Following Tetraploidy in Maize, a Short Deletion Mechanism Removed Genes Preferentially from One of the Two Homeologs
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{"title"=>"Following tetraploidy in maize, a short deletion mechanism removed genes preferentially from one of the two homeologs", "type"=>"journal", "authors"=>[{"first_name"=>"Margaret R.", "last_name"=>"Woodhouse", "scopus_author_id"=>"12766256900"}, {"first_name"=>"James C.", "last_name"=>"Schnable", "scopus_author_id"=>"36098331900"}, {"first_name"=>"Brent S.", "last_name"=>"Pedersen", "scopus_author_id"=>"7201713423"}, {"first_name"=>"Eric", "last_name"=>"Lyons", "scopus_author_id"=>"35599112200"}, {"first_name"=>"Damon", "last_name"=>"Lisch", "scopus_author_id"=>"6603800277"}, {"first_name"=>"Shabarinath", "last_name"=>"Subramaniam", "scopus_author_id"=>"55414961100"}, {"first_name"=>"Michael", "last_name"=>"Freeling", "scopus_author_id"=>"7005942891"}], "year"=>2010, "source"=>"PLoS Biology", "identifiers"=>{"scopus"=>"2-s2.0-77954741256", "sgr"=>"77954741256", "issn"=>"15449173", "doi"=>"10.1371/journal.pbio.1000409", "pmid"=>"20613864", "isbn"=>"1545-7885 (Electronic)\\r1544-9173 (Linking)", "pui"=>"359202931"}, "id"=>"783de9db-07c2-3555-912b-e73c952cdf39", "abstract"=>"Previous work in Arabidopsis showed that after an ancient tetraploidy event, genes were preferentially removed from one of the two homologs, a process known as fractionation. The mechanism of fractionation is unknown. We sought to determine whether such preferential, or biased, fractionation exists in maize and, if so, whether a specific mechanism could be implicated in this process. We studied the process of fractionation using two recently sequenced grass species: sorghum and maize. The maize lineage has experienced a tetraploidy since its divergence from sorghum approximately 12 million years ago, and fragments of many knocked-out genes retain enough sequence similarity to be easily identifiable. Using sorghum exons as the query sequence, we studied the fate of both orthologous genes in maize following the maize tetraploidy. We show that genes are predominantly lost, not relocated, and that single-gene loss by deletion is the rule. Based on comparisons with orthologous sorghum and rice genes, we also infer that the sequences present before the deletion events were flanked by short direct repeats, a signature of intra-chromosomal recombination. Evidence of this deletion mechanism is found 2.3 times more frequently on one of the maize homologs, consistent with earlier observations of biased fractionation. The over-fractionated homolog is also a greater than 3-fold better target for transposon removal, but does not have an observably higher synonymous base substitution rate, nor could we find differentially placed methylation domains. We conclude that fractionation is indeed biased in maize and that intra-chromosomal or possibly a similar illegitimate recombination is the primary mechanism by which fractionation occurs. The mechanism of intra-chromosomal recombination explains the observed bias in both gene and transposon loss in the maize lineage. The existence of fractionation bias demonstrates that the frequency of deletion is modulated. Among the evolutionary benefits of this deletion/fractionation mechanism is bulk DNA removal and the generation of novel combinations of regulatory sequences and coding regions.", "link"=>"http://www.mendeley.com/research/following-tetraploidy-maize-short-deletion-mechanism-removed-genes-preferentially-one-two-homeologs", "reader_count"=>153, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>18, "Researcher"=>44, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>45, "Student > Postgraduate"=>4, "Student > Master"=>7, "Other"=>5, "Student > Bachelor"=>10, "Lecturer > Senior Lecturer"=>1, "Professor"=>15}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>18, "Researcher"=>44, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>45, "Student > Postgraduate"=>4, "Student > Master"=>7, "Other"=>5, "Student > Bachelor"=>10, "Lecturer > Senior Lecturer"=>1, "Professor"=>15}, "reader_count_by_subject_area"=>{"Unspecified"=>6, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>10, "Agricultural and Biological Sciences"=>131, "Physics and Astronomy"=>1, "Chemistry"=>1, "Social Sciences"=>1, "Computer Science"=>2}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>131}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>10}, "Unspecified"=>{"Unspecified"=>6}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"United States"=>18, "Japan"=>1, "United Kingdom"=>1, "Spain"=>1, "Canada"=>2, "Austria"=>1, "Netherlands"=>1, "Korea (South)"=>1, "Belgium"=>1, "China"=>2, "Taiwan"=>1, "Brazil"=>2, "Mexico"=>1, "Australia"=>2}, "group_count"=>6}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/842822"], "description"=>"<p>Note that more than one gap, a single deletion, may exist within the exons identified in our search. In one case, the maize homeolog corresponding to <i>Sb10g030110</i> had gaps in two separate exons (denoted as “1” and “2,” respectively).</p>", "links"=>[], "tags"=>["analyses", "16", "deletions", "exons"], "article_id"=>513280, "categories"=>["Genetics"], "users"=>["Margaret R. Woodhouse", "James C. Schnable", "Brent S. Pedersen", "Eric Lyons", "Damon Lisch", "Shabarinath Subramaniam", "Michael Freeling"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000409.t002", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Repeat_sequence_signature_analyses_of_16_Zm_deletions_within_exons_of_eight_genes_/513280", "title"=>"Repeat sequence signature analyses of 16 <i>Zm</i> deletions within exons of eight genes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-06-29 00:54:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/842865"], "description"=>"<p>When a feature is equally represented on both homeologs, then its under/over ratio will be approximately 1, but when a feature is biased with regard to fractionation, then the under/over ratio will differ significantly from 1. All data to the right of the empty column involve under/over ratios for some or all of the nine control regions. The fractionation bias ratios of Column H are less than 1 because the under-fractionated chromosome, while longer, has fewer deleted genes. Invert these fractions to compare with the greater than 1 ratios of Columns I, J, and K. ND = no data.</p>", "links"=>[], "tags"=>["fractionation", "designation", "homeolog", "over-fractionated"], "article_id"=>513318, "categories"=>["Genetics"], "users"=>["Margaret R. Woodhouse", "James C. Schnable", "Brent S. Pedersen", "Eric Lyons", "Damon Lisch", "Shabarinath Subramaniam", "Michael Freeling"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000409.t001", "stats"=>{"downloads"=>4, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_organization_of_fractionation_and_similar_data_based_on_the_designation_Zm_under_fractionated_u_homeolog_and_Zm_over_fractionated_homeolog_o_/513318", "title"=>"The organization of fractionation and similar data based on the designation <i>Zm</i>-under-fractionated (u) homeolog and <i>Zm</i> over-fractionated homeolog (o).", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-06-29 00:55:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/842545"], "description"=>"<p>(A) Cartoon of a GEvo blastn comparison graphic depicting a 13-gene stretch of sorghum with the two orthologous regions of maize. Sorghum nucleotides were masked except those in official gene models or genes shared between sorghum and maize (SI1); maize DNA was masked for repeat sequences. Blastn high scoring pairs (hits) are colored orange if they are <i>Sb-Zm1</i> and purple if they are <i>Sb-Zm2</i>. Colored lines indicate orthology. The code B021BB2DDDB10B abbreviates these data, where B = both genes remain, 0 = gene missing in syntenous <i>Zm</i> positions (these are discarded), 1 = the gene on <i>Zm1</i> remains alone because its homeolog was deleted, 2 = the gene on <i>Zm2</i> remains alone because its homeolog was deleted, and D = local duplicates of an arbitrary mother gene leftmost in the cluster (D's are discarded). Therefore, the essential code for this 13-gene <i>Sb</i> stretch reduces to B21BB2B1B. The circle indicates a <i>Zm1</i> gene that has some completely and some partially deleted exons; we noted these partially fractionated genes for further research, but we counted them as present (B). The brackets enclose clusters of tandemly duplicated genes in both <i>Sb</i> and <i>Zm2</i>. The arrow indicates a single gene in <i>Sb</i> hitting a reverse tandem duplication in maize; maize genes like this one were counted as present. Please use <a href=\"http://genomevolution.org/r/37e\" target=\"_blank\">http://genomevolution.org/r/37e</a> to reproduce on-the-fly the <i>Sb2</i> region blast experiment, the region containing <i>Sb02g030760-Sb02g030950</i> drawn above. (B) Using the same color code of the panel above, these are two exemplary small regions from the total of 37 regions comprising our syntenic dataset. The regions exemplifying fractionation bias (AL3–7) and no bias (AL3–8) are color-coded in such a way that the number of gene deletions suffered by <i>Zm</i> homeolog 1 versus <i>Zm</i> homeolog 2 is easy to count. A 1∶1 (<i>p</i> = 0.5) ratio of these deletions computes to not biased. <i>p</i>≤0.1 is weak support and ≤0.05 is strong support that these deletions significantly deviate from this 1∶1 null hypothesis.</p>", "links"=>[], "tags"=>["maize", "homeologous", "genes", "deleted"], "article_id"=>513001, "categories"=>["Genetics"], "users"=>["Margaret R. Woodhouse", "James C. Schnable", "Brent S. Pedersen", "Eric Lyons", "Damon Lisch", "Shabarinath Subramaniam", "Michael Freeling"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000409.g003", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Determining_which_maize_homeologous_genes_were_deleted_following_tetraploidy_/513001", "title"=>"Determining which maize homeologous genes were deleted following tetraploidy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-29 00:50:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/842330"], "description"=>"<p>Inferred, ancient (at least 5 million years old) tetraploidies are identified as stars. Citations are included in a recent review <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000409#pbio.1000409-Freeling2\" target=\"_blank\">[19]</a>, except for the double tetraploidy at the base of the monocots <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000409#pbio.1000409-Tang1\" target=\"_blank\">[35]</a> and the placement of the legume-specific tetraploidy (our tentative conclusion).</p>", "links"=>[], "tags"=>["pruned", "phylogenetic", "sequenced", "genomes", "flowering"], "article_id"=>512785, "categories"=>["Genetics"], "users"=>["Margaret R. Woodhouse", "James C. Schnable", "Brent S. Pedersen", "Eric Lyons", "Damon Lisch", "Shabarinath Subramaniam", "Michael Freeling"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000409.g001", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_A_heavily_pruned_phylogenetic_tree_of_the_sequenced_genomes_of_flowering_plants_/512785", "title"=>"A heavily pruned phylogenetic tree of the sequenced genomes of flowering plants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-29 00:46:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/842461"], "description"=>"<p>Lines connect homeologous genes retained as pairs, called “retained genes.” Note that retained genes cluster automatically after fractionation.</p>", "links"=>[], "tags"=>["illustrating", "fractionation", "biased"], "article_id"=>512916, "categories"=>["Genetics"], "users"=>["Margaret R. Woodhouse", "James C. Schnable", "Brent S. Pedersen", "Eric Lyons", "Damon Lisch", "Shabarinath Subramaniam", "Michael Freeling"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000409.g002", "stats"=>{"downloads"=>3, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cartoons_illustrating_random_fractionation_and_biased_fractionation_/512916", "title"=>"Cartoons illustrating random fractionation and biased fractionation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-29 00:48:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/842724"], "description"=>"<p>(A) A cartoon of a blastn output between orthologous genes in rice, sorghum, and two maize homeologs. The colored rectangles (blue, orange, purple) represent high-scoring sequence pairs (HSPs), or regions with high sequence similarity to each other. Sorghum is the reference sequence (Sb09). The top two panels show the syntenous exon sequence (highlighted in blue) between rice (rice chromosome 5, or Os05) and sorghum (sorghum chromosome 9, or Sb09); the second and fourth panels demonstrate the location of the deletion in maize homeolog <i>Zm</i> chromosome 8 (Zm08) to its sorghum ortholog (purple). As can be seen, the deletion is evident when the Zm08 sequence (circled) is compared to the orthologous sequence of Zm06 (orange) and rice (blue) when all HSPs are aligned on sorghum. The GEvo alignment output for these data may be found at <a href=\"http://genomevolution.org/r/3em\" target=\"_blank\">http://genomevolution.org/r/3em</a>. (B) A ClustalW alignment of the rice, sorghum, and maize homeologs from <a href=\"http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1000409#pbio-1000409-g005\" target=\"_blank\">Figure 5A</a>. The purple sequence in the unfractionated maize homeolog (Zm06) indicates the location of the direct repeat sequence that originally flanked the deletion in the fractionated homeolog (Zm08). (C) A diagram representing the mechanism of intra-chromosomal recombination, based on the flanking sequence highlighted in (B). Direct repeats come together to form a circle, which is then recombined away, leaving a solo repeat in its place.</p>", "links"=>[], "tags"=>["intra-chromosomal", "recombination", "fractionated", "maize"], "article_id"=>513175, "categories"=>["Genetics"], "users"=>["Margaret R. Woodhouse", "James C. Schnable", "Brent S. Pedersen", "Eric Lyons", "Damon Lisch", "Shabarinath Subramaniam", "Michael Freeling"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000409.g005", "stats"=>{"downloads"=>4, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Deletions_and_intra_chromosomal_recombination_in_fractionated_maize_homeologs_/513175", "title"=>"Deletions and intra-chromosomal recombination in fractionated maize homeologs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-29 00:52:55"}
  • {"files"=>["https://ndownloader.figshare.com/files/419707", "https://ndownloader.figshare.com/files/419724", "https://ndownloader.figshare.com/files/419771", "https://ndownloader.figshare.com/files/419834", "https://ndownloader.figshare.com/files/419913", "https://ndownloader.figshare.com/files/419973", "https://ndownloader.figshare.com/files/420126"], "description"=>"<div><p>Previous work in Arabidopsis showed that after an ancient tetraploidy event, genes were preferentially removed from one of the two homeologs, a process known as fractionation. The mechanism of fractionation is unknown. We sought to determine whether such preferential, or biased, fractionation exists in maize and, if so, whether a specific mechanism could be implicated in this process. We studied the process of fractionation using two recently sequenced grass species: sorghum and maize. The maize lineage has experienced a tetraploidy since its divergence from sorghum approximately 12 million years ago, and fragments of many knocked-out genes retain enough sequence similarity to be easily identifiable. Using sorghum exons as the query sequence, we studied the fate of both orthologous genes in maize following the maize tetraploidy. We show that genes are predominantly lost, not relocated, and that single-gene loss by deletion is the rule. Based on comparisons with orthologous sorghum and rice genes, we also infer that the sequences present before the deletion events were flanked by short direct repeats, a signature of intra-chromosomal recombination. Evidence of this deletion mechanism is found 2.3 times more frequently on one of the maize homeologs, consistent with earlier observations of biased fractionation. The over-fractionated homeolog is also a greater than 3-fold better target for transposon removal, but does not have an observably higher synonymous base substitution rate, nor could we find differentially placed methylation domains. We conclude that fractionation is indeed biased in maize and that intra-chromosomal or possibly a similar illegitimate recombination is the primary mechanism by which fractionation occurs. The mechanism of intra-chromosomal recombination explains the observed bias in both gene and transposon loss in the maize lineage. The existence of fractionation bias demonstrates that the frequency of deletion is modulated. Among the evolutionary benefits of this deletion/fractionation mechanism is bulk DNA removal and the generation of novel combinations of regulatory sequences and coding regions.</p></div>", "links"=>[], "tags"=>["tetraploidy", "deletion", "removed", "genes", "preferentially", "homeologs"], "article_id"=>142872, "categories"=>["Genetics"], "users"=>["Margaret R. Woodhouse", "James C. Schnable", "Brent S. Pedersen", "Eric Lyons", "Damon Lisch", "Shabarinath Subramaniam", "Michael Freeling"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1000409.s001", "https://dx.doi.org/10.1371/journal.pbio.1000409.s002", "https://dx.doi.org/10.1371/journal.pbio.1000409.s003", "https://dx.doi.org/10.1371/journal.pbio.1000409.s004", "https://dx.doi.org/10.1371/journal.pbio.1000409.s005", "https://dx.doi.org/10.1371/journal.pbio.1000409.s006", "https://dx.doi.org/10.1371/journal.pbio.1000409.s007"], "stats"=>{"downloads"=>28, "page_views"=>20, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Following_Tetraploidy_in_Maize_a_Short_Deletion_Mechanism_Removed_Genes_Preferentially_from_One_of_the_Two_Homeologs/142872", "title"=>"Following Tetraploidy in Maize, a Short Deletion Mechanism Removed Genes Preferentially from One of the Two Homeologs", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-06-29 00:47:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/842631"], "description"=>"<p><i>x</i>-axis: length of the run, in genes. <i>y</i>-axis: number of runs. Black bars represent observed data. The white circles within the gray bars represent the median number of runs of that length observed from 1,000 simulations. The gray bars mark the limits within which the values of 95% from the simulations fell. Panels A–D refer to runs of deletions. Panels E and F refer to runs of genes retained from the maize lineage tetraploidy. (A) Observed and distributions of deletion runs in the over-fractionated homeologous regions including all deletion data, and simulated distributions assuming genes are lost solely through a 1 gene deletion mechanism. (B) Observed distributions of deletion runs in the over-fractionated homeologous regions with deletions longer than nine genes removed as likely segmental transpositions, and simulated distributions assuming genes are lost solely through a 1 gene deletion mechanism. (C) Observed and simulated distributions of deletions in the under-fractionated homeologous regions, assuming genes are lost solely through a 1 gene deletion mechanism. (D) Observed and simulated distributions of deletion runs in the over-fractionated homeologous regions, using a model where 80% of deletions are single gene, 15% remove two adjacent genes, and 5% of deletions remove three genes in a row, best fit ratio determined by a genetic algorithm. (E) Observed runs of genes retained in both homeologs and simulated distributions assuming genes are lost solely through a 1 gene deletion mechanism. (F) Observed runs of genes retained in both homeologs compared to the simulated expectation assuming 80% single-gene deletions, 15% two-gene, and 5% three-gene.</p>", "links"=>[], "tags"=>["runs", "genes"], "article_id"=>513085, "categories"=>["Genetics"], "users"=>["Margaret R. Woodhouse", "James C. Schnable", "Brent S. Pedersen", "Eric Lyons", "Damon Lisch", "Shabarinath Subramaniam", "Michael Freeling"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000409.g004", "stats"=>{"downloads"=>1, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Distribution_of_runs_Runs_of_lost_genes_or_runs_of_genes_retained_/513085", "title"=>"Distribution of runs: Runs of lost genes, or runs of genes retained.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-06-29 00:51:25"}

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