Amplification Biases and Consistent Recovery of Loci in a Double-Digest RAD-seq Protocol
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{"title"=>"Amplification biases and consistent recovery of loci in a double-digest RAD-seq protocol", "type"=>"journal", "authors"=>[{"first_name"=>"Jeffrey M.", "last_name"=>"DaCosta", "scopus_author_id"=>"16308992800"}, {"first_name"=>"Michael D.", "last_name"=>"Sorenson", "scopus_author_id"=>"7006005330"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"600018079", "sgr"=>"84907059380", "issn"=>"19326203", "pmid"=>"25188270", "scopus"=>"2-s2.0-84907059380", "doi"=>"10.1371/journal.pone.0106713", "isbn"=>"1932-6203"}, "id"=>"219b00e8-8aa0-3c66-a581-9a5ba0d64684", "abstract"=>"A growing variety of “genotype-by-sequencing” (GBS) methods use restriction enzymes and high throughput DNA sequencing to generate data for a subset of genomic loci, allowing the simultaneous discovery and genotyping of thousands of polymorphisms in a set of multiplexed samples. We evaluated a “double-digest” restriction-site associated DNA sequencing (ddRAD-seq) protocol by 1) comparing results for a zebra finch (Taeniopygia guttata) sample with in silico predictions from the zebra finch reference genome; 2) assessing data quality for a population sample of indigobirds (Vidua spp.); and 3) testing for consistent recovery of loci across multiple samples and sequencing runs. Comparison with in silico predictions revealed that 1) over 90% of predicted, single-copy loci in our targeted size range (178–328 bp) were recovered; 2) short restriction fragments (38–178 bp) were carried through the size selection step and sequenced at appreciable depth, generating unexpected but nonetheless useful data; 3) amplification bias favored shorter, GC-rich fragments, contributing to among locus variation in sequencing depth that was strongly correlated across samples; 4) our use of restriction enzymes with a GC-rich recognition sequence resulted in an up to four-fold overrepresentation of GC-rich portions of the genome; and 5) star activity (i.e., non-specific cutting) resulted in thousands of “extra” loci sequenced at low depth. Results for three species of indigobirds show that a common set of thousands of loci can be consistently recovered across both individual samples and sequencing runs. In a run with 46 samples, we genotyped 5,996 loci in all individuals and 9,833 loci in 42 or more individuals, resulting in <1% missing data for the larger data set. We compare our approach to similar methods and discuss the range of factors (fragment library preparation, natural genetic variation, bioinformatics) influencing the recovery of a consistent set of loci among samples.", "link"=>"http://www.mendeley.com/research/amplification-biases-consistent-recovery-loci-doubledigest-radseq-protocol", "reader_count"=>222, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>8, "Librarian"=>1, "Researcher"=>51, "Student > Doctoral Student"=>15, "Student > Ph. D. Student"=>70, "Student > Postgraduate"=>6, "Student > Master"=>48, "Other"=>6, "Student > Bachelor"=>9, "Professor"=>7}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>8, "Librarian"=>1, "Researcher"=>51, "Student > Doctoral Student"=>15, "Student > Ph. D. Student"=>70, "Student > Postgraduate"=>6, "Student > Master"=>48, "Other"=>6, "Student > Bachelor"=>9, "Professor"=>7}, "reader_count_by_subject_area"=>{"Unspecified"=>4, "Environmental Science"=>13, "Biochemistry, Genetics and Molecular Biology"=>30, "Nursing and Health Professions"=>1, "Agricultural and Biological Sciences"=>172, "Medicine and Dentistry"=>1, "Arts and Humanities"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>172}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>30}, "Unspecified"=>{"Unspecified"=>4}, "Environmental Science"=>{"Environmental Science"=>13}, "Arts and Humanities"=>{"Arts and Humanities"=>1}}, "reader_count_by_country"=>{"New Zealand"=>1, "Republic of Singapore"=>1, "Canada"=>1, "Netherlands"=>1, "United States"=>10, "Brazil"=>3, "South Africa"=>1, "Italy"=>1, "Switzerland"=>3, "Germany"=>2, "Spain"=>2}, "group_count"=>6}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1661604"], "description"=>"<p>Sequencing depth for 160 selected loci (rows), including 40 loci in each of four narrow size ranges, is shown for 10 randomly selected samples (columns) from each of seven pooled libraries. The 160 loci illustrated are a subset of the 5,996 loci recovered in all 46 indigobirds sequenced in the RAD10 sequencing run. Overall sequencing depth for each individual sample is show in the bar graph at top. Sequencing depth for each locus is indicated by color (see scale at bottom of figure), with red indicating no data. See text for more information.</p>", "links"=>[], "tags"=>["methods use restriction enzymes", "gbs", "size selection step", "fragment library preparation", "insilico predictions", "thousand", "zebra finch reference genome", "loci", "sample", "throughput DNA sequencing", "data", "depth"], "article_id"=>1161280, "categories"=>["Biological Sciences"], "users"=>["Jeffrey M. DaCosta", "Michael D. Sorenson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0106713.g006", "stats"=>{"downloads"=>1, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Recovery_of_indigobird_ddRAD_loci_across_individual_samples_and_sequencing_runs_/1161280", "title"=>"Recovery of indigobird ddRAD loci across individual samples and sequencing runs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-04 03:06:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/1661602"], "description"=>"<p>Data are shown for 1,721 loci recovered in all 46 indigobirds in the RAD10 sequencing run (<i>n</i> = 79,166 genotypes). The area of data points is proportional to the number of individual genotypes at each coordinate. Read counts for heterozygous genotypes (<i>n</i> = 11,761) were consistent with random sampling from a binomial distribution with probability 0.5 (i.e., Mendelian expectations), resulting in a strongly trimodal distribution of read counts. Most homozygous genotypes (<i>n</i> = 67,405) were based on 100% of reads (light grey) matching one of the two alleles at a given locus; only 64 genotypes (0.09%) scored as homozygous had one or more high quality reads (magenta) matching the alternative allele.</p>", "links"=>[], "tags"=>["methods use restriction enzymes", "gbs", "size selection step", "fragment library preparation", "insilico predictions", "thousand", "zebra finch reference genome", "loci", "sample", "throughput DNA sequencing", "data", "depth"], "article_id"=>1161278, "categories"=>["Biological Sciences"], "users"=>["Jeffrey M. DaCosta", "Michael D. Sorenson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0106713.g004", "stats"=>{"downloads"=>2, "page_views"=>31, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Read_counts_for_indigobird_ddRAD_loci_with_a_single_bi_allelic_SNP_/1161278", "title"=>"Read counts for indigobird ddRAD loci with a single bi-allelic SNP.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-04 03:06:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/1661607"], "description"=>"<p>Analysis based on a set of 5,996 loci genotyped in all 46 samples in RAD10 with per locus sequencing depth ≥5 reads for all 46 samples.</p><p>Summary statistics characterizing the performance of multiple sequencing runs in recovering a core set of loci.</p>", "links"=>[], "tags"=>["methods use restriction enzymes", "gbs", "size selection step", "fragment library preparation", "insilico predictions", "thousand", "zebra finch reference genome", "loci", "sample", "throughput DNA sequencing", "data", "depth"], "article_id"=>1161283, "categories"=>["Biological Sciences"], "users"=>["Jeffrey M. DaCosta", "Michael D. Sorenson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0106713.t003", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_statistics_characterizing_the_performance_of_multiple_sequencing_runs_in_recovering_a_core_set_of_loci_/1161283", "title"=>"Summary statistics characterizing the performance of multiple sequencing runs in recovering a core set of loci.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-09-04 03:06:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/1661606"], "description"=>"<p>See <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106713#s2\" target=\"_blank\">Methods</a> for more information on categories of “flagged” genotypes.</p><p>*Includes loci with ≥ one read for at least 42 of 46 samples and no more than 2 “flagged” genotypes.</p><p>Genotyping success for 9,833 loci recovered in at least 42 of 46 indigobird samples in the “RAD10” run.</p>", "links"=>[], "tags"=>["methods use restriction enzymes", "gbs", "size selection step", "fragment library preparation", "insilico predictions", "thousand", "zebra finch reference genome", "loci", "sample", "throughput DNA sequencing", "data", "depth"], "article_id"=>1161282, "categories"=>["Biological Sciences"], "users"=>["Jeffrey M. DaCosta", "Michael D. Sorenson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0106713.t002", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genotyping_success_for_9_833_loci_recovered_in_at_least_42_of_46_indigobird_samples_in_the_8220_RAD10_8221_run_/1161282", "title"=>"Genotyping success for 9,833 loci recovered in at least 42 of 46 indigobird samples in the “RAD10” run.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-09-04 03:06:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/1661601"], "description"=>"<p>Includes 7,819 loci that had one or a “best” BLAST hit and were genotyped in at least 42 of 46 samples (<i>n</i> = 5,045 variable loci, <i>n</i> = 2,774 constant loci). Data for the “chrUn” contig and small contigs with no BLAST hits (e.g., “chr16”, “LG2”, “LG5”) are excluded. (A) The number of loci mapped to each chromosome as a function of chromosome length. (B) The density of loci as a function of chromosome length. (C) The density of loci as a function of chromosome GC content. (D) The proportion of loci that was variable as a function of chromosome GC content. The Z-chromosome is indicated by a red point in each panel and was not used in regression analyses.</p>", "links"=>[], "tags"=>["methods use restriction enzymes", "gbs", "size selection step", "fragment library preparation", "insilico predictions", "thousand", "zebra finch reference genome", "loci", "sample", "throughput DNA sequencing", "data", "depth"], "article_id"=>1161277, "categories"=>["Biological Sciences"], "users"=>["Jeffrey M. DaCosta", "Michael D. Sorenson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0106713.g003", "stats"=>{"downloads"=>0, "page_views"=>34, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genomic_distribution_of_indigobird_ddRAD_loci_based_on_BLAST_results_against_the_zebra_finch_reference_genome_/1161277", "title"=>"Genomic distribution of indigobird ddRAD loci based on BLAST results against the zebra finch reference genome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-04 03:06:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/1661600"], "description"=>"<p>Categories from top to bottom include: loci mapping as expected to predicted SbfI-EcoRI restriction fragments≤328 bp in length; all loci beginning at a genomic location similar but not identical to the canonical SbfI recognition sequence (1–4 mismatches); subset of loci with one mismatch in position 1 or 8 of the SbfI recognition sequence; subset of loci with one mismatch in positions 2 through 7 of the SbfI recognition sequence; loci mapping to a genomic SbfI site without an EcoRI site within 328 bp; and loci mapping to a predicted SbfI-SbfI restriction fragment less than 328 bp in length.</p>", "links"=>[], "tags"=>["methods use restriction enzymes", "gbs", "size selection step", "fragment library preparation", "insilico predictions", "thousand", "zebra finch reference genome", "loci", "sample", "throughput DNA sequencing", "data", "depth"], "article_id"=>1161276, "categories"=>["Biological Sciences"], "users"=>["Jeffrey M. DaCosta", "Michael D. Sorenson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0106713.g002", "stats"=>{"downloads"=>5, "page_views"=>45, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sequencing_depth_for_single_copy_ddRAD_loci_in_relation_to_the_corresponding_sequence_in_the_zebra_finch_reference_genome_/1161276", "title"=>"Sequencing depth for single copy ddRAD loci in relation to the corresponding sequence in the zebra finch reference genome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-04 03:06:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/1661597"], "description"=>"<p>(A) Proportion of predicted loci recovered at three different minimum depth thresholds as a function of predicted fragment length. Each data point represents the proportion of ∼140–220 predicted loci recovered in a given 10 bp size range. Dashed vertical lines represent the upper and lower bounds of the size range isolated from the agarose gel. (B) Sequencing depth for recovered (depth ≥1), single-copy loci in the 32–500 bp size range (includes 5,232 of 5,783 predicted loci in the 38–328 bp size range). (C) The relationship between GC content and sequencing depth for zebra finch ddRAD loci. Data are shown for predicted, single-copy loci recovered at a depth ≥1 in three selected subsets of the overall size range (<i>n</i> = 502, 466, and 445 loci in the 100–125, 200–225, and 300–325 bp size ranges, respectively). The predicted length and GC content of each locus are based on the full-length fragment in the reference genome, inclusive of the SbfI and EcoRI restriction sites on either end. Note that the y-axis is on a logarithmic scale in (B) and (C).</p>", "links"=>[], "tags"=>["methods use restriction enzymes", "gbs", "size selection step", "fragment library preparation", "insilico predictions", "thousand", "zebra finch reference genome", "loci", "sample", "throughput DNA sequencing", "data", "depth"], "article_id"=>1161273, "categories"=>["Biological Sciences"], "users"=>["Jeffrey M. DaCosta", "Michael D. Sorenson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0106713.g001", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Recovery_and_sequencing_depth_for_predicted_single_copy_ddRAD_loci_in_the_empirical_zebra_finch_data_/1161273", "title"=>"Recovery and sequencing depth for predicted, single-copy ddRAD loci in the empirical zebra finch data.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-04 03:06:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/1661609", "https://ndownloader.figshare.com/files/1661610"], "description"=>"<div><p>A growing variety of “genotype-by-sequencing” (GBS) methods use restriction enzymes and high throughput DNA sequencing to generate data for a subset of genomic loci, allowing the simultaneous discovery and genotyping of thousands of polymorphisms in a set of multiplexed samples. We evaluated a “double-digest” restriction-site associated DNA sequencing (ddRAD-seq) protocol by 1) comparing results for a zebra finch (<i>Taeniopygia guttata</i>) sample with <i>in</i><i>silico</i> predictions from the zebra finch reference genome; 2) assessing data quality for a population sample of indigobirds (<i>Vidua</i> spp.); and 3) testing for consistent recovery of loci across multiple samples and sequencing runs. Comparison with <i>in</i><i>silico</i> predictions revealed that 1) over 90% of predicted, single-copy loci in our targeted size range (178–328 bp) were recovered; 2) short restriction fragments (38–178 bp) were carried through the size selection step and sequenced at appreciable depth, generating unexpected but nonetheless useful data; 3) amplification bias favored shorter, GC-rich fragments, contributing to among locus variation in sequencing depth that was strongly correlated across samples; 4) our use of restriction enzymes with a GC-rich recognition sequence resulted in an up to four-fold overrepresentation of GC-rich portions of the genome; and 5) star activity (i.e., non-specific cutting) resulted in thousands of “extra” loci sequenced at low depth. Results for three species of indigobirds show that a common set of thousands of loci can be consistently recovered across both individual samples and sequencing runs. In a run with 46 samples, we genotyped 5,996 loci in all individuals and 9,833 loci in 42 or more individuals, resulting in <1% missing data for the larger data set. We compare our approach to similar methods and discuss the range of factors (fragment library preparation, natural genetic variation, bioinformatics) influencing the recovery of a consistent set of loci among samples.</p></div>", "links"=>[], "tags"=>["methods use restriction enzymes", "gbs", "size selection step", "fragment library preparation", "insilico predictions", "thousand", "zebra finch reference genome", "loci", "sample", "throughput DNA sequencing", "data", "depth"], "article_id"=>1161285, "categories"=>["Biological Sciences"], "users"=>["Jeffrey M. DaCosta", "Michael D. Sorenson"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0106713.s001", "https://dx.doi.org/10.1371/journal.pone.0106713.s002"], "stats"=>{"downloads"=>16, "page_views"=>24, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Amplification_Biases_and_Consistent_Recovery_of_Loci_in_a_Double_Digest_RAD_seq_Protocol_/1161285", "title"=>"Amplification Biases and Consistent Recovery of Loci in a Double-Digest RAD-seq Protocol", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-09-04 03:06:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/1661608"], "description"=>"<p>All reported values are based on <i>in</i><i>silico</i> digest of the zebra finch reference genome. Table compares our “realized” size range (with “small fragment carryover”, see text) with two size selection options employed by Peterson <i>et al</i>. <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106713#pone.0106713-Peterson1\" target=\"_blank\">[6]</a>.</p><p>Number of predicted ddRAD loci in the zebra finch genome for alternative restriction enzymes and fragment size ranges.</p>", "links"=>[], "tags"=>["methods use restriction enzymes", "gbs", "size selection step", "fragment library preparation", "insilico predictions", "thousand", "zebra finch reference genome", "loci", "sample", "throughput DNA sequencing", "data", "depth"], "article_id"=>1161284, "categories"=>["Biological Sciences"], "users"=>["Jeffrey M. DaCosta", "Michael D. Sorenson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0106713.t004", "stats"=>{"downloads"=>5, "page_views"=>97, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Number_of_predicted_ddRAD_loci_in_the_zebra_finch_genome_for_alternative_restriction_enzymes_and_fragment_size_ranges_/1161284", "title"=>"Number of predicted ddRAD loci in the zebra finch genome for alternative restriction enzymes and fragment size ranges.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-09-04 03:06:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/1661605"], "description"=>"<p>*Using SbfI enzyme.</p><p>**Using “narrow” size range (see <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0106713#pone.0106713-Peterson1\" target=\"_blank\">[6]</a>).</p><p>***Using selective adapters.</p><p>To facilitate comparison, the expected number for each method is estimated for the zebra finch genome based on the specific restriction enzymes and other parameters (e.g., size selection) used in each study.</p><p>Examples of genotype-by-sequencing (GBS) methods using restriction enzymes and high throughput DNA sequencing to select, sequence and genotype a large set of loci across multiple samples.</p>", "links"=>[], "tags"=>["methods use restriction enzymes", "gbs", "size selection step", "fragment library preparation", "insilico predictions", "thousand", "zebra finch reference genome", "loci", "sample", "throughput DNA sequencing", "data", "depth"], "article_id"=>1161281, "categories"=>["Biological Sciences"], "users"=>["Jeffrey M. DaCosta", "Michael D. Sorenson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0106713.t001", "stats"=>{"downloads"=>1, "page_views"=>21, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Examples_of_genotype_by_sequencing_GBS_methods_using_restriction_enzymes_and_high_throughput_DNA_sequencing_to_select_sequence_and_genotype_a_large_set_of_loci_across_multiple_samples_/1161281", "title"=>"Examples of genotype-by-sequencing (GBS) methods using restriction enzymes and high throughput DNA sequencing to select, sequence and genotype a large set of loci across multiple samples.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-09-04 03:06:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/1661603"], "description"=>"<p>(A) Number of heterozygotes and (B) number of homozygotes for the rare allele versus rare allele frequency for 1,721 loci with a single bi-allelic SNP. The area of data points is proportional to the number of individual genotypes at each coordinate; observed relationship (sold lines), expected (dotted lines). Loci deviating from Hardy-Weinberg expectations are highlighted in green and red. (C) Comparison of the empirical allele frequency distribution for the same 1,721 loci with neutral expectations for a population of constant size. (D) Distribution of polymorphisms among full-length (97 bp) loci genotyped in all 46 samples in RAD10 compared to a Poisson distribution, which assumes equal evolutionary rates across loci.</p>", "links"=>[], "tags"=>["methods use restriction enzymes", "gbs", "size selection step", "fragment library preparation", "insilico predictions", "thousand", "zebra finch reference genome", "loci", "sample", "throughput DNA sequencing", "data", "depth"], "article_id"=>1161279, "categories"=>["Biological Sciences"], "users"=>["Jeffrey M. DaCosta", "Michael D. Sorenson"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0106713.g005", "stats"=>{"downloads"=>6, "page_views"=>75, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Comparison_of_indigobird_ddRAD_results_to_population_genetic_expectations_/1161279", "title"=>"Comparison of indigobird ddRAD results to population genetic expectations.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-09-04 03:06:53"}

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Relative Metric

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