Consequences of Lineage-Specific Gene Loss on Functional Evolution of Surviving Paralogs: ALDH1A and Retinoic Acid Signaling in Vertebrate Genomes
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{"title"=>"Consequences of lineage-specific gene loss on functional evolution of surviving paralogs: ALDH1A and retinoic acid signaling in vertebrate genomes", "type"=>"journal", "authors"=>[{"first_name"=>"Cristian", "last_name"=>"Cañestro", "scopus_author_id"=>"6602494249"}, {"first_name"=>"Julian M.", "last_name"=>"Catchen", "scopus_author_id"=>"8879140800"}, {"first_name"=>"Adriana", "last_name"=>"Rodríguez-Marí", "scopus_author_id"=>"6506267837"}, {"first_name"=>"Hayato", "last_name"=>"Yokoi", "scopus_author_id"=>"7201964024"}, {"first_name"=>"John H.", "last_name"=>"Postlethwait", "scopus_author_id"=>"7005868055"}], "year"=>2009, "source"=>"PLoS Genetics", "identifiers"=>{"scopus"=>"2-s2.0-67149129951", "pui"=>"354733123", "pmid"=>"19478994", "issn"=>"15537390", "isbn"=>"1553-7404", "doi"=>"10.1371/journal.pgen.1000496", "sgr"=>"67149129951"}, "id"=>"8e3dff01-b8e5-35b1-a17b-120c6eaa293a", "abstract"=>"Genome duplications increase genetic diversity and may facilitate the evolution of gene subfunctions. Little attention, however, has focused on the evolutionary impact of lineage-specific gene loss. Here, we show that identifying lineage-specific gene loss after genome duplication is important for understanding the evolution of gene subfunctions in surviving paralogs and for improving functional connectivity among human and model organism genomes. We examine the general principles of gene loss following duplication, coupled with expression analysis of the retinaldehyde dehydrogenase Aldh1a gene family during retinoic acid signaling in eye development as a case study. Humans have three ALDH1A genes, but teleosts have just one or two. We used comparative genomics and conserved syntenies to identify loss of ohnologs (paralogs derived from genome duplication) and to clarify uncertain phylogenies. Analysis showed that Aldh1a1 and Aldh1a2 form a clade that is sister to Aldh1a3-related genes. Genome comparisons showed secondarily loss of aldh1a1 in teleosts, revealing that Aldh1a1 is not a tetrapod innovation and that aldh1a3 was recently lost in medaka, making it the first known vertebrate with a single aldh1a gene. Interestingly, results revealed asymmetric distribution of surviving ohnologs between co-orthologous teleost chromosome segments, suggesting that local genome architecture can influence ohnolog survival. We propose a model that reconstructs the chromosomal history of the Aldh1a family in the ancestral vertebrate genome, coupled with the evolution of gene functions in surviving Aldh1a ohnologs after R1, R2, and R3 genome duplications. Results provide evidence for early subfunctionalization and late subfunction-partitioning and suggest a mechanistic model based on altered regulation leading to heterochronic gene expression to explain the acquisition or modification of subfunctions by surviving ohnologs that preserve unaltered ancestral developmental programs in the face of gene loss.", "link"=>"http://www.mendeley.com/research/consequences-lineagespecific-gene-loss-functional-evolution-surviving-paralogs-aldh1a-retinoic-acid", "reader_count"=>86, "reader_count_by_academic_status"=>{"Unspecified"=>4, "Professor > Associate Professor"=>14, "Researcher"=>21, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>20, "Student > Master"=>6, "Other"=>5, "Student > Bachelor"=>2, "Lecturer"=>3, "Lecturer > Senior Lecturer"=>1, "Professor"=>6}, "reader_count_by_user_role"=>{"Unspecified"=>4, "Professor > Associate Professor"=>14, "Researcher"=>21, "Student > Doctoral Student"=>4, "Student > Ph. D. Student"=>20, "Student > Master"=>6, "Other"=>5, "Student > Bachelor"=>2, "Lecturer"=>3, "Lecturer > Senior Lecturer"=>1, "Professor"=>6}, "reader_count_by_subject_area"=>{"Unspecified"=>9, "Biochemistry, Genetics and Molecular Biology"=>6, "Nursing and Health Professions"=>1, "Agricultural and Biological Sciences"=>64, "Medicine and Dentistry"=>3, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Chemical Engineering"=>1, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>64}, "Nursing and Health Professions"=>{"Nursing and Health Professions"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>6}, "Unspecified"=>{"Unspecified"=>9}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "Chemical Engineering"=>{"Chemical Engineering"=>1}}, "reader_count_by_country"=>{"Canada"=>1, "Sweden"=>3, "United States"=>5, "Japan"=>1, "United Kingdom"=>1, "Portugal"=>1, "Germany"=>1}, "group_count"=>5}

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  • {"files"=>["https://ndownloader.figshare.com/files/896100"], "description"=>"<p>All phylogenetic methodologies (Bayesian, Maximum-likelihood, Neighbor-joining and Maximum-parsimony; included in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496.s001\" target=\"_blank\">Figure S1</a>) agreed on a unique gene topology in which Aldh1a1 (green background) and Aldh1a2 (tan background) are the closest sister clades, while Aldh1a3 (blue background) diverged basally: ((Aldh1a1, Aldh1a2), Aldh1a3). Values at nodes correspond to the posterior probabilities inferred from the Bayesian method and generally show a highly supported tree topology. The only exception is a moderately high value of 0.76 for the Aldh1a1-Aldh1a2 node (for this node, the ML, NJ and MP supporting values are also shown). While Aldh1a2 and Aldh1a3 are present in both tetrapods (red lines) and teleosts (blue lines), Aldh1a1 is absent from teleost genomes. Scale bar indicates amino-acid substitutions. Tetrapods: Hs, <i>Homo sapiens</i>; Mm, <i>Mus musculus</i>; Rn, <i>Rattus novergicus</i>; Gg, <i>Gallus gallus</i>; Xt, <i>Xenopus tropicalis</i>; Teleosts: Dr, <i>Danio rerio</i>; Ga, <i>Gasterosteus aculeatus</i>; Ol, <i>Oryzias latipes</i>; Tn, <i>Tetraodon nigroviridis</i>; Tr, <i>Takifugu rubripes</i>; Cephalochordates: Bf, <i>Branchiostoma floridae</i>.</p>", "links"=>[], "tags"=>["vertebrate", "aldh1a"], "article_id"=>566557, "categories"=>["Developmental Biology", "Genetics", "Evolutionary Biology", "Infectious Diseases"], "users"=>["Cristian Cañestro", "Julian M. Catchen", "Adriana Rodríguez-Marí", "Hayato Yokoi", "John H. Postlethwait"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000496.g001", "stats"=>{"downloads"=>1, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_tree_of_the_vertebrate_Aldh1A_gene_family_/566557", "title"=>"Phylogenetic tree of the vertebrate Aldh1A gene family.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-29 01:49:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/896415"], "description"=>"<p>(A–C) Dotplots display the distribution of zebrafish (A), stickleback (B) and medaka (C) orthologs (red dots for Aldh1a paralogs and black crosses for neighbor genes on teleost chromosomes in y-axis) of human <i>ALDH1A</i> genes, and their neighbor genes (red dots and black dots on x-axis, respectively) within a 10 Mb-window. The dotplot reveals that all genomic neighborhoods (GN) related to the <i>Aldh1a</i> family were duplicated during R3 in teleosts, but no additional <i>Aldh1a</i>-ohnologs from R3 (e.g. <i>Aldh1a2′</i>) currently survive. Gene loci that are close to each other may appear overlapped as single crosses in the plot due to the selected graph resolution. <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496.s005\" target=\"_blank\">Table S3</a> provides gene accession numbers and genomic information for all genes and each orthology group shown in the dotplot. (D) Bar-graph representing the asymmetric distribution of conserved co-orthologs in different chromosomes resulting from the analysis of twelve genomic neighborhoods related to the <i>ALDH1A</i> family (a1: <i>ALDH1A1</i>; a2: <i>Aldh1a2</i>; a3: <i>Aldh1a3</i>; a3-ogm: <i>Aldh1a3-ogm</i>). Values represent the percentage of conserved <i>ALDH1A</i> gene neighbor co-orthologs in each chromosome. (E–G) Co-orthologous gene clusters of zebrafish (E), stickleback (F), and medaka (G) related to the human <i>ALDH1A2</i> genomic neighborhood exemplify the asymmetric distribution of conserved co-orthologs after R3. Fish co-orthologs conserved between both fish clusters and the human cluster are colored gold, fish co-orthologs preserved only in the primary chromosome are in green, and fish co-orthologs preserved only in the secondary chromosome are in blue. <i>ALDH1A2</i> orthologs are highlighted in red, and co-orthologs present in both fish chromosomes, but absent in the human <i>ALDH1A2</i> genomic neighborhood are in purple.</p>", "links"=>[], "tags"=>["genomic", "neighborhoods", "asymmetric", "surviving"], "article_id"=>566869, "categories"=>["Developmental Biology", "Genetics", "Evolutionary Biology", "Infectious Diseases"], "users"=>["Cristian Cañestro", "Julian M. Catchen", "Adriana Rodríguez-Marí", "Hayato Yokoi", "John H. Postlethwait"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000496.g004", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Syntenic_conservation_between_human_and_fish_ALDH1A_genomic_neighborhoods_and_asymmetric_distribution_of_surviving_fish_co_orthologs_/566869", "title"=>"Syntenic conservation between human and fish <i>ALDH1A</i> genomic neighborhoods and asymmetric distribution of surviving fish co-orthologs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-29 01:54:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/896841"], "description"=>"<p>(A) Evolutionary model reconstructing the evolution of <i>Aldh1a</i> gene subfunctions in the developing retina. Mechanisms of early subfunctionalization, late subfunction partitioning, and acquisition or modification of ancestral subfunctions associated to events of gene duplication or gene loss (dotted lines) are indicated in the horizontal plane of a three-dimensional tree, in which events of vertebrate diversification are indicated in the vertical plane. A schematic retina at the stage of complete cup invagination represents dorso ventral (DV) expression domains of Aldh1a genes in different colors is indicated for present species and inferred for ancestral conditions. Bars indicate co-expression in the same dorso-ventral domains (or expression of ancestral genes), and dots refer to weak or remaining expression from earlier developmental stages. <i>Aldh1a1</i>: red, <i>Aldh1a2</i>: blue and <i>Aldh1a3</i>: green. <i>Aldh1a</i> expression data have been obtained from <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Drager1\" target=\"_blank\">[58]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Pittlik1\" target=\"_blank\">[65]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Grun1\" target=\"_blank\">[69]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Lupo1\" target=\"_blank\">[77]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Li1\" target=\"_blank\">[79]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Elinson1\" target=\"_blank\">[80]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Liang1\" target=\"_blank\">[84]</a>–<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Grandel1\" target=\"_blank\">[87]</a>, <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Niederreither2\" target=\"_blank\">[111]</a>–<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Swindell1\" target=\"_blank\">[120]</a> and this work <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen-1000496-g006\" target=\"_blank\">Figure 6B</a>). (B) Evolutionary mechanistic model to explain how the ancestral developmental program can remain unaltered after gene loss. This general model, extrapolated from our findings on the evolution of the expression of <i>Aldh1a</i> paralogs during eye development, is based on how heterochronic expression could facilitate the loss of a paralog, while leading to an apparent shuffling of functions between a lost paralog and a surviving paralog without the gain of new regulatory elements, but the loss of negative regulators.</p>", "links"=>[], "tags"=>["lineage-specific", "surviving"], "article_id"=>567299, "categories"=>["Developmental Biology", "Genetics", "Evolutionary Biology", "Infectious Diseases"], "users"=>["Cristian Cañestro", "Julian M. Catchen", "Adriana Rodríguez-Marí", "Hayato Yokoi", "John H. Postlethwait"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000496.g008", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Consequences_of_lineage_specific_gene_loss_on_functional_evolution_of_surviving_paralogs_/567299", "title"=>"Consequences of lineage-specific gene loss on functional evolution of surviving paralogs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-29 02:01:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/896234"], "description"=>"<p>(A) Composite dotplot representing the distribution of paralogs of genes (black dots) within a 10 Mb-window surrounding each member of the <i>ALDH1A</i> family throughout the human genome (red crosses: <i>ALDH1A</i>-neighbor paralogs; dark blue crosses: <i>ALDH1A2</i>-neighbor paralogs, and light-green crosses: <i>ALDH1A3</i>-neighbor paralogs. The genomes of <i>Ciona intestinalis</i> and <i>Branchiostoma floridae</i>, which represent urochordates and cephalochordates, respectively, the two closest vertebrate relatives <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Bourlat1\" target=\"_blank\">[66]</a>,<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Delsuc2\" target=\"_blank\">[110]</a>, were used as outgroups to define paralogy groups in the human genome. Gene accession numbers and genomic information for each group of paralogy represented in the dotplot is provided in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496.s003\" target=\"_blank\">Table S1</a>. Human chromosomes are represented in the y-axis, and drawn to scale in the x-axis with the p-terminus of each chromosome at the left and the q-terminus at the right of each white row. Chromosomal regions that appear enriched in <i>Aldh1a</i>-neighbor paralogs are indicated with colored boxes, highlighted in pink if <i>ALDH1A</i> genes are present, and in yellow if no <i>ALDH1A</i> genes are present. The distribution of paralogs of genes located in the yellow boxes is also represented in the dotplot (golden crosses: Hsa1 <i>ALDH1A</i>-related GN; black crosses: Hsa5 <i>ALDH1A</i>-related GN; pink crosses: Hsa9 <i>ALDH1A</i>-related GN; brown crosses: Hsa15 <i>ALDH1A</i>-related GN). (B) Two clusters of genes in Hsa15 and Hsa9 display a substantial number of conserved syntenies between the <i>ALDH1A1</i> and <i>ALDH1A2</i> gene neighborhoods (red lines), but fewer conserved syntenies with the <i>ALDH1A3</i> GN (green lines), supporting the idea that <i>ALDH1A1</i> and <i>ALDH1A2</i> are the closest sister paralogs, consistent with the phylogenetic tree ((ALDH1A1, ALDH1A2), ALDH1A3) in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen-1000496-g001\" target=\"_blank\">Figure 1</a>. Golden lines show conserved synteny between Hsa15 and parts of Hsa9 probably due to a local transposition that moved material between <i>ALDH1A2</i> and <i>ALDH1A3</i> from its original location to the right of <i>ALDH1A1</i> to the left of <i>ALDH1A1</i> (or vice versa). Colored boxes correspond to regions shown in A. <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496.s002\" target=\"_blank\">Figure S2</a> provides high-resolution images including the name of conserved syntenic genes. (C) Representation of a pair of paralogous gene clusters in Hsa15 and Hsa5 displaying high amounts of conserved synteny between the <i>ALDH1A3</i> and <i>ALDH1A3</i>-ogm GNs (green lines). (D–F) Circleplots display the patterns of conserved synteny between the <i>ALDH1A</i> GN (labeled with black arcs outside of each chromosome) revealed by the dotplot in A for Hsa1, Hsa5, Hsa9, Hsa15 and Hsa19 (see main text for explanations). While the patterns of conserved synteny between <i>ALDH1A1</i> and <i>ALDH1A2</i> GNs (red lines) and between <i>ALDH1A3</i> and <i>ALDH1A3</i>-ogm GNs (green lines) are restricted to defined dense bundles (D), lines originating from Hsa1 (E) and Hsa19 (F) are not restricted to any particular <i>ALDH1A</i> GN (the different colors of the lines in E and F label various chromosomes). Circles represent chromosome centromeres, and dotted arcs label the approximate <i>ALDH1A</i> GN positions in the chromosomes.</p>", "links"=>[], "tags"=>["syntenic", "genomic", "neighborhoods"], "article_id"=>566690, "categories"=>["Developmental Biology", "Genetics", "Evolutionary Biology", "Infectious Diseases"], "users"=>["Cristian Cañestro", "Julian M. Catchen", "Adriana Rodríguez-Marí", "Hayato Yokoi", "John H. Postlethwait"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000496.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Paralogous_syntenic_conservation_among_ALDH1A_genomic_neighborhoods_GN_in_the_human_genome_/566690", "title"=>"Paralogous syntenic conservation among <i>ALDH1A</i> genomic neighborhoods (GN) in the human genome.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-29 01:51:30"}
  • {"files"=>["https://ndownloader.figshare.com/files/896521"], "description"=>"<p>This analysis provides evidence that the genomic duplication that generated <i>Aldh1a1</i> and <i>Aldh1a2</i> from an ancestral <i>Aldh1a1/2</i> gene predated the tetrapod-teleost divergence. <i>Aldh1a</i> gene family members are highlighted in red, and the nearest <i>Aldh1a1</i> conserved syntenic genes are labeled in purple. Teleost-specific <i>tmc</i> tandem duplicates located in the position predicted for the lost <i>aldh1a1</i> are brown. This analysis suggests that the loss of the <i>aldh1a1</i> ortholog probably occurred before the teleost radiation, which rules out the hypothesis that <i>Aldh1a1</i> is a tetrapod innovation. Additional paralogous clusters with low conserved synteny with the Hsa ALDH1A1 genomic neighborhood were found in secondary chromosomal regions in teleost genomes (e.g. Dre8, GacXIV, and Ola12; included in <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496.s005\" target=\"_blank\">Table S3</a> and <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496.s002\" target=\"_blank\">Figure S2</a>).</p>", "links"=>[], "tags"=>["syntenies", "was"], "article_id"=>566973, "categories"=>["Developmental Biology", "Genetics", "Evolutionary Biology", "Infectious Diseases"], "users"=>["Cristian Cañestro", "Julian M. Catchen", "Adriana Rodríguez-Marí", "Hayato Yokoi", "John H. Postlethwait"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000496.g005", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Conserved_syntenies_provide_evidence_that_aldh1a1_was_lost_in_stem_teleosts_/566973", "title"=>"Conserved syntenies provide evidence that <i>aldh1a1</i> was lost in stem teleosts.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-29 01:56:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/896728"], "description"=>"<p>Circles and numbers near chromosomes label Aldh1a paralogs, and their genomic neighborhoods are color-coded (<i>Aldh1a1</i>: red; <i>Aldh1a2</i>: blue; <i>Aldh1a3</i>: light green; and <i>Aldh1a3</i>-ogm: dark green). Duplication, preservation, losses and translocation of <i>Aldh1</i> gene paralogs are inferred in ancestral vertebrate chromosomes (e.g. A0–A5 <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Nakatani1\" target=\"_blank\">[26]</a>). Step numbers in circles label chromosome rearrangements. Vertical gray bars signify rounds of whole genome duplication events (R1, R2 and R3). Transparent images signify lost genes. In addition to the ancestral status inferred directly from comparative genomic analysis of conserved syntenies (white background; see main text for details), the figure shows two hypotheses (pink and tan boxes) to explain the mechanisms by which the <i>Aldh1a1/2/3/3-ogm</i> gene precursor located in the pre-R1 chromosome “A” generated the genome neighborhoods of <i>Aldh1a2</i> and <i>Aldh1a3</i> in chromosome “A4”, and <i>Aldh1a1</i> and <i>Aldh1a3-ogm</i> in “A0” inferred after R2 (step 1). Under hypothesis 1 (“pre-R1 duplication scenario” in the pink box), a segment from Nakatani et al.'s ancestral chromosome “A” including the original <i>Aldh1a1/2/3/3-ogm</i> gene was tandemly duplicated prior to R1 and gave rise to the <i>Aldh1a1/2</i> and <i>Aldh1a3/3-ogm</i> genes. Considering the most parsimonious situation, after R1, one of the two homeologs preserved both <i>Aldh1a1/2</i> and <i>Aldh1a3/3-ogm</i>, and the other homeolog lost both duplicated copies. After R2, the chromosome preserving the <i>Aldh1a</i> genes gave rise to “A4” and “A0”, from which today's <i>Aldh1a</i> gene family members have evolved. After R2, the chromosome that did not preserve an <i>Aldh1a</i> gene gave rise to “A2–A5” and “A1–A3”, explaining conserved syntenies related to the <i>Aldh1a</i> family observed in today's Hsa1 and Hsa19 (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen-1000496-g002\" target=\"_blank\">Figure 2</a>). An alternative hypothesis to explain the ancestral synteny of <i>Aldh1a</i> genomic neighborhoods inferred in A4 and A0 (hypothesis 2, the “translocation scenario” in the tan box) proposes a translocation event, which may have occurred either before R2 (top half of tan box) or after R2 (bottom half of tan box). In these scenarios, and in contrast to hypothesis 1, a single original gene <i>Aldh1a1/2/3/3-ogm</i> was present in the ancestral chromosome “A”, and after R1, <i>aldh1a1/2</i> and <i>aldh1a3/3-ogm</i> genes originated in duplicated chromosomes. One possibility (top half in tan box) is that, before R2, a small chromosomal translocation placed <i>Aldh1a1/2</i> and <i>Aldh1a3/3-ogm</i> on the same chromosome (dotted arrow in tan box). After R2, the chromosome “recipient” of the translocation gave rise to “A4” and “A0”, which contained all Aldh1a ancestral genes from today's Aldh1a family members, while the chromosome “donor” gave rise to “A2–A5” and “A1–A3”, which lacked any <i>Aldh1a</i> gene but still preserved syntenies for Aldh1a gene neighborhoods. The possibility that the translocation carrying <i>Aldh1a3</i> to the same chromosome as <i>Aldh1a2</i> could have occurred after R2 cannot be discarded (dotted arrow bottom half in tan box), and would be consistent with the absence of any <i>Aldh1a</i> paralog in Hsa5 (white box at the bottom on chromosome A0). In this case, however, we would not expect to find paralogs of genes that are tightly linked to <i>ALDH1A2</i> or <i>ALDH1A1</i> on Hsa5. We found, however, genes including <i>CCNB1</i>, <i>GCNT4</i>, <i>FAM81B</i> in Hsa5, whose paralogs <i>CNB2</i>, <i>GCNT3</i> and <i>FAM81A</i> are located near <i>ALDH1A2</i> in Hsa15, and <i>GCNT1</i>, a third <i>GCNT3</i> paralog, is close to <i>ALDH1A1</i> in Hsa9. Further gene translocations, however, could explain the presence of those genes in Hsa5, and therefore a hypothetical translocation after R2 cannot be discarded.</p>", "links"=>[], "tags"=>["reconstructs", "genomic", "neighborhoods", "ancestral", "vertebrate"], "article_id"=>567179, "categories"=>["Developmental Biology", "Genetics", "Evolutionary Biology", "Infectious Diseases"], "users"=>["Cristian Cañestro", "Julian M. Catchen", "Adriana Rodríguez-Marí", "Hayato Yokoi", "John H. Postlethwait"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000496.g007", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolutionary_model_reconstructs_the_history_of_the_Aldh1a_genomic_neighborhoods_from_ancestral_vertebrate_chromosomes_/567179", "title"=>"Evolutionary model reconstructs the history of the <i>Aldh1a</i> genomic neighborhoods from ancestral vertebrate chromosomes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-29 01:59:39"}
  • {"files"=>["https://ndownloader.figshare.com/files/896610"], "description"=>"<p>(A) Comparative syntenic analysis of <i>ALDH1A3</i> genomic neighborhoods in human, stickleback, and medaka. These results show that <i>aldh1a3</i> was lost in the medaka lineage. <i>ALDH1A3</i> orthologs are highlighted in red, and <i>ALDH1A3</i> nearest neighbors are labeled in purple. The presence of one LTR-flanked retrotransposon including an ORF2 reverse transcriptase (in brown) in the putative locus of the lost <i>aldh1a3</i> gene suggests the hypothesis that the insertion of the retrotransposon was related to the <i>aldh1a3</i> loss. (B) Comparative analysis by in situ hybridization of the expression of <i>aldh1a</i> gene family members in the developing eye of zebrafish and medaka reveals that the medaka <i>aldh1a2</i> gene recapitulates both the dorsal expression of <i>aldh1a2</i> and the ventral expression of <i>aldh1a3</i> in zebrafish. This result suggests that in medaka, <i>aldh1a2</i> provides a ventral RA source after the loss of <i>aldh1a3</i>.</p>", "links"=>[], "tags"=>["syntenies", "was", "secondarily"], "article_id"=>567068, "categories"=>["Developmental Biology", "Genetics", "Evolutionary Biology", "Infectious Diseases"], "users"=>["Cristian Cañestro", "Julian M. Catchen", "Adriana Rodríguez-Marí", "Hayato Yokoi", "John H. Postlethwait"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000496.g006", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Conserved_syntenies_provide_evidence_that_aldh1a3_was_secondarily_lost_in_medaka_/567068", "title"=>"Conserved syntenies provide evidence that <i>aldh1a3</i> was secondarily lost in medaka.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-29 01:57:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/444623", "https://ndownloader.figshare.com/files/444685", "https://ndownloader.figshare.com/files/444748", "https://ndownloader.figshare.com/files/444808", "https://ndownloader.figshare.com/files/444848"], "description"=>"<div><p>Genome duplications increase genetic diversity and may facilitate the evolution of gene subfunctions. Little attention, however, has focused on the evolutionary impact of lineage-specific gene loss. Here, we show that identifying lineage-specific gene loss after genome duplication is important for understanding the evolution of gene subfunctions in surviving paralogs and for improving functional connectivity among human and model organism genomes. We examine the general principles of gene loss following duplication, coupled with expression analysis of the retinaldehyde dehydrogenase <em>Aldh1a</em> gene family during retinoic acid signaling in eye development as a case study. Humans have three <em>ALDH1A</em> genes, but teleosts have just one or two. We used comparative genomics and conserved syntenies to identify loss of ohnologs (paralogs derived from genome duplication) and to clarify uncertain phylogenies. Analysis showed that <em>Aldh1a1</em> and <em>Aldh1a2</em> form a clade that is sister to <em>Aldh1a3</em>-related genes. Genome comparisons showed secondarily loss of <em>aldh1a1</em> in teleosts, revealing that <em>Aldh1a1</em> is not a tetrapod innovation and that <em>aldh1a3</em> was recently lost in medaka, making it the first known vertebrate with a single <em>aldh1a</em> gene. Interestingly, results revealed asymmetric distribution of surviving ohnologs between co-orthologous teleost chromosome segments, suggesting that local genome architecture can influence ohnolog survival. We propose a model that reconstructs the chromosomal history of the <em>Aldh1a</em> family in the ancestral vertebrate genome, coupled with the evolution of gene functions in surviving <em>Aldh1a</em> ohnologs after R1, R2, and R3 genome duplications. Results provide evidence for early subfunctionalization and late subfunction-partitioning and suggest a mechanistic model based on altered regulation leading to heterochronic gene expression to explain the acquisition or modification of subfunctions by surviving ohnologs that preserve unaltered ancestral developmental programs in the face of gene loss.</p></div>", "links"=>[], "tags"=>["consequences", "lineage-specific", "surviving", "aldh1a", "retinoic", "signaling", "vertebrate", "genomes"], "article_id"=>147621, "categories"=>["Developmental Biology", "Genetics", "Evolutionary Biology", "Cancer"], "users"=>["Cristian Cañestro", "Julian M. Catchen", "Adriana Rodríguez-Marí", "Hayato Yokoi", "John H. Postlethwait"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1000496.s001", "https://dx.doi.org/10.1371/journal.pgen.1000496.s002", "https://dx.doi.org/10.1371/journal.pgen.1000496.s003", "https://dx.doi.org/10.1371/journal.pgen.1000496.s004", "https://dx.doi.org/10.1371/journal.pgen.1000496.s005"], "stats"=>{"downloads"=>5, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Consequences_of_Lineage_Specific_Gene_Loss_on_Functional_Evolution_of_Surviving_Paralogs_ALDH1A_and_Retinoic_Acid_Signaling_in_Vertebrate_Genomes/147621", "title"=>"Consequences of Lineage-Specific Gene Loss on Functional Evolution of Surviving Paralogs: ALDH1A and Retinoic Acid Signaling in Vertebrate Genomes", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2009-05-29 02:07:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/896325"], "description"=>"<p>(A) Dotplot displays of the genomic distribution of the mouse orthologs (crosses) of the human <i>ALDH1A</i>-neighbor genes within a 10 Mb-window of the human <i>ALDH1A</i> gene (red: <i>ALDH1A1</i>-neighbor genes; blue: <i>ALDH1A2</i>-neighbor genes; green: <i>ALDH13</i>-neighbor genes; and yellow: <i>ALDH1A3-ogm</i>-neighbor genes), and reveals the presence of four regions (colored boxes) in Mmu7, Mmu9, Mmu13 and Mmu19 orthologous to the human <i>ALDH1A</i> genomic neighborhoods (GN). Mouse chromosomes are represented in the y-axis, and chromosome position is in the x-axis. <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496.s004\" target=\"_blank\">Table S2</a> provides gene accession numbers and genomic information for each orthology group represented in the dotplot. (B) A circle-plot shows the pattern of syntenic correspondence between the human <i>ALDH1A</i> GNs (black arcs outside chromosomes) and the candidate mouse orthologous <i>ALDH1A</i>-related chromosomes revealed in A. <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496.s002\" target=\"_blank\">Figure S2</a> provide high resolution images of pair-wise gene clusters identified in the orthologous syntenic database <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1000496#pgen.1000496-Catchen1\" target=\"_blank\">[48]</a> showing orthologous regions of high syntenic conservation between the human and mouse <i>Aldh1a</i> GNs shown in A and B. The correspondence of <i>ALDH1A3</i> GNs in Hsa 15 and Mmu7 (green lines), and <i>ALDH1A3</i>-ogm GNs in Hsa5 and Mmu13 (golden) strongly supports the conclusion that <i>ALDH1A3</i> in human is an ortholog, not a paralog, of <i>Aldh1a3</i> in mouse. These results show that the loss of <i>ALDH1A3</i>-ogm predated the divergence of mouse and human. Circles represent chromosome centromeres.</p>", "links"=>[], "tags"=>["syntenic", "genomic"], "article_id"=>566783, "categories"=>["Developmental Biology", "Genetics", "Evolutionary Biology", "Infectious Diseases"], "users"=>["Cristian Cañestro", "Julian M. Catchen", "Adriana Rodríguez-Marí", "Hayato Yokoi", "John H. Postlethwait"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1000496.g003", "stats"=>{"downloads"=>3, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Orthologous_syntenic_conservation_between_human_and_mouse_ALDH1A_genomic_neighborhoods_/566783", "title"=>"Orthologous syntenic conservation between human and mouse <i>ALDH1A</i> genomic neighborhoods.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2009-05-29 01:53:03"}

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