The Maternal-to-Zygotic Transition Targets Actin to Promote Robustness during Morphogenesis
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{"title"=>"The Maternal-to-Zygotic Transition Targets Actin to Promote Robustness during Morphogenesis", "type"=>"journal", "authors"=>[{"first_name"=>"Liuliu", "last_name"=>"Zheng", "scopus_author_id"=>"55938513300"}, {"first_name"=>"Leonardo A.", "last_name"=>"Sepúlveda", "scopus_author_id"=>"35178485500"}, {"first_name"=>"Rhonald C.", "last_name"=>"Lua", "scopus_author_id"=>"6507847837"}, {"first_name"=>"Olivier", "last_name"=>"Lichtarge", "scopus_author_id"=>"7003903180"}, {"first_name"=>"Ido", "last_name"=>"Golding", "scopus_author_id"=>"6701314358"}, {"first_name"=>"Anna Marie", "last_name"=>"Sokac", "scopus_author_id"=>"6602418439"}], "year"=>2013, "source"=>"PLoS Genetics", "identifiers"=>{"issn"=>"15537390", "scopus"=>"2-s2.0-84888257752", "sgr"=>"84888257752", "pui"=>"370341810", "isbn"=>"1553-7404 (Electronic)\r1553-7390 (Linking)", "pmid"=>"24244181", "doi"=>"10.1371/journal.pgen.1003901"}, "id"=>"c7931ce9-ed70-399c-b4a3-8ecdbb63094f", "abstract"=>"Robustness is a property built into biological systems to ensure stereotypical outcomes despite fluctuating inputs from gene dosage, biochemical noise, and the environment. During development, robustness safeguards embryos against structural and functional defects. Yet, our understanding of how robustness is achieved in embryos is limited. While much attention has been paid to the role of gene and signaling networks in promoting robust cell fate determination, little has been done to rigorously assay how mechanical processes like morphogenesis are designed to buffer against variable conditions. Here we show that the cell shape changes that drive morphogenesis can be made robust by mechanisms targeting the actin cytoskeleton. We identified two novel members of the Vinculin/α-Catenin Superfamily that work together to promote robustness during Drosophila cellularization, the dramatic tissue-building event that generates the primary epithelium of the embryo. We find that zygotically-expressed Serendipity-α (Sry-α) and maternally-loaded Spitting Image (Spt) share a redundant, actin-regulating activity during cellularization. Spt alone is sufficient for cellularization at an optimal temperature, but both Spt plus Sry-α are required at high temperature and when actin assembly is compromised by genetic perturbation. Our results offer a clear example of how the maternal and zygotic genomes interact to promote the robustness of early developmental events. Specifically, the Spt and Sry-α collaboration is informative when it comes to genes that show both a maternal and zygotic requirement during a given morphogenetic process. For the cellularization of Drosophilids, Sry-α and its expression profile may represent a genetic adaptive trait with the sole purpose of making this extreme event more reliable. Since all morphogenesis depends on cytoskeletal remodeling, both in embryos and adults, we suggest that robustness-promoting mechanisms aimed at actin could be effective at all life stages.", "link"=>"http://www.mendeley.com/research/maternaltozygotic-transition-targets-actin-promote-robustness-during-morphogenesis", "reader_count"=>30, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>8, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>1, "Student > Master"=>1, "Student > Bachelor"=>3, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Researcher"=>8, "Student > Ph. D. Student"=>12, "Student > Postgraduate"=>1, "Student > Master"=>1, "Student > Bachelor"=>3, "Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>7, "Agricultural and Biological Sciences"=>18, "Medicine and Dentistry"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Physics and Astronomy"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>18}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>7}, "Unspecified"=>{"Unspecified"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Argentina"=>1, "United States"=>2, "France"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1271101"], "description"=>"<p>(A, C) Frequency of multinucleation for heterozygous embryos reared (A) at 32°C, or (C) with a reduced dose of maternal Profilin (<i>½profilin</i>; mean ± s.e.m.). (B, D) Quantification of multinucleation phenotype for heterozygous embryos reared (B) at 32°C, or (D) with a reduced dose of maternal Profilin (<i>½profilin</i>). Each point represents one embryo with ≥150 nuclei analyzed (n = 23 embryos per condition). Two-way ANOVA analysis was performed to calculate P values as shown in (A–D).</p>", "links"=>[], "tags"=>["copies", "cellularization", "embryo", "challenged"], "article_id"=>843680, "categories"=>["Biological Sciences"], "users"=>["Liuliu Zheng", "Leonardo A. Sepúlveda", "Rhonald C. Lua", "Olivier Lichtarge", "Ido Golding", "Anna Marie Sokac"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003901.g007", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Two_copies_of_sry_945_are_required_for_reliable_cellularization_at_the_extreme_temperature_of_32_C_or_when_the_embryo_is_challenged_by_a_genetic_perturbation_/843680", "title"=>"Two copies of <i>sry-α</i> are required for reliable cellularization at the extreme temperature of 32°C or when the embryo is challenged by a genetic perturbation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-07 02:45:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1271099"], "description"=>"<p>(A) Surface views of furrow canals stained for Myosin-2 in embryos of indicated genotypes. Multinucleate cells highlighted (orange nuclei) in corresponding segmented images. (B) Quantification of multinucleation phenotype for indicated genotype and temperature. Each point represents one embryo with ≥150 nuclei analyzed (n = 12 embryos per condition). Two-way ANOVA analysis was performed to calculate P values as shown.</p>", "links"=>[], "tags"=>["cellularization", "optimal"], "article_id"=>843678, "categories"=>["Biological Sciences"], "users"=>["Liuliu Zheng", "Leonardo A. Sepúlveda", "Rhonald C. Lua", "Olivier Lichtarge", "Ido Golding", "Anna Marie Sokac"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003901.g006", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sry_945_is_not_required_for_cellularization_at_an_optimal_temperature_of_18_176_C_but_is_required_as_conditions_approach_an_extreme_of_32_176_C_/843678", "title"=>"Sry-α is not required for cellularization at an optimal temperature of 18°C, but is required as conditions approach an extreme of 32°C.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-07 02:45:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1271109", "https://ndownloader.figshare.com/files/1271110", "https://ndownloader.figshare.com/files/1271111", "https://ndownloader.figshare.com/files/1271112", "https://ndownloader.figshare.com/files/1271113", "https://ndownloader.figshare.com/files/1271114", "https://ndownloader.figshare.com/files/1271115", "https://ndownloader.figshare.com/files/1271116", "https://ndownloader.figshare.com/files/1271117"], "description"=>"<div><p>Robustness is a property built into biological systems to ensure stereotypical outcomes despite fluctuating inputs from gene dosage, biochemical noise, and the environment. During development, robustness safeguards embryos against structural and functional defects. Yet, our understanding of how robustness is achieved in embryos is limited. While much attention has been paid to the role of gene and signaling networks in promoting robust cell fate determination, little has been done to rigorously assay how mechanical processes like morphogenesis are designed to buffer against variable conditions. Here we show that the cell shape changes that drive morphogenesis can be made robust by mechanisms targeting the actin cytoskeleton. We identified two novel members of the Vinculin/α-Catenin Superfamily that work together to promote robustness during <i>Drosophila</i> cellularization, the dramatic tissue-building event that generates the primary epithelium of the embryo. We find that zygotically-expressed Serendipity-α (Sry-α) and maternally-loaded Spitting Image (Spt) share a redundant, actin-regulating activity during cellularization. Spt alone is sufficient for cellularization at an optimal temperature, but both Spt plus Sry-α are required at high temperature and when actin assembly is compromised by genetic perturbation. Our results offer a clear example of how the maternal and zygotic genomes interact to promote the robustness of early developmental events. Specifically, the Spt and Sry-α collaboration is informative when it comes to genes that show both a maternal and zygotic requirement during a given morphogenetic process. For the cellularization of Drosophilids, Sry-α and its expression profile may represent a genetic adaptive trait with the sole purpose of making this extreme event more reliable. Since all morphogenesis depends on cytoskeletal remodeling, both in embryos and adults, we suggest that robustness-promoting mechanisms aimed at actin could be effective at all life stages.</p></div>", "links"=>[], "tags"=>["maternal-to-zygotic", "targets", "actin", "robustness"], "article_id"=>843687, "categories"=>["Biological Sciences"], "users"=>["Liuliu Zheng", "Leonardo A. Sepúlveda", "Rhonald C. Lua", "Olivier Lichtarge", "Ido Golding", "Anna Marie Sokac"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003901.s001", "https://dx.doi.org/10.1371/journal.pgen.1003901.s002", "https://dx.doi.org/10.1371/journal.pgen.1003901.s003", "https://dx.doi.org/10.1371/journal.pgen.1003901.s004", "https://dx.doi.org/10.1371/journal.pgen.1003901.s005", "https://dx.doi.org/10.1371/journal.pgen.1003901.s006", "https://dx.doi.org/10.1371/journal.pgen.1003901.s007", "https://dx.doi.org/10.1371/journal.pgen.1003901.s008", "https://dx.doi.org/10.1371/journal.pgen.1003901.s009"], "stats"=>{"downloads"=>15, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_Maternal_to_Zygotic_Transition_Targets_Actin_to_Promote_Robustness_during_Morphogenesis_/843687", "title"=>"The Maternal-to-Zygotic Transition Targets Actin to Promote Robustness during Morphogenesis", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-11-07 02:45:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1271087"], "description"=>"<p>(A) Domain structure of Vinculin/α-Catenin Superfamily members. Vinculin Homology domains 1, 2, and 3 (VH1, VH2, VH3) are orange, purple, and blue, respectively. The green and gray domains indicate sequences shared between α-Catenin, Sry-α, and Spt. White areas indicate unique sequences. Dashed lines are guides to show how the different proteins align with each other. (B) Cladogram of Vinculin/α-Catenin Superfamily. Bootstrap statistics at branch points (1000 iterations). Outgroup is <i>M. brevicollis</i> Vinculin. Shading highlights division of the clades. (C, D) Cross sections show (C) Sry-α and (D) Spt-HA co-localization with F-actin in furrow canals. Arrows indicate furrow canal position. (E) Western blots for an F-actin co-sedimentation assay show Sry-α full-length protein (GST-Sry-α) and Spt truncate (GST-SptΔ; amino acids 250–461) pellet with F-actin. α-Actinin and GST are positive and negative controls, respectively. S, supernatant; P, pellet. (F) Quantification of percent proteins bound to F-actin from three independent co-sedimentation assays (mean ± s.e.m.). Student's t-test was performed to calculate P values as shown.</p>", "links"=>[], "tags"=>["spt", "paralogs", "redundant", "f-actin", "binding"], "article_id"=>843668, "categories"=>["Biological Sciences"], "users"=>["Liuliu Zheng", "Leonardo A. Sepúlveda", "Rhonald C. Lua", "Olivier Lichtarge", "Ido Golding", "Anna Marie Sokac"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003901.g002", "stats"=>{"downloads"=>0, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sry_945_and_Spt_are_paralogs_with_redundant_F_actin_binding_activity_/843668", "title"=>"Sry-α and Spt are paralogs with redundant F-actin binding activity.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-07 02:45:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1271092"], "description"=>"<p>(A) RT-PCR and (B) Western blots show Sry-α and Spt expression profiles. Developmental stages are (1) mitotic cycles 1–9; (2) mitotic cycles 10–11; (3) mitotic cycles 11–13; (4) cellularization (shaded); (5) ventral furrow formation; (6) segment formation. Profiles were obtained from three independent RT-PCR or Western Blotting experiments (mean ± s.e.m.).</p>", "links"=>[], "tags"=>["maternally", "zygotically"], "article_id"=>843673, "categories"=>["Biological Sciences"], "users"=>["Liuliu Zheng", "Leonardo A. Sepúlveda", "Rhonald C. Lua", "Olivier Lichtarge", "Ido Golding", "Anna Marie Sokac"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003901.g005", "stats"=>{"downloads"=>0, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Spt_is_maternally_provided_while_Sry_945_is_zygotically_expressed_in_a_pulse_for_cellularization_/843673", "title"=>"Spt is maternally provided, while Sry-α is zygotically expressed in a pulse for cellularization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-07 02:45:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1271090"], "description"=>"<p>(A) Surface views of furrows and nuclei, detected in living embryos (membrane Gap43-mCherry, green; nuclear Histone-GFP, purple), following the indicated <i>sry-α<sup>RNAi</sup></i> or <i>spt<sup>RNAi</sup></i> treatment. Multinucleate cells highlighted (orange nuclei) in corresponding segmented images. (B) Quantification of multinucleation phenotypes. Each point represents one embryo with ≥150 nuclei analyzed (n = 12 embryos per condition). (C) Frequency of multinucleation for embryos following the indicated RNAi treatment (n≥6,000 nuclei from 30 embryos per treatment; mean ± s.e.m.). Student's t-test was performed to calculate P values as shown in (B, C).</p>", "links"=>[], "tags"=>["induce"], "article_id"=>843671, "categories"=>["Biological Sciences"], "users"=>["Liuliu Zheng", "Leonardo A. Sepúlveda", "Rhonald C. Lua", "Olivier Lichtarge", "Ido Golding", "Anna Marie Sokac"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003901.g003", "stats"=>{"downloads"=>0, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_sry_945_and_spt_induce_the_same_loss_of_function_phenotype_/843671", "title"=>"<i>sry-α</i> and <i>spt</i> induce the same loss of function phenotype.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-07 02:45:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1271091"], "description"=>"<p>(A) Surface views of furrow canals stained for Myosin-2 in embryos of indicated genotypes. Multinucleate cells highlighted (orange nuclei) in corresponding segmented images. (B) Quantification of multinucleation phenotypes. Each point represents one embryo with ≥150 nuclei analyzed (n = 12 embryos per condition). (C) Quantification of F-actin in furrow canals of furrows of length 3–5.5 µm (n = 9 embryos per genotype, with 15 furrows analyzed per embryo; mean ± s.e.m.). Student's t-test was performed to calculate P values as shown in (B, C).</p>", "links"=>[], "tags"=>["spt", "redundant"], "article_id"=>843672, "categories"=>["Biological Sciences"], "users"=>["Liuliu Zheng", "Leonardo A. Sepúlveda", "Rhonald C. Lua", "Olivier Lichtarge", "Ido Golding", "Anna Marie Sokac"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003901.g004", "stats"=>{"downloads"=>0, "page_views"=>17, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sry_945_and_Spt_share_redundant_function_during_cellularization_/843672", "title"=>"Sry-α and Spt share redundant function during cellularization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-07 02:45:04"}
  • {"files"=>["https://ndownloader.figshare.com/files/1271085"], "description"=>"<p>(A) Schematic of cellularization. In wild-type embryos (WT), furrows ingress between nuclei (purple) to form mononucleate cells. In mutants with reduced F-actin, some furrows regress, resulting in multinucleate cells (orange nuclei). (B) Surface views of furrow canals stained for Myosin-2 in embryos of indicated genotypes. Multinucleate cells highlighted (orange nuclei) in corresponding segmented images. (C) Cross sections show F-actin levels, as detected by phalloidin staining. Arrow indicates furrow canal position. (D) Quantification of F-actin levels in furrow canals. Each point represents one embryo with ≥75 furrow canals measured (mean ± s.d.). (E) Quantification of Amphiphysin (Amph) tubules. Each point represents one embryo with ≥100 furrows analyzed.</p>", "links"=>[], "tags"=>["regulates", "cortical", "f-actin"], "article_id"=>843666, "categories"=>["Biological Sciences"], "users"=>["Liuliu Zheng", "Leonardo A. Sepúlveda", "Rhonald C. Lua", "Olivier Lichtarge", "Ido Golding", "Anna Marie Sokac"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1003901.g001", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Sry_945_regulates_cortical_F_actin_levels_/843666", "title"=>"Sry-α regulates cortical F-actin levels.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-11-07 02:45:04"}

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Relative Metric

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