The DOI matches its Crossref record; 11 of the 11 references it cites were found in a registry or an index.
Quantitative proteome dynamics across embryogenesis in a model chordate
Open accessPublished version of a preprint
Abstract
The evolution of gene expression programs underlying the development of vertebrates remains poorly characterized. Here, we present a comprehensive proteome atlas of the model chordate Ciona , covering eight developmental stages and ∼7,000 translated genes, accompanied by a multi-omics analysis of co-evolution with the vertebrate Xenopus . Quantitative proteome comparisons argue against the widely held hourglass model, based solely on transcriptomic profiles, whereby peak conservation is observed during mid-developmental stages. Our analysis reveals maximal divergence at these stages, particularly gastrulation and neurulation. Together, our work provides a valuable resource for evaluating conservation and divergence of multi-omics profiles underlying the diversification of vertebrates.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
OrthoFinder: phylogenetic orthology inference for comparative genomics
Emms, D. M., & Kelly, S. (2019) · Genome Biology · doi:10.1186/s13059-019-1832-y · Cited by 7,676
Global quantification of mammalian gene expression control
Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., & Selbach, M. (2011) · Nature · doi:10.1038/nature10098 · Cited by 6,566
mRNAs, proteins and the emerging principles of gene expression control
Buccitelli, C., & Selbach, M. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-020-0258-4 · Cited by 1,243
Stochastic protein expression in individual cells at the single molecule level
Cai, L., Friedman, N., & Xie, X. S. (2006) · Nature · doi:10.1038/nature04599 · Cited by 1,145
Genome evolution in the allotetraploid frog Xenopus laevis
Session, A. M., Uno, Y., Kwon, T., Chapman, J. A., Toyoda, A., Takahashi, S., Fukui, A., Hikosaka, A., Suzuki, A., Kondo, M., et al. (2016) · Nature · doi:10.1038/nature19840 · Cited by 949
Comparative analysis of proteome and transcriptome variation in mouse
Ghazalpour, A., Bennett, B., Petyuk, V. A., Orozco, L., Hagopian, R., Mungrue, I. N., Farber, C. R., Sinsheimer, J., Kang, H. M., Furlotte, N., et al. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1001393 · Cited by 624
A Review on Quantitative Multiplexed Proteomics
Pappireddi, N., Martin, L., & Wühr, M. (2019) · ChemBioChem · doi:10.1002/cbic.201800650 · Cited by 299
Self-citationRNA sequencing reveals two major classes of gene expression levels in metazoan cells
Hebenstreit, D., Fang, M., Gu, M., Charoensawan, V., van Oudenaarden, A., & Teichmann, S. A. (2011) · Molecular Systems Biology · doi:10.1038/msb.2011.28 · Cited by 289
Comparative Functional Analysis of the Caenorhabditis elegans and Drosophila melanogaster Proteomes
Schrimpf, S. P., Weiss, M., Reiter, L., Ahrens, C. H., Jovanovic, M., Malmström, J., Brunner, E., Mohanty, S., Lercher, M. J., Hunziker, P. E., et al. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000048 · Cited by 229
Deeply conserved synteny and the evolution of metazoan chromosomes
Simakov, O., Bredeson, J., Berkoff, K., Marletaz, F., Mitros, T., Schultz, D. T., O’Connell, B. L., Dear, P., Martinez, D. E., Steele, R. E., et al. (2022) · Science Advances · doi:10.1126/sciadv.abi5884 · Cited by 197
Gillespie, M. A., Palii, C. G., Sanchez-Taltavull, D., Shannon, P., Longabaugh, W. J. R., Downes, D. J., Sivaraman, K., Espinoza, H. M., Hughes, J. R., Price, N. D., et al. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.03.031 · Cited by 110
Flagged first, then by citations
Research works printed but not linked: 134
- Hausser, 2019, Central dogma rates and the trade-off between precision and economy in gene expression, Nat. Commun., 10, 68, 10.1038/s41467-018-07391-8 · DOI · Paper page
- Li, 2014, Quantifying Absolute Protein Synthesis Rates Reveals Principles Underlying Allocation of Cellular Resources, Cell, 157, 624, 10.1016/j.cell.2014.02.033 · DOI
- Teixeira, 2019, Translational Control during Developmental Transitions, Cold Spring Harb. Perspect. Biol., 11, a032987, 10.1101/cshperspect.a032987 · DOI
- Peshkin, 2015, On the Relationship of Protein and mRNA Dynamics in Vertebrate Embryonic Development, Dev. Cell, 35, 383, 10.1016/j.devcel.2015.10.010 · DOI
- Smits, 2014, Global absolute quantification reveals tight regulation of protein expression in single Xenopus eggs, Nucleic Acids Res., 42, 9880, 10.1093/nar/gku661 · DOI
- Vogel, 2012, Insights into the regulation of protein abundance from proteomic and transcriptomic analyses, Nat. Rev. Genet., 13, 227, 10.1038/nrg3185 · DOI · Paper page
- Wegler, 2020, Global variability analysis of mRNA and protein concentrations across and within human tissues, NAR Genom. Bioinform., 2, lqz010, 10.1093/nargab/lqz010 · DOI
- Raj, 2008, Nature, Nurture, or Chance: Stochastic Gene Expression and Its Consequences, Cell, 135, 216, 10.1016/j.cell.2008.09.050 · DOI · Paper page
- Sonneveld, 2020, Heterogeneity in mRNA Translation, Trends Cell Biol., 30, 606, 10.1016/j.tcb.2020.04.008 · DOI
- Livingston, 2023, Bursting translation on single mRNAs in live cells, Mol. Cell, 83, 2276, 10.1016/j.molcel.2023.05.019 · DOI
- Aebersold, 2003, Mass spectrometry-based proteomics, Nature, 422, 198, 10.1038/nature01511 · DOI · Paper page
- Johnson, 2021, TMTpro Complementary Ion Quantification Increases Plexing and Sensitivity for Accurate Multiplexed Proteomics at the MS2 Level, J. Proteome Res., 20, 3043, 10.1021/acs.jproteome.0c00813 · DOI
- Thompson, 2003, Tandem Mass Tags: A Novel Quantification Strategy for Comparative Analysis of Complex Protein Mixtures by MS/MS, Anal. Chem., 75, 1895, 10.1021/ac0262560 · DOI
- Demichev, 2020, DIA-NN: neural networks and interference correction enable deep proteome coverage in high throughput, Nat. Methods, 17, 41, 10.1038/s41592-019-0638-x · DOI
- Ammar, 2023, Accurate label-free quantification by directLFQ to compare unlimited numbers of proteomes, Mol. Cell. Proteomics, 22, 100581, 10.1016/j.mcpro.2023.100581 · DOI
- McAlister, 2014, MultiNotch MS3 Enables Accurate, Sensitive, and Multiplexed Detection of Differential Expression across Cancer Cell Line Proteomes, Anal. Chem., 86, 7150, 10.1021/ac502040v · DOI · Paper page
- Lucitt, 2008, Analysis of the Zebrafish Proteome during Embryonic Development, Mol. Cell. Proteomics, 7, 981, 10.1074/mcp.M700382-MCP200 · DOI
- Gao, 2017, Protein Expression Landscape of Mouse Embryos during Pre-implantation Development, Cell Rep., 21, 3957, 10.1016/j.celrep.2017.11.111 · DOI
- Purushothaman, 2019, Proteomics Analysis of Early Developmental Stages of Zebrafish Embryos, Int. J. Mol. Sci., 20, 6359, 10.3390/ijms20246359 · DOI
- Sun, 2014, Quantitative proteomics of Xenopus laevis embryos: expression kinetics of nearly 4000 proteins during early development, Sci. Rep., 4, 4365, 10.1038/srep04365 · DOI
- Abdulghani, 2019, Comparative Analysis of the Transcriptome and Proteome during Mouse Placental Development, J. Proteome Res., 18, 2088, 10.1021/acs.jproteome.8b00970 · DOI
- Delsuc, 2006, Tunicates and not cephalochordates are the closest living relatives of vertebrates, Nature, 439, 965, 10.1038/nature04336 · DOI · Paper page
- Dehal, 2002, The Draft Genome of Ciona intestinalis: Insights into Chordate and Vertebrate Origins, Science, 298, 2157, 10.1126/science.1080049 · DOI · Paper page
- Olinski, 2006, Conserved Synteny Between the Ciona Genome and Human Paralogons Identifies Large Duplication Events in the Molecular Evolution of the Insulin-Relaxin Gene Family, Mol. Biol. Evol., 23, 10, 10.1093/molbev/msj002 · DOI
- Kikuta, 2007, Genomic regulatory blocks encompass multiple neighboring genes and maintain conserved synteny in vertebrates, Genome Res., 17, 545, 10.1101/gr.6086307 · DOI
- Doglio, 2013, Parallel Evolution of Chordate Cis-Regulatory Code for Development, PLoS Genet., 9, e1003904, 10.1371/journal.pgen.1003904 · DOI
- Sanges, 2013, Highly conserved elements discovered in vertebrates are present in non-syntenic loci of tunicates, act as enhancers and can be transcribed during development, Nucleic Acids Res., 41, 3600, 10.1093/nar/gkt030 · DOI
- Prummel, 2019, A conserved regulatory program initiates lateral plate mesoderm emergence across chordates, Nat. Commun., 10, 3857, 10.1038/s41467-019-11561-7 · DOI
- Abitua, 2012, Identification of a rudimentary neural crest in a non-vertebrate chordate, Nature, 492, 104, 10.1038/nature11589 · DOI
- Abitua, 2015, The pre-vertebrate origins of neurogenic placodes, Nature, 524, 462, 10.1038/nature14657 · DOI
- Stolfi, 2010, Early Chordate Origins of the Vertebrate Second Heart Field, Science, 329, 565, 10.1126/science.1190181 · DOI
- Stolfi, 2015, Migratory neuronal progenitors arise from the neural plate borders in tunicates, Nature, 527, 371, 10.1038/nature15758 · DOI
- Horie, 2018, Shared evolutionary origin of vertebrate neural crest and cranial placodes, Nature, 560, 228, 10.1038/s41586-018-0385-7 · DOI
- Lemaire, 2021, The hypothalamus predates the origin of vertebrates, Sci. Adv., 7, eabf7452, 10.1126/sciadv.abf7452 · DOI
- Long, 2023, Cereblon influences the timing of muscle differentiation in Ciona tadpoles, Proc. Natl. Acad. Sci. USA, 120, 10.1073/pnas.2309989120 · DOI
- Reeves, 2017, Functional and evolutionary insights from the Ciona notochord transcriptome, Development, 144, 3375, 10.1242/dev.156174 · DOI
- Papadogiannis, 2022, Hmx gene conservation identifies the origin of vertebrate cranial ganglia, Nature, 605, 701, 10.1038/s41586-022-04742-w · DOI
- Cao, 2019, Comprehensive single-cell transcriptome lineages of a proto-vertebrate, Nature, 571, 349, 10.1038/s41586-019-1385-y · DOI
- Keller, 2016, Evolutionary Transition of Promoter and Gene Body DNA Methylation across Invertebrate–Vertebrate Boundary, Mol. Biol. Evol., 33, 1019, 10.1093/molbev/msv345 · DOI
- Zhang, 2020, A single-cell analysis of the molecular lineage of chordate embryogenesis, Sci. Adv., 6, eabc4773, 10.1126/sciadv.abc4773 · DOI
- Sladitschek, 2020, MorphoSeq: Full Single-Cell Transcriptome Dynamics Up to Gastrulation in a Chordate, Cell, 181, 922, 10.1016/j.cell.2020.03.055 · DOI
- Suzuki, 2016, The Ciona intestinalis cleavage clock is independent of DNA methylation, Genomics, 108, 168, 10.1016/j.ygeno.2016.10.001 · DOI
- Madgwick, 2019, Evolution of embryonic cis-regulatory landscapes between divergent Phallusia and Ciona ascidians, Dev. Biol., 448, 71, 10.1016/j.ydbio.2019.01.003 · DOI
- Kubo, 2010, Genomic cis-regulatory networks in the early Ciona intestinalis embryo, Development, 137, 1613, 10.1242/dev.046789 · DOI
- Irie, 2011, Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis, Nat. Commun., 2, 248, 10.1038/ncomms1248 · DOI
- Yanai, 2011, Mapping Gene Expression in Two Xenopus Species: Evolutionary Constraints and Developmental Flexibility, Dev. Cell, 20, 483, 10.1016/j.devcel.2011.03.015 · DOI
- Gerstein, 2014, Comparative analysis of the transcriptome across distant species, Nature, 512, 445, 10.1038/nature13424 · DOI
- Chan, 2021, Comparative transcriptomics reveals distinct patterns of gene expression conservation through vertebrate embryogenesis, Genome Biol. Evol., 13, evab160, 10.1093/gbe/evab160 · DOI
- Uesaka, 2022, The developmental hourglass model and recapitulation: An attempt to integrate the two models, J. Exp. Zool. B Mol. Dev. Evol., 338, 76, 10.1002/jez.b.23027 · DOI
- Hu, 2017, Constrained vertebrate evolution by pleiotropic genes, Nat. Ecol. Evol., 1, 1722, 10.1038/s41559-017-0318-0 · DOI
- Marlétaz, 2018, Amphioxus functional genomics and the origins of vertebrate gene regulation, Nature, 564, 64, 10.1038/s41586-018-0734-6 · DOI
- Levin, 2016, The mid-developmental transition and the evolution of animal body plans, Nature, 531, 637, 10.1038/nature16994 · DOI
- Wu, 2019, Gene Expression Does Not Support the Developmental Hourglass Model in Three Animals with Spiralian Development, Mol. Biol. Evol., 36, 1373, 10.1093/molbev/msz065 · DOI
- Bininda-Emonds, 2003, Inverting the hourglass: quantitative evidence against the phylotypic stage in vertebrate development, Proc. R. Soc. Lond. Ser. B Biol. Sci., 270, 341, 10.1098/rspb.2002.2242 · DOI
- Dunn, 2018, Pairwise comparisons across species are problematic when analyzing functional genomic data, Proc. Natl. Acad. Sci. USA, 115, E409, 10.1073/pnas.1707515115 · DOI
- Yanai, 2018, Development and Evolution through the Lens of Global Gene Regulation, Trends Genet., 34, 11, 10.1016/j.tig.2017.09.011 · DOI
- Laurent, 2010, Protein abundances are more conserved than mRNA abundances across diverse taxa, Proteomics, 10, 4209, 10.1002/pmic.201000327 · DOI · Paper page
- Baxi, 2018, Proteomic Characterization of the Neural Ectoderm Fated Cell Clones in the Xenopus laevis Embryo by High-Resolution Mass Spectrometry, ACS Chem. Neurosci., 9, 2064, 10.1021/acschemneuro.7b00525 · DOI
- Wühr, 2014, Deep Proteomics of the Xenopus laevis Egg using an mRNA-Derived Reference Database, Curr. Biol., 24, 1467, 10.1016/j.cub.2014.05.044 · DOI
- Gupta, 2018, Quantitative Proteomics of Xenopus Embryos I, Sample Preparation, Methods Mol. Biol., 1865, 175, 10.1007/978-1-4939-8784-9_13 · DOI
- Evans, 2012, De novo derivation of proteomes from transcriptomes for transcript and protein identification, Nat. Methods, 9, 1207, 10.1038/nmeth.2227 · DOI · Paper page
- Kaplan, 2019, Initial characterization of Wnt-Tcf functions during Ciona heart development, Dev. Biol., 448, 199, 10.1016/j.ydbio.2018.12.018 · DOI
- Sharma, 2019, Single-cell transcriptome profiling of the Ciona larval brain, Dev. Biol., 448, 226, 10.1016/j.ydbio.2018.09.023 · DOI
- Wang, 2019, A single-cell transcriptional roadmap for cardiopharyngeal fate diversification, Nat. Cell Biol., 21, 674, 10.1038/s41556-019-0336-z · DOI
- Bateman, 2022, UniProt: the Universal Protein Knowledgebase in 2023, Nucleic Acids Res., 51, D523
- Satou, 2019, A Nearly Complete Genome of Ciona intestinalis Type A (C. robusta) Reveals the Contribution of Inversion to Chromosomal Evolution in the Genus Ciona, Genome Biol. Evol., 11, 3144, 10.1093/gbe/evz228 · DOI
- Satou, 2022, A Manually Curated Gene Model Set for an Ascidian, Ciona robusta (Ciona intestinalis Type A), Zoolog. Sci., 39, 253, 10.2108/zs210102 · DOI
- Tsagkogeorga, 2012, The Population Genomics of a Fast Evolver: High Levels of Diversity, Functional Constraint, and Molecular Adaptation in the Tunicate Ciona intestinalis, Genome Biol. Evol., 4, 740, 10.1093/gbe/evs054 · DOI
- Santesmasses, 2018, Selenoproteins, Methods and Protocols, Methods Mol. Biol., 1661, 17, 10.1007/978-1-4939-7258-6_2 · DOI
- Satou, 2006, Genomic overview of mRNA 5′-leader trans-splicing in the ascidian Ciona intestinalis, Nucleic Acids Res., 34, 3378, 10.1093/nar/gkl418 · DOI
- Messerschmidt, 2012, Trim28 Is Required for Epigenetic Stability During Mouse Oocyte to Embryo Transition, Science, 335, 1499, 10.1126/science.1216154 · DOI
- Bultman, 2006, Maternal BRG1 regulates zygotic genome activation in the mouse, Genes Dev., 20, 1744, 10.1101/gad.1435106 · DOI
- Toralova, 2020, The neglected part of early embryonic development: maternal protein degradation, Cell. Mol. Life Sci., 77, 3177, 10.1007/s00018-020-03482-2 · DOI
- Zhang, 2023, Stable maternal proteins underlie distinct transcriptome, translatome, and proteome reprogramming during mouse oocyte-to-embryo transition, Genome Biol., 24, 166, 10.1186/s13059-023-02997-8 · DOI
- Yamada, 2009, Comprehensive Egg Coat Proteome of the Ascidian Ciona intestinalis Reveals Gamete Recognition Molecules Involved in Self-sterility, J. Biol. Chem., 284, 9402, 10.1074/jbc.M809672200 · DOI
- Nomura, 2009, Proteomic profiles of embryonic development in the ascidian Ciona intestinalis, Dev. Biol., 325, 468, 10.1016/j.ydbio.2008.10.038 · DOI
- Imai, 2004, Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: towards a comprehensive understanding of gene networks, Development, 131, 4047, 10.1242/dev.01270 · DOI
- Ahn, 2012, The Ascidian Numb Gene Involves in the Formation of Neural Tissues, Dev. Reprod., 16, 371, 10.12717/DR.2012.16.4.371 · DOI
- Walton, 2006, Genomics and expression profiles of the Hedgehog and Notch signaling pathways in sea urchin development, Dev. Biol., 300, 153, 10.1016/j.ydbio.2006.08.064 · DOI
- Oda-Ishii, 2016, A Maternal System Initiating the Zygotic Developmental Program through Combinatorial Repression in the Ascidian Embryo, PLoS Genet., 12, e1006045, 10.1371/journal.pgen.1006045 · DOI
- Yamada, 2006, Embryonic expression profiles and conserved localization mechanisms of pem/postplasmic mRNAs of two species of ascidian, Ciona intestinalis and Ciona savignyi, Dev. Biol., 296, 524, 10.1016/j.ydbio.2006.05.018 · DOI
- Shirae-Kurabayashi, 2011, Ci-Pem-1 localizes to the nucleus and represses somatic gene transcription in the germline of Ciona intestinalis embryos, Development, 138, 2871, 10.1242/dev.058131 · DOI
- Tsitsiridis, 2023, CORUM: the comprehensive resource of mammalian protein complexes–2022, Nucleic Acids Res., 51, D539, 10.1093/nar/gkac1015 · DOI
- Bochman, 2009, The Mcm Complex: Unwinding the Mechanism of a Replicative Helicase, Microbiol. Mol. Biol. Rev., 73, 652, 10.1128/MMBR.00019-09 · DOI
- Kubota, 2002, Function and regulation of cytosolic molecular chaperone CCT, Vitam. Horm., 65, 313, 10.1016/S0083-6729(02)65069-1 · DOI
- Uehara, 2009, The augmin complex plays a critical role in spindle microtubule generation for mitotic progression and cytokinesis in human cells, Proc. Natl. Acad. Sci. USA, 106, 6998, 10.1073/pnas.0901587106 · DOI
- Liang, 2020, The functions and mechanisms of prefoldin complex and prefoldin-subunits, Cell Biosci., 10, 87, 10.1186/s13578-020-00446-8 · DOI
- Elias, 2007, Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry, Nat. Methods, 4, 207, 10.1038/nmeth1019 · DOI · Paper page
- Cao, 2020, Precise Temporal Regulation of Post-transcriptional Repressors Is Required for an Orderly Drosophila Maternal-to-Zygotic Transition, Cell Rep., 31, 107783, 10.1016/j.celrep.2020.107783 · DOI
- White, 2017, A high-resolution mRNA expression time course of embryonic development in zebrafish, Elife, 6, e30860, 10.7554/eLife.30860 · DOI
- Imai, 2006, Regulatory Blueprint for a Chordate Embryo, Science, 312, 1183, 10.1126/science.1123404 · DOI
- Kobayashi, 2018, Controlling Cell Fate Specification System by Key Genes Determined from Network Structure, iScience, 4, 281, 10.1016/j.isci.2018.05.004 · DOI
- Mochizuki, 2003, Large-scale characterization of genes specific to the larval nervous system in the ascidian Ciona intestinalis, Genesis, 36, 62, 10.1002/gene.10199 · DOI
- Satou, 2001, Gene expression profiles in Ciona intestinalis tailbud embryos, Development, 128, 2893, 10.1242/dev.128.15.2893 · DOI
- Kawai, 2015, Hox10-regulated endodermal cell migration is essential for development of the ascidian intestine, Dev. Biol., 403, 43, 10.1016/j.ydbio.2015.03.018 · DOI
- Wang, 2019, A deep proteome and transcriptome abundance atlas of 29 healthy human tissues, Mol. Syst. Biol., 15, e8503, 10.15252/msb.20188503 · DOI · Paper page
- Mergner, 2020, Mass-spectrometry-based draft of the Arabidopsis proteome, Nature, 579, 409, 10.1038/s41586-020-2094-2 · DOI
- Sonnett, 2018, Quantitative Proteomics for Xenopus Embryos II, Data Analysis, Methods Mol. Biol., 1865, 195, 10.1007/978-1-4939-8784-9_14 · DOI
- Itallie, 2021, Transitions in the proteome and phospho-proteome during xenopus laevis development, bioRxiv
- Delsuc, 2018, A phylogenomic framework and timescale for comparative studies of tunicates, BMC Biol., 16, 39, 10.1186/s12915-018-0499-2 · DOI
- Izzi, 2013, Functional studies of the Ciona intestinalis myogenic regulatory factor reveal conserved features of chordate myogenesis, Dev. Biol., 376, 213, 10.1016/j.ydbio.2013.01.033 · DOI
- Veeman, 2008, chongmague reveals an essential role for laminin-mediated boundary formation in chordate convergence and extension movements, Development, 135, 33, 10.1242/dev.010892 · DOI
- Hanel, 2009, Muscular dystrophy candidate gene FRG1 is critical for muscle development, Dev. Dyn., 238, 1502, 10.1002/dvdy.21830 · DOI
- Wuebbles, 2009, FSHD region gene 1 (FRG1) is crucial for angiogenesis linking FRG1 to facioscapulohumeral muscular dystrophy-associated vasculopathy, Dis. Model. Mech., 2, 267, 10.1242/dmm.002261 · DOI
- Lyabin, 2014, YB-1 protein: functions and regulation, Wiley Interdiscip. Rev. RNA, 5, 95, 10.1002/wrna.1200 · DOI · Paper page
- Kumari, 2013, An essential role for maternal control of Nodal signaling, Elife, 2, e00683, 10.7554/eLife.00683 · DOI
- Winkley, 2020, Tunicate gastrulation, Curr. Top. Dev. Biol., 136, 219, 10.1016/bs.ctdb.2019.09.001 · DOI
- Liu, 2018, Adaptive Evolution of Animal Proteins over Development: Support for the Darwin Selection Opportunity Hypothesis of Evo-Devo, Mol. Biol. Evol., 35, 2862
- Roux, 2008, Developmental Constraints on Vertebrate Genome Evolution, PLoS Genet., 4, e1000311, 10.1371/journal.pgen.1000311 · DOI
- Klont, 2018, Assessment of Sample Preparation Bias in Mass Spectrometry-Based Proteomics, Anal. Chem., 90, 5405, 10.1021/acs.analchem.8b00600 · DOI
- Brozovic, 2018, ANISEED 2017: extending the integrated ascidian database to the exploration and evolutionary comparison of genome-scale datasets, Nucleic Acids Res., 46, D718, 10.1093/nar/gkx1108 · DOI
- Altschul, 1990, Basic local alignment search tool, J. Mol. Biol., 215, 403, 10.1016/S0022-2836(05)80360-2 · DOI · Paper page
- Grabherr, 2011, Full-length transcriptome assembly from RNA-Seq data without a reference genome, Nat. Biotechnol., 29, 644, 10.1038/nbt.1883 · DOI
- Pertea, 2003, TIGR Gene Indices clustering tools (TGICL): a software system for fast clustering of large EST datasets, Bioinformatics, 19, 651, 10.1093/bioinformatics/btg034 · DOI
- Huang, 1999, CAP3: A DNA Sequence Assembly Program, Genome Res., 9, 868, 10.1101/gr.9.9.868 · DOI · Paper page
- Fu, 2012, CD-HIT: accelerated for clustering the next-generation sequencing data, Bioinformatics, 28, 3150, 10.1093/bioinformatics/bts565 · DOI · Paper page
- Li, 2006, Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences, Bioinformatics, 22, 1658, 10.1093/bioinformatics/btl158 · DOI
- Kolberg, 2023, g:Profiler—interoperable web service for functional enrichment analysis and gene identifier mapping (2023 update), Nucleic Acids Res., 51, W207, 10.1093/nar/gkad347 · DOI · Paper page
- Patro, 2017, Salmon provides fast and bias-aware quantification of transcript expression, Nat. Methods, 14, 417, 10.1038/nmeth.4197 · DOI · Paper page
- Hotta, 2007, A web-based interactive developmental table for the ascidian Ciona intestinalis, including 3D real-image embryo reconstructions: I. From fertilized egg to hatching larva, Dev. Dyn., 236, 1790, 10.1002/dvdy.21188 · DOI
- Zahn, 2022, Normal Table of Xenopus development: a new graphical resource, Development, 149, dev200356, 10.1242/dev.200356 · DOI
- Brunetti, 2015, Morphological evidence that the molecularly determined Ciona intestinalis type A and type B are different species: Ciona robusta and Ciona intestinalis, J. Zoolog. Syst. Evol. Res., 53, 186, 10.1111/jzs.12101 · DOI
- Christiaen, 2009, Isolation of Sea Squirt (Ciona) Gametes, Fertilization, Dechorionation, and Development: Figure 1, Cold Spring Harb. Protoc., 10.1101/pdb.prot5344 · DOI
- Abdul-Wajid, 2014, Exploiting the Extraordinary Genetic Polymorphism of Ciona for Developmental Genetics with Whole Genome Sequencing, Genetics, 197, 49, 10.1534/genetics.114.161778 · DOI
- Wessel, 1984, A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids, Anal. Biochem., 138, 141, 10.1016/0003-2697(84)90782-6 · DOI
- Nguyen, 2022, Differential nuclear import sets the timing of protein access to the embryonic genome, Nat. Commun., 13, 5887, 10.1038/s41467-022-33429-z · DOI
- Edwards, 2016, Multiplexed Quantitative Proteomics for High-Throughput Comprehensive Proteome Comparisons of Human Cell Lines, Methods Mol. Biol., 1394, 1, 10.1007/978-1-4939-3341-9_1 · DOI
- Rappsilber, 2007, Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips, Nat. Protoc., 2, 1896, 10.1038/nprot.2007.261 · DOI · Paper page
- Eng, 1994, An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database, J. Am. Soc. Mass Spectrom., 5, 976, 10.1016/1044-0305(94)80016-2 · DOI · Paper page
- Savitski, 2015, A Scalable Approach for Protein False Discovery Rate Estimation in Large Proteomic Data Sets[S], Mol. Cell. Proteomics, 14, 2394, 10.1074/mcp.M114.046995 · DOI
- Satou, 2005, An Integrated Database of the Ascidian, Ciona intestinalis: Towards Functional Genomics, Zoolog. Sci., 22, 837, 10.2108/zsj.22.837 · DOI
- Nitta, 2019, High-Throughput Protein Production and Purification, Methods and Protocols, Methods Mol. Biol., 2025, 487, 10.1007/978-1-4939-9624-7_23 · DOI
- Treen, 2023, An FGF timer for zygotic genome activation, Genes Dev., 37, 80, 10.1101/gad.350164.122 · DOI
- Soneson, 2015, Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences, F1000Res., 4, 1521, 10.12688/f1000research.7563.1 · DOI · Paper page
Metadata
- Authors
- Frese, A. N., Mariossi, A., Levine, M. S., & Wühr, M.
- Affiliations
- Princeton University (US)
- Corresponding author
- Levine, Michael S.
- Wühr, Martin
- Venue
- iScience
- Publisher
- Elsevier BV
- Published
- 2024-04
- Volume
- 27
- Issue
- 4
- Pages
- 109355
- ISSN
- 2589-0042 (ISSN-L)
- PMC
- PMC10951915
- OpenAlex
- W4392302660
- Cited by
- 10
- References
- 11
- Citations by year
- 2026: 6 · 2025: 2 · 2024: 2
- FWCI
- 1.36
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- iScience (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Princeton University (R35GM128813, NS076542)
- NIH (R35GM128813, NS076542, T32GM007388)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- embryonic development, proteome dynamics, Ciona intestinalis, Xenopus, hourglass model, developmental gene expression, gastrulation, neurulation, vertebrate evolution
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review