PreprintCited by 10Developmental Biology and Gene RegulationAdvanced Proteomics Techniques and ApplicationsGenomics and Phylogenetic Studies

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Quantitative proteome dynamics across embryogenesis in a model chordate

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Preprint — published as 10.1016/j.isci.2024.109355 · Paper page

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.

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  1. 10.1021/acs.jproteome.8b00970 · DOI
  2. 10.1534/genetics.114.161778 · DOI
  3. 10.1038/nature14657 · DOI
  4. 10.1038/nature11589 · DOI
  5. 2012, The Ascidian Numb Gene Involves in the Formation of Neural Tissues, Dev Reprod, 16, 371, 10.12717/DR.2012.16.4.371 · DOI
  6. 10.1006/jmbi.1990.9999 · DOI · Paper page
  7. Ammar C , Schessner JP , Willems S , Michaelis AC , Mann M. 2023. Accurate label-free quantification by directLFQ to compare unlimited numbers of proteomes. Mol Cell Proteom 100581. · DOI
  8. 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
  9. 2021, Mass spectrometry based proteomics for developmental neurobiology in the amphibian Xenopus laevis, Curr Top Dev Biology, 145, 205, 10.1016/bs.ctdb.2021.04.002 · DOI
  10. 2018, Complexity and conservation of regulatory landscapes underlie evolutionary resilience of mammalian gene expression, Nat Ecol Evol, 2, 152
  11. 10.1093/nar/gkv966 · DOI
  12. 2015, Morphological evidence that the molecularly determined Ciona intestinalis type A and type B are different species: Ciona robusta and Ciona intestinalis, J Zoo□l Syst Evol Res, 53, 186, 10.1111/jzs.12101 · DOI
  13. 10.1101/gad.1435106 · DOI
  14. 2019, Comprehensive single-cell transcriptome lineages of a proto-vertebrate, Nature, 571, 349, 10.1038/s41586-019-1385-y · DOI
  15. 2021, Comparative Transcriptomics Reveals Distinct Patterns of Gene Expression Conservation through Vertebrate Embryogenesis, Genome Biol Evol, 13, evab160, 10.1093/gbe/evab160 · DOI
  16. Christiaen L , Wagner E , Shi W , Levine M. 2009. Isolation of sea squirt (Ciona) gametes, fertilization, dechorionation, and development. Cold Spring Harb Protoc 2009: pdb.prot5344. · DOI
  17. 10.1126/science.abn3943 · DOI · Paper page
  18. 10.1126/science.1080049 · DOI · Paper page
  19. 10.1038/nature04336 · DOI · Paper page
  20. 10.1186/s12915-018-0499-2 · DOI
  21. 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
  22. 10.15252/msb.20167144 · DOI · Paper page
  23. 2015, Multiplexed Quantitative Proteomics for High-Throughput Comprehensive Proteome Comparisons of Human Cell Lines, Methods Mol biology Clifton N J, 1394, 1
  24. 10.1038/nmeth1019 · DOI · Paper page
  25. 10.1186/s13059-019-1832-y · DOI · Paper page
  26. 10.1038/nmeth.2227 · DOI · Paper page
  27. 10.1093/bioinformatics/bts565 · DOI · Paper page
  28. 10.1038/nature02046 · DOI · Paper page
  29. 10.1371/journal.pgen.1001393 · DOI · Paper page
  30. 2022, Gain of gene regulatory network interconnectivity at the origin of vertebrates, Proc National Acad Sci, 119, e2114802119, 10.1073/pnas.2114802119 · DOI
  31. Goldberger R. 1980. Biological Regulation and Development, Molecular Organization and Cell Function. · DOI
  32. 10.1038/nbt.1883 · DOI
  33. 2018, Quantitative Proteomics of Xenopus Embryos I, Sample Preparation, Methods Mol Biology Clifton N J, 1865, 175, 10.1007/978-1-4939-8784-9_13 · DOI
  34. Haeckel E. 1866. bd. Allgemeine entwickelungsgeschichte der organismen. G. Reimer. · DOI
  35. 10.1038/s41586-018-0385-7 · DOI
  36. 10.1002/dvdy.21188 · DOI
  37. 2017, Constrained vertebrate evolution by pleiotropic genes, Nat Ecol Evol, 1, 1722, 10.1038/s41559-017-0318-0 · DOI
  38. 10.1101/gr.9.9.868 · DOI · Paper page
  39. 10.1242/dev.01270 · DOI
  40. 10.1126/science.1123404 · DOI
  41. 10.1016/j.ydbio.2013.01.033 · DOI
  42. 10.1021/acs.jproteome.0c00813 · DOI
  43. 10.1016/j.ydbio.2018.12.018 · DOI
  44. 10.1093/molbev/msv345 · DOI
  45. 2021, Disruption of left-right axis specification in Ciona induces molecular, cellular, and functional defects in asymmetric brain structures, BMC Biol, 19, 141, 10.1186/s12915-021-01075-4 · DOI
  46. 10.1242/dev.046789 · DOI
  47. 10.1002/pmic.201000327 · DOI · Paper page
  48. 10.1038/nature16994 · DOI
  49. 10.1093/bioinformatics/btl158 · DOI
  50. 10.1242/bio.024786 · DOI
  51. 10.1016/j.ydbio.2019.01.003 · DOI
  52. 2018, Amphioxus functional genomics and the origins of vertebrate gene regulation, Nature, 564, 64, 10.1038/s41586-018-0734-6 · DOI
  53. 10.1021/ac502040v · DOI · Paper page
  54. 10.1126/science.1216154 · DOI
  55. 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
  56. 10.1016/j.ydbio.2008.10.038 · DOI
  57. 2019, A Review on Quantitative Multiplexed Proteomics, ChemBioChem, 20, 1210, 10.1002/cbic.201800650 · DOI · Paper page
  58. 10.1016/j.devcel.2015.10.010 · DOI
  59. 10.1242/dev.156174 · DOI
  60. 2017, Selenoproteins, Methods and Protocols, Methods Mol Biology, 1661, 17
  61. 10.1093/nar/gkl418 · DOI
  62. 10.1093/gbe/evz228 · DOI
  63. 10.2108/zs210102 · DOI
  64. 2013, Proteome map of the neural complex of the tunicate Ciona intestinalis, the closest living relative to vertebrates, PROTEOMICS, 13, 860, 10.1002/pmic.201200148 · DOI
  65. 10.1371/journal.pbio.1000048 · DOI · Paper page
  66. 10.1038/nature19840 · DOI · Paper page
  67. 2019, Single-cell transcriptome profiling of the Ciona larval brain, Dev Biology, 448, 226, 10.1016/j.ydbio.2018.09.023 · DOI
  68. 10.1016/j.cell.2020.03.055 · DOI
  69. 10.1093/nar/gku661 · DOI
  70. 2018, Quantitative Proteomics for Xenopus Embryos II, Data Analysis, Methods Mol Biology Clifton N J, 1865, 195, 10.1007/978-1-4939-8784-9_14 · DOI
  71. 10.1021/acs.analchem.7b04713 · DOI
  72. 10.1126/science.1190181 · DOI
  73. 10.1038/nature15758 · DOI
  74. 2016, Proteomics of Xenopus development, MHR Basic Sci reproductive medicine, 22, 193, 10.1093/molehr/gav052 · DOI
  75. 2016, The Ciona intestinalis cleavage clock is independent of DNA methylation, Genomics, 108, 168, 10.1016/j.ygeno.2016.10.001 · DOI
  76. 10.1021/ac0262560 · DOI
  77. 2020, Ancient genomic regulatory blocks are a source for regulatory gene deserts in vertebrates after whole genome duplications, Mol Biol Evol, 37, msaa123.
  78. 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, 852, 10.1093/gbe/evs054 · DOI
  79. 2022, CORUM: the comprehensive resource of mammalian protein complexes–2022, Nucleic Acids Res, 51, D539
  80. 2022, The developmental hourglass model and recapitulation: An attempt to integrate the two models, J Exp Zoo □l Part B, Mol Dev Evol, 338, 76, 10.1002/jez.b.23027 · DOI
  81. 10.1242/dev.010892 · DOI
  82. 10.1038/nrg3185 · DOI · Paper page
  83. 10.1016/j.ydbio.2006.08.064 · DOI
  84. 10.1242/dev.024539 · DOI
  85. 10.1038/s41556-019-0336-z · DOI
  86. Wegler C , Ölander M , Wiśniewski JR , Lundquist P , Zettl K , Ásberg A , Hjelmesæth J , Andersson TB , Artursson P. 2019. Global variability analysis of mRNA and protein concentrations across and within human tissues. Nar Genom Bioinform 2: qz010. · DOI
  87. 2019, Tunicate gastrulation, Curr Top Dev Biol, 136, 219
  88. 10.1016/j.cub.2014.05.044 · DOI
  89. 10.1074/jbc.M809672200 · DOI
  90. 10.1126/sciadv.abc4773 · DOI

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
openRxiv
Published
2023-10-06
Volume
27
Issue
4
Pages
109355-109355
ISSN
2589-0042 (ISSN-L)
OpenAlex
W4392302660
Cited by
10
References
1
Citations by year
2026: 6 · 2025: 2 · 2024: 2
FWCI
1.36
Type
journal article
Language
en
Open access
Licence
cc-by
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)
  • National Institutes of Health
  • National Institute of General Medical Sciences (T32GM007388, R35GM128813)
  • National Institute of Neurological Disorders and Stroke (R01NS076542)
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

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