduction contains three linkage groups (Bottom). Numbers at the bottom of linkage groups indicate the serial numbers of the genetic markers analyzed in this study (see Table 2). Numbers at the top of the linkage groups indicate the genetic distance of the markers from the beginning of their respective linkage groups. Middle panel: A schematic illustration of the genetic markers employed to genotype mating products from α-α unisexual reproduction and a-α bisexual reproduction. The black bar represents chromosome 4, the vertical lines indicate physical positions of the genetic markers along chromosome 4, and the red and green bars indicate locations of the centromere and MAT locus, respectively.

Mentions: For α-α unisexual reproduction, we constructed a genetic linkage map of the 42 markers based on the genotyping results for the 144 mating products that were monomorphic at all of the 42 genetic markers analyzed. The 42 markers formed three linkage groups (LGI–LGIII) that were 134.9 cM, 78.7 cM, and 10.2 cM in size, and spanned 19, 20, and 3 markers, respectively (Fig. 4). The orders of markers within the linkage groups are in overall agreement with their physical positions on chromosome 4, with the exceptions of three markers (No. 37–No. 39) in LGII and one marker (No. 40) in LGIII (Fig. 4). The three linkage groups had a total length of 223.8 cM, and encompassed 1596 kb of chromosome 4, which produced an average recombination frequency of 7.13 kb/cM (Table 3).


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 maps based on analysis of α-α unisexual and a-α bisexual reproduction meiotic progeny.Top and bottom panels: Genetic maps were constructed for a-α bisexual and α-α unisexual reproduction, respectively. The genetic map from a-α bisexual reproduction contains four linkage groups (LG) and three genetic markers that are not linked to any other markers (Top), while the genetic map from α-α unisexual reproduction contains three linkage groups (Bottom). Numbers at the bottom of linkage groups indicate the serial numbers of the genetic markers analyzed in this study (see Table 2). Numbers at the top of the linkage groups indicate the genetic distance of the markers from the beginning of their respective linkage groups. Middle panel: A schematic illustration of the genetic markers employed to genotype mating products from α-α unisexual reproduction and a-α bisexual reproduction. The black bar represents chromosome 4, the vertical lines indicate physical positions of the genetic markers along chromosome 4, and the red and green bars indicate locations of the centromere and MAT locus, respectively.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1004849-g004: Genetic maps based on analysis of α-α unisexual and a-α bisexual reproduction meiotic progeny.Top and bottom panels: Genetic maps were constructed for a-α bisexual and α-α unisexual reproduction, respectively. The genetic map from a-α bisexual reproduction contains four linkage groups (LG) and three genetic markers that are not linked to any other markers (Top), while the genetic map from α-α unisexual reproduction contains three linkage groups (Bottom). Numbers at the bottom of linkage groups indicate the serial numbers of the genetic markers analyzed in this study (see Table 2). Numbers at the top of the linkage groups indicate the genetic distance of the markers from the beginning of their respective linkage groups. Middle panel: A schematic illustration of the genetic markers employed to genotype mating products from α-α unisexual reproduction and a-α bisexual reproduction. The black bar represents chromosome 4, the vertical lines indicate physical positions of the genetic markers along chromosome 4, and the red and green bars indicate locations of the centromere and MAT locus, respectively.
Mentions: For α-α unisexual reproduction, we constructed a genetic linkage map of the 42 markers based on the genotyping results for the 144 mating products that were monomorphic at all of the 42 genetic markers analyzed. The 42 markers formed three linkage groups (LGI–LGIII) that were 134.9 cM, 78.7 cM, and 10.2 cM in size, and spanned 19, 20, and 3 markers, respectively (Fig. 4). The orders of markers within the linkage groups are in overall agreement with their physical positions on chromosome 4, with the exceptions of three markers (No. 37–No. 39) in LGII and one marker (No. 40) in LGIII (Fig. 4). The three linkage groups had a total length of 223.8 cM, and encompassed 1596 kb of chromosome 4, which produced an average recombination frequency of 7.13 kb/cM (Table 3).

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