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Species and population level molecular profiling reveals cryptic recombination and emergent asymmetry in the dimorphic mating locus of C. reinhardtii.

De Hoff PL, Ferris P, Olson BJ, Miyagi A, Geng S, Umen JG - PLoS Genet. (2013)

Bottom Line: We used new sequence information to redefine the genetic contents of MT and found repeated translocations from autosomes as well as sexually controlled expression patterns for several newly identified genes.Our population data revealed two previously unreported types of genetic exchange in Chlamydomonas MT--gene conversion in the rearranged domains, and crossover exchanges in flanking domains--both of which contribute to maintenance of genetic homogeneity between haplotypes.Together our findings reveal new evolutionary dynamics for mating loci and have implications for the evolution of heteromorphic sex chromosomes and other non-recombining genomic regions.

View Article: PubMed Central - PubMed

Affiliation: The Salk Institute for Biological Studies, La Jolla, California, United States of America.

ABSTRACT
Heteromorphic sex-determining regions or mating-type loci can contain large regions of non-recombining sequence where selection operates under different constraints than in freely recombining autosomal regions. Detailed studies of these non-recombining regions can provide insights into how genes are gained and lost, and how genetic isolation is maintained between mating haplotypes or sex chromosomes. The Chlamydomonas reinhardtii mating-type locus (MT) is a complex polygenic region characterized by sequence rearrangements and suppressed recombination between its two haplotypes, MT+ and MT-. We used new sequence information to redefine the genetic contents of MT and found repeated translocations from autosomes as well as sexually controlled expression patterns for several newly identified genes. We examined sequence diversity of MT genes from wild isolates of C. reinhardtii to investigate the impacts of recombination suppression. Our population data revealed two previously unreported types of genetic exchange in Chlamydomonas MT--gene conversion in the rearranged domains, and crossover exchanges in flanking domains--both of which contribute to maintenance of genetic homogeneity between haplotypes. To investigate the cause of blocked recombination in MT we assessed recombination rates in crosses where the parents were homozygous at MT. While normal recombination was restored in MT+ ×MT+ crosses, it was still suppressed in MT- ×MT- crosses. These data revealed an underlying asymmetry in the two MT haplotypes and suggest that sequence rearrangements are insufficient to fully account for recombination suppression. Together our findings reveal new evolutionary dynamics for mating loci and have implications for the evolution of heteromorphic sex chromosomes and other non-recombining genomic regions.

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Haplotype networks of MT and autosomal genes.A–E. Unrooted parsimony splits networks of R-domain genes A. PR46 and B. PDK1, C/T domain genes C. SAD1 and D. SPP3, and autosomal gene E. GP1. Distances between nodes represent number of nucleotide changes. Bootstrap values from 1000 replicates are shown next to edges and expressed as rounded percentages. Circular nodes represent individual isolates with red and blue shading to indicate MT+ and MT− respectively. Node size is proportional to the number of isolates in the node.
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pgen-1003724-g005: Haplotype networks of MT and autosomal genes.A–E. Unrooted parsimony splits networks of R-domain genes A. PR46 and B. PDK1, C/T domain genes C. SAD1 and D. SPP3, and autosomal gene E. GP1. Distances between nodes represent number of nucleotide changes. Bootstrap values from 1000 replicates are shown next to edges and expressed as rounded percentages. Circular nodes represent individual isolates with red and blue shading to indicate MT+ and MT− respectively. Node size is proportional to the number of isolates in the node.

Mentions: We graphically depicted the genetic relationships between MT+ and MT− allelic diversity by constructing unrooted parsimony-based networks that are similar to phylogenetic trees, but accommodate incongruities by incorporating alternative paths or splits [42]. As suggested above, the networks for the R-domain genes PR46 and PDK1 show clear differentiation between MT+ and MT− isolates (Figure 5A,B) with tight clustering of the MT+ alleles. In contrast, genes in the T- and C-domains (SAD1 and SPP3) show complete intermixing between MT+ and MT− isolates (Figure 5C,D), with no apparent association of specific polymorphisms with mating-type. The MAT3 gene did show some MT-associated differentiation, but this differentiation did not extend to the nearby SAD1 gene (Figure S3) or to the SPP3 gene indicating that these three loci are all separable from each other and from the R-domain by recombination. As expected none of the polymorphisms present in autosomal genes (GP1, YPT4, IDA5, CBLP) showed association with mating haplotype (Figures 5E and S3).


Species and population level molecular profiling reveals cryptic recombination and emergent asymmetry in the dimorphic mating locus of C. reinhardtii.

De Hoff PL, Ferris P, Olson BJ, Miyagi A, Geng S, Umen JG - PLoS Genet. (2013)

Haplotype networks of MT and autosomal genes.A–E. Unrooted parsimony splits networks of R-domain genes A. PR46 and B. PDK1, C/T domain genes C. SAD1 and D. SPP3, and autosomal gene E. GP1. Distances between nodes represent number of nucleotide changes. Bootstrap values from 1000 replicates are shown next to edges and expressed as rounded percentages. Circular nodes represent individual isolates with red and blue shading to indicate MT+ and MT− respectively. Node size is proportional to the number of isolates in the node.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3757049&req=5

pgen-1003724-g005: Haplotype networks of MT and autosomal genes.A–E. Unrooted parsimony splits networks of R-domain genes A. PR46 and B. PDK1, C/T domain genes C. SAD1 and D. SPP3, and autosomal gene E. GP1. Distances between nodes represent number of nucleotide changes. Bootstrap values from 1000 replicates are shown next to edges and expressed as rounded percentages. Circular nodes represent individual isolates with red and blue shading to indicate MT+ and MT− respectively. Node size is proportional to the number of isolates in the node.
Mentions: We graphically depicted the genetic relationships between MT+ and MT− allelic diversity by constructing unrooted parsimony-based networks that are similar to phylogenetic trees, but accommodate incongruities by incorporating alternative paths or splits [42]. As suggested above, the networks for the R-domain genes PR46 and PDK1 show clear differentiation between MT+ and MT− isolates (Figure 5A,B) with tight clustering of the MT+ alleles. In contrast, genes in the T- and C-domains (SAD1 and SPP3) show complete intermixing between MT+ and MT− isolates (Figure 5C,D), with no apparent association of specific polymorphisms with mating-type. The MAT3 gene did show some MT-associated differentiation, but this differentiation did not extend to the nearby SAD1 gene (Figure S3) or to the SPP3 gene indicating that these three loci are all separable from each other and from the R-domain by recombination. As expected none of the polymorphisms present in autosomal genes (GP1, YPT4, IDA5, CBLP) showed association with mating haplotype (Figures 5E and S3).

Bottom Line: We used new sequence information to redefine the genetic contents of MT and found repeated translocations from autosomes as well as sexually controlled expression patterns for several newly identified genes.Our population data revealed two previously unreported types of genetic exchange in Chlamydomonas MT--gene conversion in the rearranged domains, and crossover exchanges in flanking domains--both of which contribute to maintenance of genetic homogeneity between haplotypes.Together our findings reveal new evolutionary dynamics for mating loci and have implications for the evolution of heteromorphic sex chromosomes and other non-recombining genomic regions.

View Article: PubMed Central - PubMed

Affiliation: The Salk Institute for Biological Studies, La Jolla, California, United States of America.

ABSTRACT
Heteromorphic sex-determining regions or mating-type loci can contain large regions of non-recombining sequence where selection operates under different constraints than in freely recombining autosomal regions. Detailed studies of these non-recombining regions can provide insights into how genes are gained and lost, and how genetic isolation is maintained between mating haplotypes or sex chromosomes. The Chlamydomonas reinhardtii mating-type locus (MT) is a complex polygenic region characterized by sequence rearrangements and suppressed recombination between its two haplotypes, MT+ and MT-. We used new sequence information to redefine the genetic contents of MT and found repeated translocations from autosomes as well as sexually controlled expression patterns for several newly identified genes. We examined sequence diversity of MT genes from wild isolates of C. reinhardtii to investigate the impacts of recombination suppression. Our population data revealed two previously unreported types of genetic exchange in Chlamydomonas MT--gene conversion in the rearranged domains, and crossover exchanges in flanking domains--both of which contribute to maintenance of genetic homogeneity between haplotypes. To investigate the cause of blocked recombination in MT we assessed recombination rates in crosses where the parents were homozygous at MT. While normal recombination was restored in MT+ ×MT+ crosses, it was still suppressed in MT- ×MT- crosses. These data revealed an underlying asymmetry in the two MT haplotypes and suggest that sequence rearrangements are insufficient to fully account for recombination suppression. Together our findings reveal new evolutionary dynamics for mating loci and have implications for the evolution of heteromorphic sex chromosomes and other non-recombining genomic regions.

Show MeSH
Related in: MedlinePlus