Determinative Developmental Cell Lineages Are Robust to Cell Deaths
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{"title"=>"Determinative Developmental Cell Lineages Are Robust to Cell Deaths", "type"=>"journal", "authors"=>[{"first_name"=>"Jian Rong", "last_name"=>"Yang", "scopus_author_id"=>"25822774600"}, {"first_name"=>"Shuxiang", "last_name"=>"Ruan", "scopus_author_id"=>"55313910400"}, {"first_name"=>"Jianzhi", "last_name"=>"Zhang", "scopus_author_id"=>"56752433600"}], "year"=>2014, "source"=>"PLoS Genetics", "identifiers"=>{"sgr"=>"84905483300", "pui"=>"373701252", "doi"=>"10.1371/journal.pgen.1004501", "pmid"=>"25058586", "scopus"=>"2-s2.0-84905483300", "issn"=>"15537404", "isbn"=>"10.1371/journal.pgen.1004501"}, "id"=>"b536ab6e-0a4e-3bc7-bfc9-baac38256e63", "abstract"=>"All forms of life are confronted with environmental and genetic perturbations, making phenotypic robustness an important characteristic of life. Although development has long been viewed as a key component of phenotypic robustness, the underlying mechanism is unclear. Here we report that the determinative developmental cell lineages of two protostomes and one deuterostome are structured such that the resulting cellular compositions of the organisms are only modestly affected by cell deaths. Several features of the cell lineages, including their shallowness, topology, early ontogenic appearances of rare cells, and non-clonality of most cell types, underlie the robustness. Simple simulations of cell lineage evolution demonstrate the possibility that the observed robustness arose as an adaptation in the face of random cell deaths in development. These results reveal general organizing principles of determinative developmental cell lineages and a conceptually new mechanism of phenotypic robustness, both of which have important implications for development and evolution.", "link"=>"http://www.mendeley.com/research/determinative-developmental-cell-lineages-robust-cell-deaths", "reader_count"=>20, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>2, "Researcher"=>6, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>1, "Student > Master"=>1, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>2, "Researcher"=>6, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>7, "Student > Postgraduate"=>1, "Student > Master"=>1, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Biochemistry, Genetics and Molecular Biology"=>3, "Mathematics"=>1, "Agricultural and Biological Sciences"=>14, "Medicine and Dentistry"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>14}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Mathematics"=>{"Mathematics"=>1}}, "reader_count_by_country"=>{"Korea (South)"=>1, "United States"=>3, "Denmark"=>1, "France"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1607650"], "description"=>"<p>(A–B) Complex relationships between lineage complexity and robustness to (A) necrosis or (B) program failure among three types of random lineages. Each dot represents a random lineage, whereas the triangle shows the real lineage of <i>C. elegans</i>. <i>P</i><sub>1</sub> is the probability that the complexity is equal between the dots of two colors compared (Mann-Whitney <i>U</i> test), whereas <i>P</i><sub>2</sub> is the probability that the robustness (<i>f</i><sub>n</sub> or <i>f</i><sub>p</sub>) is equal between the dots of two colors compared (Mann-Whitney <i>U</i> test). All <i>P</i> values are calculated based on 10,000 dots of each color. For clarity, however, only 100 dots of each color are shown here. (C–D) Lineage complexity and robustness to (C) necrosis or (D) program failure of lineages generated in the macroevolution. Each evolutionary simulation is conducted 100 times, shown by 100 dots of the same color. The quantity being selected for is defined in the symbol legend, where <i>S</i> and <i>R</i> represent simplicity (i.e., 1/complexity) and robustness against necrosis (<i>f</i><sub>n</sub>), respectively. The fitness functions used in various simulations (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004501#s4\" target=\"_blank\">Materials and Methods</a>) are shown in the dash-lined box. The actual <i>C. elegans</i> lineage is indicated by a triangle.</p>", "links"=>[], "tags"=>["Computational biology", "Evolutionary modeling", "developmental biology", "Evolutionary developmental biology", "Evolutionary biology", "Theoretical biology", "simplicity", "cannot", "robustness"], "article_id"=>1116606, "categories"=>["Biological Sciences"], "users"=>["Jian-Rong Yang", "Shuxiang Ruan", "Jianzhi Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004501.g007", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Selection_for_simplicity_cannot_explain_the_robustness_of_the_C_elegans_cell_lineage_/1116606", "title"=>"Selection for simplicity cannot explain the robustness of the <i>C. elegans</i> cell lineage.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-24 02:59:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/1607647"], "description"=>"<p>(A–E) Frequency distributions of (A) lineage robustness in the presence of necrosis (<i>f</i><sub>n</sub>), (B) maximum depth, (C) mean depth, (D) rare-early correlation, and (E) lineage robustness in the presence of program failure (<i>f</i><sub>p</sub>) among lineages generated from the macroevolution with different intensities of selection for high <i>f</i><sub>n</sub>. The observed values from the <i>C. elegans</i> lineage are indicated by black arrows. Each distribution in each panel is based on 100 simulation replications. The number next to the color scheme shows the fraction of most robust lineages from which the progenitor of next evolutionary expansion of cell lineage is randomly chosen. That is, the lower the number, the stronger the selection. (F–J) Frequency distributions of (F) lineage robustness in the presence of program failure (<i>f</i><sub>p</sub>), (G) maximum depth, (H) mean depth, (I) rare-early correlation, and (J) lineage robustness in the presence of necrosis (<i>f</i><sub>n</sub>) among lineages generated from the macroevolution with different intensities of selection for high <i>f</i><sub>p</sub>. The observed values from the <i>C. elegans</i> lineage are indicated by black arrows.</p>", "links"=>[], "tags"=>["Computational biology", "Evolutionary modeling", "developmental biology", "Evolutionary developmental biology", "Evolutionary biology", "Theoretical biology", "macroevolution", "simulation", "suggests", "robustness", "lineage", "arose", "adaptation", "necrosis"], "article_id"=>1116603, "categories"=>["Biological Sciences"], "users"=>["Jian-Rong Yang", "Shuxiang Ruan", "Jianzhi Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004501.g006", "stats"=>{"downloads"=>1, "page_views"=>16, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_macroevolution_simulation_suggests_the_possibility_that_the_robustness_of_the_C_elegans_lineage_arose_as_an_adaptation_to_necrosis_but_not_program_failure_/1116603", "title"=>"The macroevolution simulation suggests the possibility that the robustness of the <i>C. elegans</i> lineage arose as an adaptation to necrosis but not program failure.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-24 02:59:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/1607632"], "description"=>"<p>(A) Positive correlation between the depth of a terminal cell and its cell type size. Spearman's rank correlation (ρ) for the original unbinned data and the associated <i>P</i>-value are presented. Error bars show one standard deviation of the depth within a cell type. Bla, blast; Epi, epithelial; Ger, germ; Gla, gland; Int, intestinal; Mus, muscle; Str, neural structural; Neu, neuron. The rare-early correlation remains strong even when the germ cells are removed (ρ = 0.515, <i>P</i><10<sup>−38</sup>). (B) Frequency distribution of the rare-early correlation coefficient from 10,000 random lineages that have the same topology as that of <i>C. elegans</i> but have their terminal cells randomly relabeled. The arrow indicates the correlation coefficient for the <i>C. elegans</i> lineage. <i>P</i>-value is the probability that a random lineage above generated has a higher rare-early correlation than that observed in <i>C. elegans</i>. <i>Z</i>-score is the number of standard deviations by which the observed correlation deviates from the expected correlation of the random lineages with the same topology. (C–D) The stronger the rare-early correlation (ρ<sub>rare-early</sub>) in a random lineage, the higher the robustness of the lineage in the presence of (C) necrosis or (D) program failure. Although 10,000 random lineages are generated, for clarity, only 1000 are shown (grey dots). The dashed line is the linear least-square regression of these 1000 dots. The rank correlation between ρ<sub>rare-early</sub> and robustness, as well as the associated <i>P</i>-value, are calculated from all 10,000 lineages. The <i>C. elegans</i> lineage is represented by a triangle.</p>", "links"=>[], "tags"=>["Computational biology", "Evolutionary modeling", "developmental biology", "Evolutionary developmental biology", "Evolutionary biology", "Theoretical biology", "cells", "depths", "improves", "robustness"], "article_id"=>1116588, "categories"=>["Biological Sciences"], "users"=>["Jian-Rong Yang", "Shuxiang Ruan", "Jianzhi Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004501.g004", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_tendency_for_rare_cells_to_have_low_depths_improves_the_robustness_of_the_C_elegans_lineage_/1116588", "title"=>"The tendency for rare cells to have low depths improves the robustness of the <i>C. elegans</i> lineage.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-24 02:59:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/1607627"], "description"=>"<p>(A–B) Frequency distribution of the robustness of 10,000 random lineages (grey bars) in the presence of (A) necrosis or (B) program failure. These random lineages have exactly the same depths as in <i>C. elegans</i> for all terminal cells but have randomized topologies. The arrow indicates the robustness of the <i>C. elegans</i> lineage. <i>P</i>-value is the probability that a random lineage above created is more robust than the <i>C. elegans</i> lineage. <i>Z</i>-score is the number of standard deviations by which the observation deviates from the mean of the random lineages. (C–D) Frequency distribution of the robustness of 10,000 random lineages (grey bars) in the presence of (A) necrosis or (B) program failure. These random lineages have exactly the same topology as the <i>C. elegans</i> lineage but have their terminal cells randomly relabeled. The arrow indicates the robustness of the <i>C. elegans</i> lineage. <i>P</i>-value is the probability that a random lineage above created is more robust than the <i>C. elegans</i> lineage. <i>Z</i>-score is the number of standard deviations by which the observation deviates from the mean of the random lineages.</p>", "links"=>[], "tags"=>["Computational biology", "Evolutionary modeling", "developmental biology", "Evolutionary developmental biology", "Evolutionary biology", "Theoretical biology", "topology", "terminal", "robustness"], "article_id"=>1116583, "categories"=>["Biological Sciences"], "users"=>["Jian-Rong Yang", "Shuxiang Ruan", "Jianzhi Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004501.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Lineal_topology_and_terminal_cell_organization_contribute_to_the_robustness_of_the_C_elegans_lineage_/1116583", "title"=>"Lineal topology and terminal cell organization contribute to the robustness of the <i>C. elegans</i> lineage.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-24 02:59:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/1607626"], "description"=>"<p>(A) Frequency distribution of the maximum cell depth in 10,000 lineages (grey bars), which are generated by random coalescence of the terminal cells of the <i>C. elegans</i> lineage. The arrow indicates the observed maximum cell depth in the <i>C. elegans</i> lineage. <i>P</i>-value is the probability that the maximum depth of a random lineage is smaller than that of <i>C. elegans</i>. <i>Z</i>-score is the number of standard deviations by which the observation deviates from the mean of the random lineages. (B–C) Violin plot for the robustness of randomly generated lineages with defined maximum depths in the presence of (B) necrosis or (C) program failure. Each violin is essentially a horizontal histogram showing the relative probability densities of different robustness of random lineages with the indicated maximum depth. The horizontal line in each violin plot shows the mean value. The real lineage is shown by a triangle. <i>P</i>-value is the probability that the robustness of a random lineage (with the same maximum depth as that of <i>C. elegans</i>) is higher than that of <i>C. elegans</i>. <i>Z</i>-score is the number of standard deviations by which the observation deviates from the mean of the random lineages. (D) Frequency distribution of the mean terminal cell depth in 5,000 lineages (grey bars), which are generated by random coalescence of the terminal cells of the <i>C. elegans</i> lineage with the requirement that the maximum depth is the same as in <i>C. elegans</i>. The arrow indicates the observed mean depth in the <i>C. elegans</i> lineage. <i>P</i>-value is the probability that the mean depth is smaller in a random lineage than in <i>C. elegans</i> when their maximum depths are the same. (E–F) Violin plot for the robustness of randomly generated lineages with the maximum depth equal to that of <i>C. elegans</i> and defined mean depths, in the presence of (E) necrosis or (F) program failure. The real lineage is indicated by a triangle. <i>P</i>-value is the probability that the robustness is higher in a random lineage (with the same maximum depth and similar mean depth as those of <i>C. elegans</i>) than in <i>C. elegans</i>. <i>Z</i>-score is the number of standard deviations by which the observation deviates from the mean of the random lineages.</p>", "links"=>[], "tags"=>["Computational biology", "Evolutionary modeling", "developmental biology", "Evolutionary developmental biology", "Evolutionary biology", "Theoretical biology", "depths", "terminal", "cells", "robustness", "lineage", "necrosis"], "article_id"=>1116582, "categories"=>["Biological Sciences"], "users"=>["Jian-Rong Yang", "Shuxiang Ruan", "Jianzhi Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004501.g002", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Low_depths_of_terminal_cells_improve_the_robustness_of_the_C_elegans_lineage_to_necrosis_and_program_failure_/1116582", "title"=>"Low depths of terminal cells improve the robustness of the <i>C. elegans</i> lineage to necrosis and program failure.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-24 02:59:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/1607623"], "description"=>"<p>(A) A hypothetical cell lineage. Internal cells are prefixed with “I” and terminal cells are prefixed with “T”. Terminal cells belonging to the same cell type have the same name. Internal cells are colored according to their cell division programs. (B) The same cell lineage showing division programs for internal cells. Internal cells having the same division programs share the same color and program name (prefixed by “P”). (C) An example showing robustness calculation upon a necrotic cell depth. The internal cell I3 dies, which causes the loss of I3 as well as all of its direct and indirect descendant cells. Robustness is calculated by the product of the fraction of live terminal cells of each cell type. (D) An example showing robustness calculation upon a program failure. The failure of program P3 results in the loss of all descendant cells of internal cells that use P3. Robustness is calculated by the product of the fraction of live terminal cells of each cell type. (E–F) The <i>Caenorhabditis elegans</i> developmental cell lineage is more robust than the corresponding random lineages in the presence of (E) necrosis or (F) program failure. The grey bars show the frequency distribution of the robustness of 10,000 random lineages, whereas the arrow indicates the robustness of the <i>C. elegans</i> cell lineage. The random lineages are generated by randomly coalescing the terminal cells of the <i>C. elegans</i> lineage. <i>P</i>-value indicates the probability that a randomly generated lineage is more robust than the real lineage. <i>Z</i>-score is the number of standard deviations (of the random lineages) by which the observation deviates from the mean of the random lineages. (G–H) The <i>Pellioditis marina</i> cell lineage is more robust than the corresponding random lineages in the presence of (G) necrosis or (H) program failure. (I–J) The <i>Halocynthia roretzi</i> cell lineage is more robust than the corresponding random lineages in the presence of (I) necrosis or (J) program failure.</p>", "links"=>[], "tags"=>["Computational biology", "Evolutionary modeling", "developmental biology", "Evolutionary developmental biology", "Evolutionary biology", "Theoretical biology", "lineages", "robust", "necrosis"], "article_id"=>1116579, "categories"=>["Biological Sciences"], "users"=>["Jian-Rong Yang", "Shuxiang Ruan", "Jianzhi Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004501.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Animal_developmental_cell_lineages_are_robust_to_necrosis_and_program_failure_/1116579", "title"=>"Animal developmental cell lineages are robust to necrosis and program failure.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-24 02:59:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/1607636"], "description"=>"<p>(A–B) Lineage robustness in the presence of (A) necrosis or (B) program failure declines with the rise of clonality in 1050 random lineages with different levels of clonality. These lineages are generated by different degrees of clustering of terminal cells of the same types while constraining the lineal topology and depths of all terminal cells as in <i>C. elegans</i>. The different degrees of clustering are shown by different colors, with the scale shown at the top left corner of the figure. The dashed line is the linear least-square regression. The rank correlation between clonality and robustness, as well as the associated <i>P</i>-value, are presented. The <i>C. elegans</i> lineage is indicated by a triangle. (C) Spatial requirements cannot explain the low clonality of the real lineage. The 1050 random lineages with different levels of clonality are plotted, showing that the increase of clonality promotes the rank correlation (ρ<sub>p-l</sub>) between <i>p</i>hysical and <i>l</i>ineal distances of terminal cells of the same type. The triangle indicates the real lineage, while the square indicates an artificial lineage with the same topology, depths of all cells, and clonality as the real lineage, but a higher ρ<sub>p-l</sub>. The <i>C</i> values here are different from those appearing in panels A, B and F, because not all <i>C. elegans</i> terminal cells have three-dimensional coordinates. (D–E) Spatial constraint lowers lineage robustness in the presence of (D) necrosis or (E) program failure. Red dots are random lineages generated by random rearrangement of terminal cells within their respective depths, whereas blue dots are generated with the additional constraint that twin terminal cells, which share their immediate progenitor and their cell type, are maintained. <i>P</i><sub>1</sub> is the probability that the clonality is equal between the blue and red dots (Mann-Whitney <i>U</i> test), whereas <i>P</i><sub>2</sub> is the probability that the robustness is equal between the blue and red dots (Mann-Whitney <i>U</i> test). All <i>P</i> values are calculated based on 10,000 red and 10,000 blue dots. For clarity, only 100 red and 100 blue dots are shown here. (F) Lineage complexity decreases with the rise of clonality among the 1050 random lineages. The rank correlation between clonality and complexity, as well as the associated <i>P</i>-value, are presented. The <i>C. elegans</i> lineage is indicated by a triangle.</p>", "links"=>[], "tags"=>["Computational biology", "Evolutionary modeling", "developmental biology", "Evolutionary developmental biology", "Evolutionary biology", "Theoretical biology", "types", "contributes", "robustness"], "article_id"=>1116592, "categories"=>["Biological Sciences"], "users"=>["Jian-Rong Yang", "Shuxiang Ruan", "Jianzhi Zhang"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1004501.g005", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Non_clonality_of_cell_types_contributes_to_the_robustness_of_the_C_elegans_lineage_/1116592", "title"=>"Non-clonality of cell types contributes to the robustness of the <i>C. elegans</i> lineage.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-07-24 02:59:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/1607662", "https://ndownloader.figshare.com/files/1607663", "https://ndownloader.figshare.com/files/1607664", "https://ndownloader.figshare.com/files/1607665", "https://ndownloader.figshare.com/files/1607666", "https://ndownloader.figshare.com/files/1607667", "https://ndownloader.figshare.com/files/1607668", "https://ndownloader.figshare.com/files/1607669", "https://ndownloader.figshare.com/files/1607670", "https://ndownloader.figshare.com/files/1607671"], "description"=>"<div><p>All forms of life are confronted with environmental and genetic perturbations, making phenotypic robustness an important characteristic of life. Although development has long been viewed as a key component of phenotypic robustness, the underlying mechanism is unclear. Here we report that the determinative developmental cell lineages of two protostomes and one deuterostome are structured such that the resulting cellular compositions of the organisms are only modestly affected by cell deaths. Several features of the cell lineages, including their shallowness, topology, early ontogenic appearances of rare cells, and non-clonality of most cell types, underlie the robustness. Simple simulations of cell lineage evolution demonstrate the possibility that the observed robustness arose as an adaptation in the face of random cell deaths in development. These results reveal general organizing principles of determinative developmental cell lineages and a conceptually new mechanism of phenotypic robustness, both of which have important implications for development and evolution.</p></div>", "links"=>[], "tags"=>["Computational biology", "Evolutionary modeling", "developmental biology", "Evolutionary developmental biology", "Evolutionary biology", "Theoretical biology", "lineages", "robust"], "article_id"=>1116614, "categories"=>["Biological Sciences"], "users"=>["Jian-Rong Yang", "Shuxiang Ruan", "Jianzhi Zhang"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1004501.s001", "https://dx.doi.org/10.1371/journal.pgen.1004501.s002", "https://dx.doi.org/10.1371/journal.pgen.1004501.s003", "https://dx.doi.org/10.1371/journal.pgen.1004501.s004", "https://dx.doi.org/10.1371/journal.pgen.1004501.s005", "https://dx.doi.org/10.1371/journal.pgen.1004501.s006", "https://dx.doi.org/10.1371/journal.pgen.1004501.s007", "https://dx.doi.org/10.1371/journal.pgen.1004501.s008", "https://dx.doi.org/10.1371/journal.pgen.1004501.s009", "https://dx.doi.org/10.1371/journal.pgen.1004501.s010"], "stats"=>{"downloads"=>14, "page_views"=>15, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Determinative_Developmental_Cell_Lineages_Are_Robust_to_Cell_Deaths_/1116614", "title"=>"Determinative Developmental Cell Lineages Are Robust to Cell Deaths", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-07-24 02:59:46"}

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Relative Metric

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