Detecting heterozygosity in shotgun genome assemblies: Lessons from obligately outcrossing nematodes
The majority of nematodes are gonochoristic (dioecious) with distinct male and female sexes, but the best-studied species, Caenorhabditis elegans, is a self-fertile hermaphrodite. The sequencing of the genomes of C. elegans and a second hermaphrodite, C. briggsae, was facilitated in part by the low...
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Published in | Genome Research Vol. 19; no. 3; pp. 470 - 480 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Cold Spring Harbor Laboratory Press
01.03.2009
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Abstract | The majority of nematodes are gonochoristic (dioecious) with distinct male and female sexes, but the best-studied species, Caenorhabditis elegans, is a self-fertile hermaphrodite. The sequencing of the genomes of C. elegans and a second hermaphrodite, C. briggsae, was facilitated in part by the low amount of natural heterozygosity, which typifies selfing species. Ongoing genome projects for gonochoristic Caenorhabditis species seek to approximate this condition by intense inbreeding prior to sequencing. Here we show that despite this inbreeding, the heterozygous fraction of the whole genome shotgun assemblies of three gonochoristic Caenorhabditis species, C. brenneri, C. remanei, and C. japonica, is considerable. We first demonstrate experimentally that independently assembled sequence variants in C. remanei and C. brenneri are allelic. We then present gene-based approaches for recognizing heterozygous regions of WGS assemblies. We also develop a simple method for quantifying heterozygosity that can be applied to assemblies lacking gene annotations. Consistently we find that approximately 10% and 30% of the C. remanei and C. brenneri genomes, respectively, are represented by two alleles in the assemblies. Heterozygosity is restricted to autosomes and its retention is accompanied by substantial inbreeding depression, suggesting that it is caused by multiple recessive deleterious alleles and not merely by chance. Both the overall amount and chromosomal distribution of heterozygous DNA is highly variable between assemblies of close relatives produced by identical methodologies, and allele frequencies have continued to change after strains were sequenced. Our results highlight the impact of mating systems on genome sequencing projects. |
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AbstractList | The majority of nematodes are gonochoristic (dioecious) with distinct male and female sexes, but the best-studied species,
Caenorhabditis elegans
, is a self-fertile hermaphrodite. The sequencing of the genomes of
C. elegans
and a second hermaphrodite,
C. briggsae
, was facilitated in part by the low amount of natural heterozygosity, which typifies selfing species. Ongoing genome projects for gonochoristic
Caenorhabditis
species seek to approximate this condition by intense inbreeding prior to sequencing. Here we show that despite this inbreeding, the heterozygous fraction of the whole genome shotgun assemblies of three gonochoristic
Caenorhabditis
species,
C. brenneri
,
C. remanei
, and
C. japonica
, is considerable. We first demonstrate experimentally that independently assembled sequence variants in
C. remanei
and
C. brenneri
are allelic. We then present gene-based approaches for recognizing heterozygous regions of WGS assemblies. We also develop a simple method for quantifying heterozygosity that can be applied to assemblies lacking gene annotations. Consistently we find that ∼10% and 30% of the
C. remanei
and
C. brenneri
genomes, respectively, are represented by two alleles in the assemblies. Heterozygosity is restricted to autosomes and its retention is accompanied by substantial inbreeding depression, suggesting that it is caused by multiple recessive deleterious alleles and not merely by chance. Both the overall amount and chromosomal distribution of heterozygous DNA is highly variable between assemblies of close relatives produced by identical methodologies, and allele frequencies have continued to change after strains were sequenced. Our results highlight the impact of mating systems on genome sequencing projects. The majority of nematodes are gonochoristic (dioecious) with distinct male and female sexes, but the best-studied species, Caenorhabditis elegans, is a self-fertile hermaphrodite. The sequencing of the genomes of C. elegans and a second hermaphrodite, C. briggsae, was facilitated in part by the low amount of natural heterozygosity, which typifies selfing species. Ongoing genome projects for gonochoristic Caenorhabditis species seek to approximate this condition by intense inbreeding prior to sequencing. Here we show that despite this inbreeding, the heterozygous fraction of the whole genome shotgun assemblies of three gonochoristic Caenorhabditis species, C. brenneri, C. remanei, and C. japonica, is considerable. We first demonstrate experimentally that independently assembled sequence variants in C. remanei and C. brenneri are allelic. We then present gene-based approaches for recognizing heterozygous regions of WGS assemblies. We also develop a simple method for quantifying heterozygosity that can be applied to assemblies lacking gene annotations. Consistently we find that approximately 10% and 30% of the C. remanei and C. brenneri genomes, respectively, are represented by two alleles in the assemblies. Heterozygosity is restricted to autosomes and its retention is accompanied by substantial inbreeding depression, suggesting that it is caused by multiple recessive deleterious alleles and not merely by chance. Both the overall amount and chromosomal distribution of heterozygous DNA is highly variable between assemblies of close relatives produced by identical methodologies, and allele frequencies have continued to change after strains were sequenced. Our results highlight the impact of mating systems on genome sequencing projects. |
Author | Yang, Shiaw-Pyng Ruvinsky, Ilya Pekarek, Elizabeth Barrière, Antoine Thomas, Cristel G Haag, Eric S |
AuthorAffiliation | 2 Genome Sequencing Center, Washington University, St. Louis, Missouri 63108, USA 1 Department of Ecology and Evolution and Institute for Genomics and Systems Biology, The University of Chicago, Chicago, Illinois 60637, USA 3 Department of Biology and Molecular and Cell Biology Program, University of Maryland, College Park, Maryland 20742, USA |
AuthorAffiliation_xml | – name: 1 Department of Ecology and Evolution and Institute for Genomics and Systems Biology, The University of Chicago, Chicago, Illinois 60637, USA – name: 2 Genome Sequencing Center, Washington University, St. Louis, Missouri 63108, USA – name: 3 Department of Biology and Molecular and Cell Biology Program, University of Maryland, College Park, Maryland 20742, USA |
Author_xml | – sequence: 1 givenname: Antoine surname: Barrière fullname: Barrière, Antoine organization: Department of Ecology and Evolution and Institute for Genomics and Systems Biology, The University of Chicago, Chicago, Illinois 60637, USA – sequence: 2 givenname: Shiaw-Pyng surname: Yang fullname: Yang, Shiaw-Pyng – sequence: 3 givenname: Elizabeth surname: Pekarek fullname: Pekarek, Elizabeth – sequence: 4 givenname: Cristel G surname: Thomas fullname: Thomas, Cristel G – sequence: 5 givenname: Eric S surname: Haag fullname: Haag, Eric S – sequence: 6 givenname: Ilya surname: Ruvinsky fullname: Ruvinsky, Ilya |
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SubjectTerms | Alleles Animals Chromosome Mapping - methods Crosses, Genetic Disorders of Sex Development - genetics Female Genetic Carrier Screening - methods Genome, Helminth Heterozygote Inbreeding Methods Nematoda - genetics Sequence Analysis, DNA Species Specificity |
Title | Detecting heterozygosity in shotgun genome assemblies: Lessons from obligately outcrossing nematodes |
URI | https://www.ncbi.nlm.nih.gov/pubmed/19204328 https://search.proquest.com/docview/66986859 https://pubmed.ncbi.nlm.nih.gov/PMC2661809 |
Volume | 19 |
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