How complexity increases in development: An analysis of the spatial-temporal dynamics of Gene expression in Ciona intestinalis

The increase in complexity in an embryo over developmental time is perhaps one of the most intuitive processes of animal development. It is also intuitive that the embryo becomes progressively compartmentalized over time and space. In spite of this intuitiveness, there are no systematic attempts to quantify how this occurs. Here, we present a quantitative analysis of the compartmentalization and spatial complexity of Ciona intestinalis over developmental time by analyzing thousands of gene expression spatial patterns from the ANISEED database. We measure compartmentalization in two ways: as the relative volume of expression of genes and as the disparity in gene expression between body parts. We also use a measure of the curvature of each gene expression pattern in 3D space. These measures show a similar increase over time, with the most dramatic change occurring from the 112-cell stage to the early tailbud stage. Combined, these measures point to a global pattern of increase in complexity in the Ciona embryo. Finally, we cluster the different regions of the embryo depending on their gene expression similarity, within and between stages. Results from this clustering analysis, which partially correspond to known fate maps, provide a global quantitative overview about differentiation and compartmentalization between body parts at each developmental stage.

[1]  C. M. Child.  The Organization and Cell-lineage of the Ascidian Egg , 1906 .

[2]  Julia M. Winchester,et al.  MorphoTester: An Open Source Application for Morphological Topographic Analysis , 2016, PloS one.

[3]  N. Satoh,et al.  Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. II. The 16- and 32-cell stages. , 1985, Developmental biology.

[4]  Michael Levine,et al.  Regulatory Blueprint for a Chordate Embryo , 2006, Science.

[5]  N. Satoh.  Tunicate Embryos and Cell Specification , 2011 .

[6]  I. Meinertzhagen,et al.  Development of the central nervous system of the larva of the ascidian, Ciona intestinalis L. II. Neural plate morphogenesis and cell lineages during neurulation. , 1988, Developmental biology.

[7]  Frédéric Delsuc,et al.  ANISEED 2015: a digital framework for the comparative developmental biology of ascidians , 2015, Nucleic Acids Res..

[8]  V. Papaioannou.  The T-box gene family: emerging roles in development, stem cells and cancer , 2014, Development.

[9]  P. Lemaire.  Unfolding a chordate developmental program, one cell at a time: invariant cell lineages, short-range inductions and evolutionary plasticity in ascidians. , 2009, Developmental biology.

[10]  Kevin Struhl,et al.  Mechanisms for diversity in gene expression patterns , 1991, Neuron.

[11]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[12]  D. Hinton,et al.  Gene expression throughout a vertebrate's embryogenesis , 2011, BMC Genomics.

[13]  C. Hudson,et al.  Sequential and combinatorial inputs from Nodal, Delta2/Notch and FGF/MEK/ERK signalling pathways establish a grid-like organisation of distinct cell identities in the ascidian neural plate , 2007, Development.

[14]  Michael Garland,et al.  Surface simplification using quadric error metrics , 1997, SIGGRAPH.

[15]  Yaron Lipman,et al.  Comparing Dirichlet normal surface energy of tooth crowns, a new technique of molar shape quantification for dietary inference, with previous methods in isolation and in combination. , 2011, American Journal of Physical Anthropology.

[16]  Yutaka Satou,et al.  Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: towards a comprehensive understanding of gene networks , 2004, Development.

[17]  C. Hudson,et al.  A signalling relay involving Nodal and Delta ligands acts during secondary notochord induction in Ciona embryos , 2006, Development.

[18]  H. Nishida,et al.  Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III. Up to the tissue restricted stage. , 1987, Developmental biology.

[19]  V. Simons.  Three-dimensional anatomy , 2015, Veterinary Record.

[20]  Delphine Dauga,et al.  The ANISEED database: digital representation, formalization, and elucidation of a chordate developmental program. , 2010, Genome research.

[21]  Martin Vingron,et al.  Gene expression screening in Xenopus identifies molecular pathways, predicts gene function and provides a global view of embryonic patterning , 1998, Mechanisms of Development.

[22]  D. McShea.  PERSPECTIVE METAZOAN COMPLEXITY AND EVOLUTION: IS THERE A TREND? , 1996, Evolution; international journal of organic evolution.

[23]  Ian A Meinertzhagen,et al.  The central nervous system of the ascidian larva: mitotic history of cells forming the neural tube in late embryonic Ciona intestinalis. , 2004, Developmental biology.

[24]  Ulrich Bodenhofer,et al.  APCluster: an R package for affinity propagation clustering , 2011, Bioinform..

[25]  B. S. Baker,et al.  Gene Expression During the Life Cycle of Drosophila melanogaster , 2002, Science.

[26]  Paolo Cignoni,et al.  Ieee Transactions on Visualization and Computer Graphics 1 Efficient and Flexible Sampling with Blue Noise Properties of Triangular Meshes , 2022 .

[27]  E. Davidson.  Developmental biology at the systems level. , 2009, Biochimica et biophysica acta.

[28]  Takeshi Kawashima,et al.  An Integrated Database of the Ascidian, Ciona intestinalis: Towards Functional Genomics , 2005, Zoological science.

[29]  E. Conklin.  Scientific Books: The Organization and Cell-Lineage of the Ascidian Egg , 1905 .

[30]  M. Levine,et al.  Regulation of Ci-tropomyosin-like, a Brachyury target gene in the ascidian, Ciona intestinalis. , 1999, Development.

[31]  Ken Dewar,et al.  Improved genome assembly and evidence-based global gene model set for the chordate Ciona intestinalis: new insight into intron and operon populations , 2008, Genome Biology.

[32]  M. Levine,et al.  Dorsoventral patterning of the vertebrate neural tube is conserved in a protochordate. , 1997, Development.

[33]  N. Satoh,et al.  Early embryonic expression of FGF4/6/9 gene and its role in the induction of mesenchyme and notochord in Ciona savignyi embryos. , 2002, Development.

[34]  Kazuho Ikeo,et al.  A web‐based interactive developmental table for the ascidian Ciona intestinalis, including 3D real‐image embryo reconstructions: I. From fertilized egg to hatching larva , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[35]  M. Levine,et al.  Characterization of a notochord-specific enhancer from the Brachyury promoter region of the ascidian, Ciona intestinalis. , 1997, Development.

[36]  C. Hudson,et al.  Patterning across the ascidian neural plate by lateral Nodal signalling sources , 2005, Development.

[37]  E. Davidson.  Genomic Regulatory Systems: Development and Evolution , 2005 .

[38]  Khalid Raza,et al.  GENE EXPRESSION PROFILES , 2007 .

[39]  Y. Kohara,et al.  Gene expression profiles in Ciona intestinalis tailbud embryos. , 2001, Development.

[40]  Y. Kohara,et al.  Gene expression profiles in tadpole larvae of Ciona intestinalis. , 2002, Developmental biology.

[41]  I. Meinertzhagen,et al.  Development of the central nervous system of the larva of the ascidian, Ciona intestinalis L. I. The early lineages of the neural plate. , 1988, Developmental biology.

[42]  F. Conlon,et al.  T‐box genes in early embryogenesis , 2004, Developmental dynamics : an official publication of the American Association of Anatomists.

[43]  H. Nishida,et al.  Ascidian embryonic development: An emerging model system for the study of cell fate specification in chordates , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[44]  N. Satoh,et al.  Systematic analysis of embryonic expression profiles of zinc finger genes in Ciona intestinalis. , 2006, Developmental biology.

[45]  C. Sardet,et al.  From oocyte to 16‐cell stage: Cytoplasmic and cortical reorganizations that pattern the ascidian embryo , 2007, Developmental dynamics : an official publication of the American Association of Anatomists.

[46]  Itai Yanai,et al.  Developmental milestones punctuate gene expression in the Caenorhabditis embryo. , 2012, Developmental cell.

[47]  J T Bonner,et al.  PERSPECTIVE: THE SIZE‐COMPLEXITY RULE , 2004, Evolution; international journal of organic evolution.

[48]  I. Salazar-Ciudad,et al.  How complexity increases in development: An analysis of the spatial-temporal dynamics of 1218 genes in Drosophila melanogaster. , 2015, Developmental biology.

[49]  Arne Ø. Mooers,et al.  Size and complexity among multicellular organisms , 1997 .

[50]  Johannes Jaeger,et al.  Cellular and Molecular Life Sciences REVIEW The gap gene network , 2022 .

[51]  Leif Kobbelt,et al.  Subdivision scheme tuning around extraordinary vertices , 2004, Comput. Aided Geom. Des..

[52]  P. Lemaire,et al.  A Quantitative Approach to the Study of Cell Shapes and Interactions during Early Chordate Embryogenesis , 2006, Current Biology.

[53]  R. Shackleton.  A Quantitative Approach , 2005 .

[54]  N. Satoh,et al.  Ci-Tbx6b and Ci-Tbx6c are key mediators of the maternal effect gene Ci-macho1 in muscle cell differentiation in Ciona intestinalis embryos. , 2005, Developmental biology.

[55]  Alicia N. Schep,et al.  A Comparative Analysis of Transcription Factor Expression during Metazoan Embryonic Development , 2013, PloS one.

[56]  Y. Satou,et al.  Transcriptome dynamics in early embryos of the ascidian, Ciona intestinalis. , 2013, Developmental biology.

[57]  Y. Kohara,et al.  Gene expression profiles in young adult Ciona intestinalis , 2002, Development Genes and Evolution.

[58]  Paul Richardson,et al.  The Draft Genome of Ciona intestinalis: Insights into Chordate and Vertebrate Origins , 2002, Science.

[59]  T. Hughes,et al.  Early evolution of the T-box transcription factor family , 2013, Proceedings of the National Academy of Sciences.

[60]  Kotaro Oka,et al.  Three-dimensional anatomy of the Ciona intestinalis tailbud embryo at single-cell resolution. , 2012, Developmental biology.

[61]  K. Hotta,et al.  Brachyury downstream notochord differentiation in the ascidian embryo. , 1999, Genes & development.

[62]  S. Carroll.  Chance and necessity: the evolution of morphological complexity and diversity , 2001, Nature.