Sepsid even-skipped Enhancers Are Functionally Conserved in Drosophila Despite Lack of Sequence Conservation
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{"title"=>"Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation", "type"=>"journal", "authors"=>[{"first_name"=>"Emily E.", "last_name"=>"Hare", "scopus_author_id"=>"8325639500"}, {"first_name"=>"Brant K.", "last_name"=>"Peterson", "scopus_author_id"=>"24448667400"}, {"first_name"=>"Venky N.", "last_name"=>"Iyer", "scopus_author_id"=>"9746295800"}, {"first_name"=>"Rudolf", "last_name"=>"Meier", "scopus_author_id"=>"35269600400"}, {"first_name"=>"Michael B.", "last_name"=>"Eisen", "scopus_author_id"=>"7004331829"}], "year"=>2008, "source"=>"PLoS Genetics", "identifiers"=>{"scopus"=>"2-s2.0-46249134068", "sgr"=>"46249134068", "issn"=>"15537390", "doi"=>"10.1371/journal.pgen.1000106", "pmid"=>"18584029", "isbn"=>"1553-7404 (Electronic)", "pui"=>"351914797"}, "id"=>"053290a6-42f1-3db2-86c4-a99119f39464", "abstract"=>"The gene expression pattern specified by an animal regulatory sequence is generally viewed as arising from the particular arrangement of transcription factor binding sites it contains. However, we demonstrate here that regulatory sequences whose binding sites have been almost completely rearranged can still produce identical outputs. We sequenced the even-skipped locus from six species of scavenger flies (Sepsidae) that are highly diverged from the model species Drosophila melanogaster, but share its basic patterns of developmental gene expression. Although there is little sequence similarity between the sepsid eve enhancers and their well-characterized D. melanogaster counterparts, the sepsid and Drosophila enhancers drive nearly identical expression patterns in transgenic D. melanogaster embryos. We conclude that the molecular machinery that connects regulatory sequences to the transcription apparatus is more flexible than previously appreciated. In exploring this diverse collection of sequences to identify the shared features that account for their similar functions, we found a small number of short (20-30 bp) sequences nearly perfectly conserved among the species. These highly conserved sequences are strongly enriched for pairs of overlapping or adjacent binding sites. Together, these observations suggest that the local arrangement of binding sites relative to each other is more important than their overall arrangement into larger units of cis-regulatory function.", "link"=>"http://www.mendeley.com/research/sepsid-evenskipped-enhancers-functionally-conserved-drosophila-despite-lack-sequence-conservation", "reader_count"=>206, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>20, "Researcher"=>58, "Student > Doctoral Student"=>6, "Student > Ph. D. Student"=>66, "Student > Postgraduate"=>6, "Student > Master"=>19, "Other"=>6, "Student > Bachelor"=>19, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>20, "Researcher"=>58, "Student > Doctoral Student"=>6, "Student > Ph. D. Student"=>66, "Student > Postgraduate"=>6, "Student > Master"=>19, "Other"=>6, "Student > Bachelor"=>19, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>25, "Agricultural and Biological Sciences"=>161, "Medicine and Dentistry"=>4, "Neuroscience"=>2, "Business, Management and Accounting"=>1, "Physics and Astronomy"=>3, "Chemistry"=>1, "Social Sciences"=>1, "Computer Science"=>4, "Earth and Planetary Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Neuroscience"=>{"Neuroscience"=>2}, "Chemistry"=>{"Chemistry"=>1}, "Social Sciences"=>{"Social Sciences"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>3}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>161}, "Computer Science"=>{"Computer Science"=>4}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>25}, "Unspecified"=>{"Unspecified"=>3}}, "reader_count_by_country"=>{"Canada"=>1, "Netherlands"=>1, "United States"=>12, "Denmark"=>1, "United Kingdom"=>6, "France"=>2, "Germany"=>3, "Spain"=>3, "Indonesia"=>1}, "group_count"=>7}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/927705"], "description"=>"<p>Genome and <i>eve</i> locus size in sepsids.</p>", "links"=>[], "tags"=>["locus"], "article_id"=>598157, "categories"=>["Medicine", "Developmental Biology", "Evolutionary Biology", "Genetics", "Computational Biology"], "users"=>["Emily E. Hare", "Brant K. Peterson", "Venky N. Iyer", "Rudolf Meier", "Michael B. Eisen"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000106.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genome_and_eve_locus_size_in_sepsids_/598157", "title"=>"Genome and <i>eve</i> locus size in sepsids.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-06-27 02:15:57"}
  • {"files"=>["https://ndownloader.figshare.com/files/927328"], "description"=>"<p>Expression patterns were visualized by <i>in situ</i> hybridization with species-specific digoxigenin-labeled antisense RNA probes. The gap transcription factors <i>hb</i>, <i>gt</i> and <i>Kr</i> are expressed in similar domains during stage 5 in <i>D. melanogaster</i> (A–C) and <i>T. minor</i> (E–G). <i>eve</i> is expressed in seven transverse stripes during cellularization in both species (D, H). Embryos are oriented with anterior to the left and dorsal up.</p>", "links"=>[], "tags"=>["upstream", "transcriptional", "regulators", "conserved", "sepsid"], "article_id"=>597772, "categories"=>["Medicine", "Developmental Biology", "Evolutionary Biology", "Genetics", "Computational Biology"], "users"=>["Emily E. Hare", "Brant K. Peterson", "Venky N. Iyer", "Rudolf Meier", "Michael B. Eisen"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000106.g004", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_eve_and_its_upstream_transcriptional_regulators_is_conserved_between_Drosophila_melanogaster_and_the_sepsid_Themira_minor_/597772", "title"=>"Expression of <i>eve</i> and its upstream transcriptional regulators is conserved between <i>Drosophila melanogaster</i> and the sepsid <i>Themira minor</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-06-27 02:09:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/927257"], "description"=>"<p>(A) Maximum likelihood tree of protein-coding genes inferred from seven genes using CODEML module of PAML <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000106#pgen.1000106-Yang1\" target=\"_blank\">[59]</a>. Branch lengths are in substitutions per codon using the [F3×4] model. (B) Maximum likelihood non-coding trees of six <i>Drosophila</i> and six sepsids computed using the BASEML module of PAML <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000106#pgen.1000106-Yang1\" target=\"_blank\">[59]</a>. Branch lengths are in substitutions per site using the HKY model.</p>", "links"=>[], "tags"=>["non-coding", "trees", "sepsids"], "article_id"=>597705, "categories"=>["Medicine", "Developmental Biology", "Evolutionary Biology", "Genetics", "Computational Biology"], "users"=>["Emily E. Hare", "Brant K. Peterson", "Venky N. Iyer", "Rudolf Meier", "Michael B. Eisen"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000106.g003", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Coding_and_non_coding_trees_of_sepsids_and_Drosophila_/597705", "title"=>"Coding and non-coding trees of sepsids and <i>Drosophila.</i>", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-06-27 02:08:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/927740"], "description"=>"<p>Positions of borders and width of <i>eve</i> stripes driven by <i>Drosophila</i> and sepsid enhancers.</p>", "links"=>[], "tags"=>["borders", "width", "stripes", "driven", "sepsid"], "article_id"=>598183, "categories"=>["Medicine", "Developmental Biology", "Evolutionary Biology", "Genetics", "Computational Biology"], "users"=>["Emily E. Hare", "Brant K. Peterson", "Venky N. Iyer", "Rudolf Meier", "Michael B. Eisen"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000106.t002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Positions_of_borders_and_width_of_eve_stripes_driven_by_Drosophila_and_sepsid_enhancers_/598183", "title"=>"Positions of borders and width of <i>eve</i> stripes driven by <i>Drosophila</i> and sepsid enhancers.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2008-06-27 02:16:23"}
  • {"files"=>["https://ndownloader.figshare.com/files/927642"], "description"=>"<p>Binding sites in the stripe 2, stripe 3+7, and MHE enhancers were classified as “overlapping” if they shared at least one base pair with a site for a different factor, “close” if the nearest base of another site (for a different factor) is within 10 bp, and “isolated” if neither condition is met. Binding sites in <i>D. melanogaster</i> were classified as non-conserved, minimally conserved (only within <i>melanogaster</i> subgroup), highly conserved (within 12 sequenced <i>Drosophila</i> species) and extremely conserved (12 <i>Drosophila</i> and 6 sepsids). (A) The distribution of conservation scores as a function of binding-site proximity shows overlapping and close sites are more likely to be highly or extremely conserved than isolated sites. (B) The fraction of each conservation category in different proximity groups again shows that extremely and highly conserved sites are strongly enriched for overlapping and close binding sites.</p>", "links"=>[], "tags"=>["binding", "sites", "proximity"], "article_id"=>598088, "categories"=>["Medicine", "Developmental Biology", "Evolutionary Biology", "Genetics", "Computational Biology"], "users"=>["Emily E. Hare", "Brant K. Peterson", "Venky N. Iyer", "Rudolf Meier", "Michael B. Eisen"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000106.g007", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolutionary_fate_of_binding_sites_is_dependent_on_their_proximity_to_other_sites_/598088", "title"=>"Evolutionary fate of binding sites is dependent on their proximity to other sites.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-06-27 02:14:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/927076"], "description"=>"<p>Predicted binding sites for the five factors known to regulate expression from the <i>eve</i> stripe 2 enhancer in the twelve sequenced <i>Drosophila</i> species <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000106#pgen.1000106-Clark1\" target=\"_blank\">[56]</a>. Sites were predicted independently in each species using PATSER <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000106#pgen.1000106-Hertz1\" target=\"_blank\">[61]</a> and mapped onto an MLAGAN <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000106#pgen.1000106-Brudno1\" target=\"_blank\">[65]</a> multiple alignment of the <i>eve</i> stripe 2 enhancer sequences. The height of the box representing each binding site is scaled by its PATSER p-value (taller boxes represent sites with higher predicted affinities). The top panel (grey shading) shows the positions of biochemically-verified (in vitro footprinting) binding sites <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000106#pgen.1000106-Bergman1\" target=\"_blank\">[27]</a>. The indicated coordinates are for the multiple-alignment, which is longer than individual enhancers due to the high frequency of alignment gaps.</p>", "links"=>[], "tags"=>["turnover", "stripe"], "article_id"=>597525, "categories"=>["Medicine", "Developmental Biology", "Evolutionary Biology", "Genetics", "Computational Biology"], "users"=>["Emily E. Hare", "Brant K. Peterson", "Venky N. Iyer", "Rudolf Meier", "Michael B. Eisen"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000106.g001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Binding_site_conservation_and_turnover_in_Drosophila_even_skipped_stripe_2_enhancer_/597525", "title"=>"Binding site conservation and turnover in <i>Drosophila even-skipped</i> stripe 2 enhancer.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-06-27 02:05:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/457671", "https://ndownloader.figshare.com/files/457681", "https://ndownloader.figshare.com/files/457700", "https://ndownloader.figshare.com/files/457730", "https://ndownloader.figshare.com/files/457751", "https://ndownloader.figshare.com/files/457763", "https://ndownloader.figshare.com/files/457778", "https://ndownloader.figshare.com/files/457785", "https://ndownloader.figshare.com/files/457801", "https://ndownloader.figshare.com/files/457814"], "description"=>"<div><p>The gene expression pattern specified by an animal regulatory sequence is generally viewed as arising from the particular arrangement of transcription factor binding sites it contains. However, we demonstrate here that regulatory sequences whose binding sites have been almost completely rearranged can still produce identical outputs. We sequenced the <em>even</em>-<em>skipped</em> locus from six species of scavenger flies (Sepsidae) that are highly diverged from the model species <em>Drosophila melanogaster</em>, but share its basic patterns of developmental gene expression. Although there is little sequence similarity between the sepsid <em>eve</em> enhancers and their well-characterized <em>D. melanogaster</em> counterparts, the sepsid and <em>Drosophila</em> enhancers drive nearly identical expression patterns in transgenic <em>D. melanogaster</em> embryos. We conclude that the molecular machinery that connects regulatory sequences to the transcription apparatus is more flexible than previously appreciated. In exploring this diverse collection of sequences to identify the shared features that account for their similar functions, we found a small number of short (20–30 bp) sequences nearly perfectly conserved among the species. These highly conserved sequences are strongly enriched for pairs of overlapping or adjacent binding sites. Together, these observations suggest that the local arrangement of binding sites relative to each other is more important than their overall arrangement into larger units of <em>cis</em>-regulatory function.</p></div>", "links"=>[], "tags"=>["sepsid", "enhancers", "are", "functionally", "conserved"], "article_id"=>150160, "categories"=>["Medicine", "Developmental Biology", "Evolutionary Biology", "Genetics", "Biological Sciences"], "users"=>["Emily E. Hare", "Brant K. Peterson", "Venky N. Iyer", "Rudolf Meier", "Michael B. Eisen"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000106.s001", "https://dx.doi.org/10.1371/journal.pgen.1000106.s002", "https://dx.doi.org/10.1371/journal.pgen.1000106.s003", "https://dx.doi.org/10.1371/journal.pgen.1000106.s004", "https://dx.doi.org/10.1371/journal.pgen.1000106.s005", "https://dx.doi.org/10.1371/journal.pgen.1000106.s006", "https://dx.doi.org/10.1371/journal.pgen.1000106.s007", "https://dx.doi.org/10.1371/journal.pgen.1000106.s008", "https://dx.doi.org/10.1371/journal.pgen.1000106.s009", "https://dx.doi.org/10.1371/journal.pgen.1000106.s010"], "stats"=>{"downloads"=>19, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Sepsid_even_skipped_Enhancers_Are_Functionally_Conserved_in_Drosophila_Despite_Lack_of_Sequence_Conservation/150160", "title"=>"Sepsid <em>even-skipped</em> Enhancers Are Functionally Conserved in <em>Drosophila</em> Despite Lack of Sequence Conservation", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2008-06-27 00:02:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/927549"], "description"=>"<p>Predicted binding sites for the five factors known to regulate expression from the <i>eve</i> stripe 2 enhancer in six <i>Drosophila</i> species <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000106#pgen.1000106-Clark1\" target=\"_blank\">[56]</a> and six sepsid species. Sites were predicted independently in each species using PATSER <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000106#pgen.1000106-Hertz1\" target=\"_blank\">[61]</a> and mapped onto an MLAGAN <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000106#pgen.1000106-Brudno1\" target=\"_blank\">[65]</a> multiple alignment of the <i>eve</i> stripe 2 enhancer sequences. The height of the box representing each binding site is scaled by its PATSER p-value (taller boxes represent sites with higher predicted affinities). The top panel (grey shading) shows the positions of biochemically-verified (<i>in vitro</i> footprinting) binding sites <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000106#pgen.1000106-Bergman1\" target=\"_blank\">[27]</a>. Binding sites conserved within families are indicated by solid boxes. A BCD-KR site pair conserved across families is indicated by a dashed box. Alignment coordinates are indicated.</p>", "links"=>[], "tags"=>["reorganization", "binding", "sites", "sepsid", "stripe"], "article_id"=>597995, "categories"=>["Medicine", "Developmental Biology", "Evolutionary Biology", "Genetics", "Computational Biology"], "users"=>["Emily E. Hare", "Brant K. Peterson", "Venky N. Iyer", "Rudolf Meier", "Michael B. Eisen"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000106.g006", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Extensive_reorganization_of_binding_sites_between_Drosophila_and_sepsid_eve_stripe_2_enhancers_/597995", "title"=>"Extensive reorganization of binding sites between <i>Drosophila</i> and sepsid <i>eve</i> stripe 2 enhancers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-06-27 02:13:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/927184"], "description"=>"<p>The <i>eve</i> locus (20 kb flanking the <i>eve</i> protein-coding gene) is shown for two <i>Drosophila</i> (<i>D. melanogaster</i> and <i>D. virilis</i>) and two sepsid species (<i>S. cynipsea</i> and <i>T. putris</i>), centered on the <i>eve</i> homeodomain. Black lines represent significant BLASTZ <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000106#pgen.1000106-Schwartz1\" target=\"_blank\">[15]</a> hits on the plus strand, red lines on the minus strand (BLASTZ parameters: K = 1800, with chaining). Verified <i>D. melanogaster</i> enhancers are shown in green and predicted sepsid enhancers in black. Note that only a subset of <i>D. melanogaster eve</i> enhancers are shown here; all BLASTZ matches between <i>D. melanogaster</i> and <i>S. cynipsea</i> fall within known enhancers with the exception of those falling within 500 bp of the transcription start site in <i>D. melanogaster</i>.</p>", "links"=>[], "tags"=>["sepsids"], "article_id"=>597637, "categories"=>["Medicine", "Developmental Biology", "Evolutionary Biology", "Genetics", "Computational Biology"], "users"=>["Emily E. Hare", "Brant K. Peterson", "Venky N. Iyer", "Rudolf Meier", "Michael B. Eisen"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000106.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Conservation_within_and_between_sepsids_and_Drosophila_/597637", "title"=>"Conservation within and between sepsids and <i>Drosophila</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-06-27 02:07:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/927439"], "description"=>"<p>Expression patterns of <i>eve</i> stripe 2, stripe 3+7, stripe 4+6 and muscle-heart enhancers from sepsids <i>S. cynipsea</i>, <i>T. putris</i> and <i>T. superba</i> were compared to their <i>D. melanogaster</i> counterparts in transgenic <i>D. melanogaster</i> embryos by RNA <i>in situ</i> hybridization with digoxigenin-labeled antisense RNA probes against the reporter genes lacZ (A, D, G) and CFP (B,C,E,F,H,I,K,L), or staining with βGal antibodies (J). (A–C) Sepsid stripe 2 enhancers drive strong expression in an anterior stripe corresponding to <i>D. melanogaster</i> stripe 2. (D–F) Sepsid stripe 3+7 enhancers drive expression within the limits of <i>D. melanogaster</i> stripe 3 and 7, with additional expression in the posterior. (G–I) Sepsid stripe 4+6 enhancers drive expression within the limits of <i>D. melanogaster</i> stripes 4 and 6. (J–L) Sepsid MHE enhancers are expressed in metameric clusters in the dorsal mesoderm in stage, as in <i>D. melanogaster</i>. Embryos were imaged during cellularization and are oriented with anterior to the left and dorsal up.</p>", "links"=>[], "tags"=>["enhancers", "conserved", "patterns"], "article_id"=>597887, "categories"=>["Medicine", "Developmental Biology", "Evolutionary Biology", "Genetics", "Computational Biology"], "users"=>["Emily E. Hare", "Brant K. Peterson", "Venky N. Iyer", "Rudolf Meier", "Michael B. Eisen"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000106.g005", "stats"=>{"downloads"=>0, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sepsid_eve_enhancers_drive_conserved_expression_patterns_in_Drosophila_melanogaster_embryos_/597887", "title"=>"Sepsid <i>eve</i> enhancers drive conserved expression patterns in <i>Drosophila melanogaster</i> embryos.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2008-06-27 02:11:27"}

PMC Usage Stats | Further Information

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Relative Metric

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