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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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Recombination within the MAT locus during α-α unisexual reproduction.A) Of the 42 genetic markers (only No. 21 to No. 42 are shown here for simplicity) that were analyzed for progeny from α-α unisexual reproduction, progeny SSB369 inherited “a” alleles from parental strain 431α for all but 6 markers (No. 31–No. 36; see Table 2 for detailed marker information), which were continuous and located either within or at the edge of the MAT locus. The run of allele “b” stopped between markers No. 36 and No. 37 within the MAT locus at the 5′ end, and between markers No. 30 and No. 31 that flank the MAT locus at the 3′ end. The red dashed-lined rectangle indicates the MAT locus. B) Fine mapping conducted by sequencing the region between markers No. 36 and No. 37 showed that in progeny SSB369 the breakpoint within the MAT locus for the run of “b” alleles is located inside the GEF1 gene, within a region of 150 bp in size.
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pgen-1004849-g005: Recombination within the MAT locus during α-α unisexual reproduction.A) Of the 42 genetic markers (only No. 21 to No. 42 are shown here for simplicity) that were analyzed for progeny from α-α unisexual reproduction, progeny SSB369 inherited “a” alleles from parental strain 431α for all but 6 markers (No. 31–No. 36; see Table 2 for detailed marker information), which were continuous and located either within or at the edge of the MAT locus. The run of allele “b” stopped between markers No. 36 and No. 37 within the MAT locus at the 5′ end, and between markers No. 30 and No. 31 that flank the MAT locus at the 3′ end. The red dashed-lined rectangle indicates the MAT locus. B) Fine mapping conducted by sequencing the region between markers No. 36 and No. 37 showed that in progeny SSB369 the breakpoint within the MAT locus for the run of “b” alleles is located inside the GEF1 gene, within a region of 150 bp in size.

Mentions: Among the 156 meiotic progeny recovered from α-α unisexual reproduction, we found evidence of crossover within the MAT locus in one progeny, SSB369. Specifically, progeny SSB369 inherited alleles from parental strain 431α (“a”) at all but 6 of the 42 genetic markers that were applied for genotyping progeny from α-α unisexual reproduction (S3 Table; Fig. 5). Interestingly, the 6 genetic markers for which progeny SSB369 inherited “b” alleles from parental strain XL280αSS are continuous and are all located within (5 markers) or at the edge (1 marker) of the MAT locus. Thus, the MAT locus of progeny SSB369 is composed of two tracks of alleles inherited from different parental strains, with alleles from parental strain 431α (“a”) at 2 loci and alleles from parental strain XL280αSS (“b”) at the other 5 loci, with the breakpoint located between markers “Inter-RPO41-STE12” (No. 36 in Table 2) and “Inter-RUM1-GEF1” (No. 37 in Table 2) (S3 Table; Fig. 5). There are two possible explanations for this observed pattern. It could be the result of a single gene conversion event encompassing the 6 loci for which progeny inherited the “b” alleles. Alternatively, it could have resulted from two crossover events that are located between markers “Inter-RPO41-STE12” and “Inter-RUM1-GEF1”, and between markers Inter-CND05590–CND05600 (No. 30 in Table 2) and Inter-BSP3-IKS1 (No. 31 in Table 2), respectively. By sequencing the region between these two markers from progeny SSB369, as well as the two parental strains, we mapped the breakpoint to an interval of 150 bp in size (between bp 1,600,099 and 1,600,248; Fig. 5) that is located within the GEF1 gene (Fig. 5). Thus, the run of alleles from parental strain XL280αSS (“b”) within the MAT locus of progeny SSB369 is more than 50 kb in size, which is likely too large to be the result of a single gene conversion event. Instead, the mosaic allele composition of the MAT locus in progeny SSB369 can be best explained as the result of a crossover event that occurred within the GEF1 gene, accompanied by another crossover event between markers No. 30 (Inter-CND05590–CND05600) and No. 31 (Inter-BSP3-IKS1) that flank the MAT locus (Fig. 5).


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

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

Recombination within the MAT locus during α-α unisexual reproduction.A) Of the 42 genetic markers (only No. 21 to No. 42 are shown here for simplicity) that were analyzed for progeny from α-α unisexual reproduction, progeny SSB369 inherited “a” alleles from parental strain 431α for all but 6 markers (No. 31–No. 36; see Table 2 for detailed marker information), which were continuous and located either within or at the edge of the MAT locus. The run of allele “b” stopped between markers No. 36 and No. 37 within the MAT locus at the 5′ end, and between markers No. 30 and No. 31 that flank the MAT locus at the 3′ end. The red dashed-lined rectangle indicates the MAT locus. B) Fine mapping conducted by sequencing the region between markers No. 36 and No. 37 showed that in progeny SSB369 the breakpoint within the MAT locus for the run of “b” alleles is located inside the GEF1 gene, within a region of 150 bp in size.
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Related In: Results  -  Collection

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

pgen-1004849-g005: Recombination within the MAT locus during α-α unisexual reproduction.A) Of the 42 genetic markers (only No. 21 to No. 42 are shown here for simplicity) that were analyzed for progeny from α-α unisexual reproduction, progeny SSB369 inherited “a” alleles from parental strain 431α for all but 6 markers (No. 31–No. 36; see Table 2 for detailed marker information), which were continuous and located either within or at the edge of the MAT locus. The run of allele “b” stopped between markers No. 36 and No. 37 within the MAT locus at the 5′ end, and between markers No. 30 and No. 31 that flank the MAT locus at the 3′ end. The red dashed-lined rectangle indicates the MAT locus. B) Fine mapping conducted by sequencing the region between markers No. 36 and No. 37 showed that in progeny SSB369 the breakpoint within the MAT locus for the run of “b” alleles is located inside the GEF1 gene, within a region of 150 bp in size.
Mentions: Among the 156 meiotic progeny recovered from α-α unisexual reproduction, we found evidence of crossover within the MAT locus in one progeny, SSB369. Specifically, progeny SSB369 inherited alleles from parental strain 431α (“a”) at all but 6 of the 42 genetic markers that were applied for genotyping progeny from α-α unisexual reproduction (S3 Table; Fig. 5). Interestingly, the 6 genetic markers for which progeny SSB369 inherited “b” alleles from parental strain XL280αSS are continuous and are all located within (5 markers) or at the edge (1 marker) of the MAT locus. Thus, the MAT locus of progeny SSB369 is composed of two tracks of alleles inherited from different parental strains, with alleles from parental strain 431α (“a”) at 2 loci and alleles from parental strain XL280αSS (“b”) at the other 5 loci, with the breakpoint located between markers “Inter-RPO41-STE12” (No. 36 in Table 2) and “Inter-RUM1-GEF1” (No. 37 in Table 2) (S3 Table; Fig. 5). There are two possible explanations for this observed pattern. It could be the result of a single gene conversion event encompassing the 6 loci for which progeny inherited the “b” alleles. Alternatively, it could have resulted from two crossover events that are located between markers “Inter-RPO41-STE12” and “Inter-RUM1-GEF1”, and between markers Inter-CND05590–CND05600 (No. 30 in Table 2) and Inter-BSP3-IKS1 (No. 31 in Table 2), respectively. By sequencing the region between these two markers from progeny SSB369, as well as the two parental strains, we mapped the breakpoint to an interval of 150 bp in size (between bp 1,600,099 and 1,600,248; Fig. 5) that is located within the GEF1 gene (Fig. 5). Thus, the run of alleles from parental strain XL280αSS (“b”) within the MAT locus of progeny SSB369 is more than 50 kb in size, which is likely too large to be the result of a single gene conversion event. Instead, the mosaic allele composition of the MAT locus in progeny SSB369 can be best explained as the result of a crossover event that occurred within the GEF1 gene, accompanied by another crossover event between markers No. 30 (Inter-CND05590–CND05600) and No. 31 (Inter-BSP3-IKS1) that flank the MAT locus (Fig. 5).

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