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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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Related in: MedlinePlus

Diagram of the Chlamydomonas reinhardtii mating locus.The MT+ (left side) and MT− (right side) haplotypes are aligned vertically with regions of synteny connected by gray shading. The three major domains are labeled as T, (Telomere Proximal, ∼82–84 kb), R (Rearranged, ∼204–396 kb), and C (Centromere Proximal, ∼116 kb). The R-domain section of each haplotype is shaded light pink (MT+) or blue (MT−). Genes are designated by black or brown pointed rectangles with pointed ends showing their relative orientation. Gene names are shown to the left or right of each gene symbol. The 16 kb repeat region in MT+ is depicted as an expansion to the left of the main diagram with unassembled regions indicated by thin lines. MT+ and MT− limited genes are boxed. Names of genes used for population studies are highlighted in yellow. Gene expression patterns compiled from this study, from [19], and from publicly available transcriptome data are denoted by colored shapes as follows: blue circle, all stages; green diamond, vegetative; pink triangle, gametic and zygotic; orange square, zygotic; open square, not detected; small black square, transcript detected but expression pattern not determined. The expression pattern shown for the SRL region is specific to the SRLb gene that is indicated by an asterisk. The thin bars to the left and right of each diagram show the region where recombination was measured in MT+×MT+ or MT−×MT− homozygous crosses. Crosshatches show markers that were scored for recombination and numbers of recombinants/total progeny scored are shown next to each recombination interval.
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pgen-1003724-g001: Diagram of the Chlamydomonas reinhardtii mating locus.The MT+ (left side) and MT− (right side) haplotypes are aligned vertically with regions of synteny connected by gray shading. The three major domains are labeled as T, (Telomere Proximal, ∼82–84 kb), R (Rearranged, ∼204–396 kb), and C (Centromere Proximal, ∼116 kb). The R-domain section of each haplotype is shaded light pink (MT+) or blue (MT−). Genes are designated by black or brown pointed rectangles with pointed ends showing their relative orientation. Gene names are shown to the left or right of each gene symbol. The 16 kb repeat region in MT+ is depicted as an expansion to the left of the main diagram with unassembled regions indicated by thin lines. MT+ and MT− limited genes are boxed. Names of genes used for population studies are highlighted in yellow. Gene expression patterns compiled from this study, from [19], and from publicly available transcriptome data are denoted by colored shapes as follows: blue circle, all stages; green diamond, vegetative; pink triangle, gametic and zygotic; orange square, zygotic; open square, not detected; small black square, transcript detected but expression pattern not determined. The expression pattern shown for the SRL region is specific to the SRLb gene that is indicated by an asterisk. The thin bars to the left and right of each diagram show the region where recombination was measured in MT+×MT+ or MT−×MT− homozygous crosses. Crosshatches show markers that were scored for recombination and numbers of recombinants/total progeny scored are shown next to each recombination interval.

Mentions: Structural data on the Chlamydomonas reinhardtii mating locus (hereafter referred to as Chlamydomonas MT) was previously based on a restriction-enzyme-mapped phage walk through both mating types [22]. In addition, the published V3 genome sequence contains portions of the plus haplotype (MT+) but its assembly was not contiguous through the mating locus [20]. An updated assembly of Chromosome 6 available through Phytozome [23] is contiguous through the MT+ region, though there are still some repeats whose copy number has not been accurately determined. We recently cloned and sequenced the minus haplotype (MT−) that allowed direct comparisons between nearly complete sequences of both mating types from Chlamydomonas (Figure 1 and [11]). Below we describe new and updated analyses of Chlamydomonas MT including two regions of the MT+ haplotype that derive from autosomal insertions, a redefined border for the R-domain, and a revised description of the 16 kb repeat region.


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)

Diagram of the Chlamydomonas reinhardtii mating locus.The MT+ (left side) and MT− (right side) haplotypes are aligned vertically with regions of synteny connected by gray shading. The three major domains are labeled as T, (Telomere Proximal, ∼82–84 kb), R (Rearranged, ∼204–396 kb), and C (Centromere Proximal, ∼116 kb). The R-domain section of each haplotype is shaded light pink (MT+) or blue (MT−). Genes are designated by black or brown pointed rectangles with pointed ends showing their relative orientation. Gene names are shown to the left or right of each gene symbol. The 16 kb repeat region in MT+ is depicted as an expansion to the left of the main diagram with unassembled regions indicated by thin lines. MT+ and MT− limited genes are boxed. Names of genes used for population studies are highlighted in yellow. Gene expression patterns compiled from this study, from [19], and from publicly available transcriptome data are denoted by colored shapes as follows: blue circle, all stages; green diamond, vegetative; pink triangle, gametic and zygotic; orange square, zygotic; open square, not detected; small black square, transcript detected but expression pattern not determined. The expression pattern shown for the SRL region is specific to the SRLb gene that is indicated by an asterisk. The thin bars to the left and right of each diagram show the region where recombination was measured in MT+×MT+ or MT−×MT− homozygous crosses. Crosshatches show markers that were scored for recombination and numbers of recombinants/total progeny scored are shown next to each recombination interval.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1003724-g001: Diagram of the Chlamydomonas reinhardtii mating locus.The MT+ (left side) and MT− (right side) haplotypes are aligned vertically with regions of synteny connected by gray shading. The three major domains are labeled as T, (Telomere Proximal, ∼82–84 kb), R (Rearranged, ∼204–396 kb), and C (Centromere Proximal, ∼116 kb). The R-domain section of each haplotype is shaded light pink (MT+) or blue (MT−). Genes are designated by black or brown pointed rectangles with pointed ends showing their relative orientation. Gene names are shown to the left or right of each gene symbol. The 16 kb repeat region in MT+ is depicted as an expansion to the left of the main diagram with unassembled regions indicated by thin lines. MT+ and MT− limited genes are boxed. Names of genes used for population studies are highlighted in yellow. Gene expression patterns compiled from this study, from [19], and from publicly available transcriptome data are denoted by colored shapes as follows: blue circle, all stages; green diamond, vegetative; pink triangle, gametic and zygotic; orange square, zygotic; open square, not detected; small black square, transcript detected but expression pattern not determined. The expression pattern shown for the SRL region is specific to the SRLb gene that is indicated by an asterisk. The thin bars to the left and right of each diagram show the region where recombination was measured in MT+×MT+ or MT−×MT− homozygous crosses. Crosshatches show markers that were scored for recombination and numbers of recombinants/total progeny scored are shown next to each recombination interval.
Mentions: Structural data on the Chlamydomonas reinhardtii mating locus (hereafter referred to as Chlamydomonas MT) was previously based on a restriction-enzyme-mapped phage walk through both mating types [22]. In addition, the published V3 genome sequence contains portions of the plus haplotype (MT+) but its assembly was not contiguous through the mating locus [20]. An updated assembly of Chromosome 6 available through Phytozome [23] is contiguous through the MT+ region, though there are still some repeats whose copy number has not been accurately determined. We recently cloned and sequenced the minus haplotype (MT−) that allowed direct comparisons between nearly complete sequences of both mating types from Chlamydomonas (Figure 1 and [11]). Below we describe new and updated analyses of Chlamydomonas MT including two regions of the MT+ haplotype that derive from autosomal insertions, a redefined border for the R-domain, and a revised description of the 16 kb repeat region.

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