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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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R-domain gene conversion between MT+ and MT− haplotypes.Polymorphic positions in alignments of R-domain genes PR46 and PDK1 from 7 MT+ and 6 MT− isolates described in Table S7. The position in the alignment is displayed vertically above each column reading downward. The domain (dom) of the gene in which the polymorphism occurs is indicated below each column as follows: E (exon), I (intron) and U (untranslated region). For exonic positions the type of substitution (typ) is indicated as synonymous (S) or non-synonymous (N). Small insertion/deletion polymorphisms are indicated by dashes, while larger insertion/deletion polymorphisms are abbreviated as [ins] or [del]. Red background shading indicates polymorphisms specific to MT+ isolates and blue background shading indicates polymorphisms specific to MT− isolates. Bold red sequences with yellow background shading show gene tracts where MT− sequences converted to MT+. Orange and green shading show polymorphisms segregating within MT+ and MT− subgroups.
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pgen-1003724-g006: R-domain gene conversion between MT+ and MT− haplotypes.Polymorphic positions in alignments of R-domain genes PR46 and PDK1 from 7 MT+ and 6 MT− isolates described in Table S7. The position in the alignment is displayed vertically above each column reading downward. The domain (dom) of the gene in which the polymorphism occurs is indicated below each column as follows: E (exon), I (intron) and U (untranslated region). For exonic positions the type of substitution (typ) is indicated as synonymous (S) or non-synonymous (N). Small insertion/deletion polymorphisms are indicated by dashes, while larger insertion/deletion polymorphisms are abbreviated as [ins] or [del]. Red background shading indicates polymorphisms specific to MT+ isolates and blue background shading indicates polymorphisms specific to MT− isolates. Bold red sequences with yellow background shading show gene tracts where MT− sequences converted to MT+. Orange and green shading show polymorphisms segregating within MT+ and MT− subgroups.

Mentions: Gene conversion can be identified by comparing polymorphisms that are nearly fixed between the two mating-types and then identifying tracts where two or more adjacent polymorphisms have switched their pattern from one haplotype to the other [43]. Here we identified four short regions of gene conversion in the two R-domain genes that were randomly selected for this study–two tracts in PDK1 and two tracts in PR46 (Figures 6 and S6). None of the tracts were in repeat regions or microsatellites (Figure S6), and in all four cases the direction of conversion was from MT+ to MT−. One of the gene conversion tracts in PDK1 is present in both CC1952 and CC2931 (Figure 6) making its occurrence likely to predate the split between these two isolates. These previously undocumented gene conversion events may have important implications for mating locus evolution that are further elaborated below.


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)

R-domain gene conversion between MT+ and MT− haplotypes.Polymorphic positions in alignments of R-domain genes PR46 and PDK1 from 7 MT+ and 6 MT− isolates described in Table S7. The position in the alignment is displayed vertically above each column reading downward. The domain (dom) of the gene in which the polymorphism occurs is indicated below each column as follows: E (exon), I (intron) and U (untranslated region). For exonic positions the type of substitution (typ) is indicated as synonymous (S) or non-synonymous (N). Small insertion/deletion polymorphisms are indicated by dashes, while larger insertion/deletion polymorphisms are abbreviated as [ins] or [del]. Red background shading indicates polymorphisms specific to MT+ isolates and blue background shading indicates polymorphisms specific to MT− isolates. Bold red sequences with yellow background shading show gene tracts where MT− sequences converted to MT+. Orange and green shading show polymorphisms segregating within MT+ and MT− subgroups.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1003724-g006: R-domain gene conversion between MT+ and MT− haplotypes.Polymorphic positions in alignments of R-domain genes PR46 and PDK1 from 7 MT+ and 6 MT− isolates described in Table S7. The position in the alignment is displayed vertically above each column reading downward. The domain (dom) of the gene in which the polymorphism occurs is indicated below each column as follows: E (exon), I (intron) and U (untranslated region). For exonic positions the type of substitution (typ) is indicated as synonymous (S) or non-synonymous (N). Small insertion/deletion polymorphisms are indicated by dashes, while larger insertion/deletion polymorphisms are abbreviated as [ins] or [del]. Red background shading indicates polymorphisms specific to MT+ isolates and blue background shading indicates polymorphisms specific to MT− isolates. Bold red sequences with yellow background shading show gene tracts where MT− sequences converted to MT+. Orange and green shading show polymorphisms segregating within MT+ and MT− subgroups.
Mentions: Gene conversion can be identified by comparing polymorphisms that are nearly fixed between the two mating-types and then identifying tracts where two or more adjacent polymorphisms have switched their pattern from one haplotype to the other [43]. Here we identified four short regions of gene conversion in the two R-domain genes that were randomly selected for this study–two tracts in PDK1 and two tracts in PR46 (Figures 6 and S6). None of the tracts were in repeat regions or microsatellites (Figure S6), and in all four cases the direction of conversion was from MT+ to MT−. One of the gene conversion tracts in PDK1 is present in both CC1952 and CC2931 (Figure 6) making its occurrence likely to predate the split between these two isolates. These previously undocumented gene conversion events may have important implications for mating locus evolution that are further elaborated below.

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