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Maintenance of pluripotency-like signature in the entire ectoderm leads to neural crest stem cell potential
How the neural crest gains its pluripotency-like stem cell potential is unclear. Here, the authors show that the entire post-gastrula ectoderm maintains expression of pluripotency genes, leading to the high stem cell capacity in the neural crest.
- Ceren Pajanoja
- , Jenny Hsin
- & Laura Kerosuo
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Article
| Open Access
Activator-blocker model of transcriptional regulation by pioneer-like factors
How gene expression timing is regulated during development remains a key area of research. Here they show that zebrafish genome activators Pou5f3 and Nanog block each other’s activity on the enhancers of differentiation genes, preventing their premature expression.
- Aileen Julia Riesle
- , Meijiang Gao
- & Daria Onichtchouk
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| Open Access
Time space and single-cell resolved tissue lineage trajectories and laterality of body plan at gastrulation
Gastrulation entails a series of events that are highly coordinated in space and time. Here they construct a spatiotemporal molecular atlas of lineage trajectories in the gastrulating mouse embryo by mapping single cells to spatial coordinates in the germ layers with reference to positional data in the transcriptome.
- Ran Wang
- , Xianfa Yang
- & Naihe Jing
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| Open Access
Serotonin signaling regulates actomyosin contractility during morphogenesis in evolutionarily divergent lineages
Serotonin signaling is well known for modulating animal behavior. Here the authors discovered it plays a developmental role in regulating actomyosin contractility driven cellular mechanics and tissue flows during gastrulation of insect and bird.
- Sanjay Karki
- , Mehdi Saadaoui
- & Thomas Lecuit
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| Open Access
Base editing-mediated one-step inactivation of the Dnmt gene family reveals critical roles of DNA methylation during mouse gastrulation
The role of DNA methylation in early embryo development has been difficult to determine due to the functional redundancy of DNA methyltransferases. Here they develop an efficient base editing system that enables one-step generation of Dnmt-null embryos and show that DNA methylation-related miRNA suppression may be involved in gastrulation.
- Qing Li
- , Jiansen Lu
- & Jinsong Li
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Article
| Open Access
A Yap-dependent mechanoregulatory program sustains cell migration for embryo axis assembly
YAP signaling has been established as a mechanotransductive pathway in multiple contexts, but its developmental roles are still being explored. Here they show that YAP signaling sustains intracellular tension to direct cell migration during embryonic axis assembly.
- Ana Sousa-Ortega
- , Javier Vázquez-Marín
- & Juan R. Martínez-Morales
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| Open Access
Intercellular exchange of Wnt ligands reduces cell population heterogeneity during embryogenesis
Neuromesodermal progenitor (NMP) cells produce and receive Wnt ligands. Here, the authors show that mutual intercellular exchange of Wnt ligands reduces heterogeneity between NMP cells and makes NMP populations robust to environmental stress.
- Yudai Hatakeyama
- , Nen Saito
- & Shinji Takada
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| Open Access
Epithelial disruption drives mesendoderm differentiation in human pluripotent stem cells by enabling TGF-β protein sensing
Fate specification in the mammalian epiblast rely on complex interactions between morphogens and tissue organization. Here, the authors highlight epithelial integrity as a key determinant of TGF-β activity and a mechanism guiding morphogen sensing and spatial cell fate change.
- Thomas Legier
- , Diane Rattier
- & Rosanna Dono
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Article
| Open Access
Primate-specific transposable elements shape transcriptional networks during human development
The human genome harbors more than 4.5 million transposable element (TE)-derived insertions, the result of recurrent waves of invasion and internal propagation. Here they show that TEs belonging to evolutionarily recent subfamilies go on to regulate later stages of human embryonic development, notably conditioning the expression of genes involved in gastrulation and early organogenesis.
- Julien Pontis
- , Cyril Pulver
- & Didier Trono
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| Open Access
Live imaging and conditional disruption of native PCP activity using endogenously tagged zebrafish sfGFP-Vangl2
Planar cell polarity (PCP) is critical for tissue-wide coordination and successful development. Here Jussila et al. generate a GFP-Vangl2 fusion for live imaging and discover a surprising directionality to the intercellular propagation of cell polarity, and ultimately link PCP defects with idiopathic scoliosis.
- Maria Jussila
- , Curtis W. Boswell
- & Brian Ciruna
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Article
| Open Access
Adar-mediated A-to-I editing is required for embryonic patterning and innate immune response regulation in zebrafish
Additional roles for A-to-I editing of RNA continue to be uncovered. Niescierowicz et al. report prevalent A-to-I editing in the zebrafish transcriptome, and the distinct maternal and zygotic functions of the editing enzyme Adar in embryonic patterning and in the regulation of innate immune response, respectively.
- Katarzyna Niescierowicz
- , Leszek Pryszcz
- & Cecilia Winata
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Article
| Open Access
G1/S restriction point coordinates phasic gene expression and cell differentiation
Somatic cells display phasic gene expression with compartmentalized gene expression during the cell cycle, while pluripotent cells lack phasic expression. Here, the authors describe a pathway linking microRNA regulation of the G1/S restriction point with phasic gene expression and cell differentiation during mammalian development.
- Brian DeVeale
- , Leqian Liu
- & Robert Blelloch
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Article
| Open Access
Embryo-scale epithelial buckling forms a propagating furrow that initiates gastrulation
Drosophila mesoderm invagination begins with the formation of a furrow. Here they show that a long-range mechanism, powered by actomyosin contraction between the embryo polar caps, works like a ‘cheese-cutter wire’ indenting the tissue surface and folding it into a propagating furrow.
- Julien Fierling
- , Alphy John
- & Matteo Rauzi
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| Open Access
Pluripotency factors determine gene expression repertoire at zygotic genome activation
Zygotic genome activation in zebrafish relies on pluripotency transcription factors Pou5f3 and Sox19b. Here the authors investigate how these factors interact in vivo by analyzing the changes in chromatin state and time-resolved transcription in Pou5f3 and Sox19b single and double mutant embryos.
- Meijiang Gao
- , Marina Veil
- & Daria Onichtchouk
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Article
| Open Access
Nodal is a short-range morphogen with activity that spreads through a relay mechanism in human gastruloids
Studying morphogen gradient formation and reception in mammalian development is challenging. Here, the authors show with human gastruloids that Nodal activity in live cells spreads via a relay mechanism with timing that is locally controlled by Lefty, which dictates mesoderm differentiation timing.
- Lizhong Liu
- , Anastasiia Nemashkalo
- & Aryeh Warmflash
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Article
| Open Access
Vangl2 promotes the formation of long cytonemes to enable distant Wnt/β-catenin signaling
Cytonemes are cellular projections known to transfer Wnt ligands between cells, but their regulation remains unclear. Here, the authors show that activation of the planar cell polarity protein Vangl2 generates long and branched cytonemes increasing paracrine Wnt/β-catenin signaling.
- Lucy Brunt
- , Gediminas Greicius
- & Steffen Scholpp
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| Open Access
Regionalized tissue fluidization is required for epithelial gap closure during insect gastrulation
The mechanics of embryonic tissue spreading over spherical eggs is not fully understood. Here, the authors show that during gastrulation in the red flour beetle, extraembryonic tissue epiboly is facilitated by local actomyosin-mediated fluidization of the tissue at the leading edge.
- Akanksha Jain
- , Vladimir Ulman
- & Anastasios Pavlopoulos
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Article
| Open Access
Multi-scale imaging and analysis identify pan-embryo cell dynamics of germlayer formation in zebrafish
The precise cell dynamics of early development have not yet been visualized. Here, the authors use custom 4-lens light sheet microscopy to image and analyze the dynamics of all three fluorescently labeled germlayers, yielding a comprehensive, pan-embryo description of early zebrafish gastrulation.
- Gopi Shah
- , Konstantin Thierbach
- & Jan Huisken
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| Open Access
Mouse embryo geometry drives formation of robust signaling gradients through receptor localization
How receptor localization affects morphogen gradient formation during embryonic development is unclear. Here, the authors study the relationship between the BMP gradient, receptor localization, and compartmentalized geometry in the early mouse embryo, using experimental data and computational simulation.
- Zhechun Zhang
- , Steven Zwick
- & Sharad Ramanathan
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| Open Access
Implantation initiation of self-assembled embryo-like structures generated using three types of mouse blastocyst-derived stem cells
The precise cellular patterning and decisions of early embryogenesis have been hard to mimic in vitro. Here, the authors culture murine embryonic and trophoblast stem cells together with extra-embryonic endoderm stem cells to form embryo-like structures (ETX-embryoids), which can initiate an implantation response.
- Shaopeng Zhang
- , Tianzhi Chen
- & Jianyong Han
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Article
| Open Access
Distinct contributions of tensile and shear stress on E-cadherin levels during morphogenesis
The effects of mechanical forces, generated by actomyosin contractility, on E-cadherin based cell adhesion are poorly characterized in vivo. Here, the authors report that normal stress increases E-cadherin levels, whereas shear stress reduces E-Cadherin levels, in the developing Drosophila embryo.
- Girish R. Kale
- , Xingbo Yang
- & Thomas Lecuit
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| Open Access
Guided morphogenesis through optogenetic activation of Rho signalling during early Drosophila embryogenesis
Optogenetics is opening the possibility to not only perturb morphogenesis, but also to guide it. Here, the authors use this technique to reconstruct epithelial folding in Drosophila embryos and study the relationship between strength of Rho activation, apical constrictions, and tissue invagination.
- Emiliano Izquierdo
- , Theresa Quinkler
- & Stefano De Renzis
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| Open Access
P53 and mTOR signalling determine fitness selection through cell competition during early mouse embryonic development
During embryo development, cell fitness determines survival but how this is regulated is unclear. Here, the authors show that in early embryonic development and stem cells exiting the naive state, cells sense the fitness of their neighbours and trigger p53 to repress mTOR to eliminate a third of cells.
- Sarah Bowling
- , Aida Di Gregorio
- & Tristan A. Rodríguez
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| Open Access
Gon4l regulates notochord boundary formation and cell polarity underlying axis extension by repressing adhesion genes
Anteroposterior axis extension during gastrulation is dynamically coordinated, but how this is regulated at a molecular level is unclear. Here, the authors show in zebrafish that the chromatin factor Gon4l, encoded by ugly duckling, coordinates axis extension by modulating EpCAM and Integrinα3b expression.
- Margot L. K. Williams
- , Atsushi Sawada
- & Lilianna Solnica-Krezel
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Article
| Open Access
Spatial regulation of contractility by Neuralized and Bearded during furrow invagination in Drosophila
In the Drosophila embryo, increased cortical contractility in ventral cells causes furrow formation and gastrulation. Here, the authors show that contractility is regulated by Neuralized (an E3 ubiquitin ligase) in ventral cells, and that inhibiting this process with Bearded in the ectoderm causes furrow invagination.
- Gantas Perez-Mockus
- , Khalil Mazouni
- & François Schweisguth
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Article
| Open Access
Leucine repeat adaptor protein 1 interacts with Dishevelled to regulate gastrulation cell movements in zebrafish
Gastrulation is an early morphogenic event driven by coordinated asymmetric/polarised cell movements. Here, the authors show in zebrafish that Lurap1, a protein that interacts with Dishevelled, regulates Wnt and planar cell polarity, coordinating centriole positioning during convergence and extension.
- Xiao-Ning Cheng
- , Ming Shao
- & De-Li Shi
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Article
| Open Access
Planar polarized Rab35 functions as an oscillatory ratchet during cell intercalation in the Drosophila epithelium
Various stages of tissue morphogenesis involve the contraction of epithelial surfaces. Here, the authors identify the Rab GTPase Rab35 as an essential component of this contractile process, which functions as a membrane ratchet to ensure unidirectional movement of intercalating cells.
- Cayla E. Jewett
- , Timothy E. Vanderleest
- & J. Todd Blankenship
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Article
| Open Access
Actomyosin meshwork mechanosensing enables tissue shape to orient cell force
Large-scale tissue reorganization requires the generation of directional tension, which requires orientation of the cytoskeleton. Here Chanetet al. alter tissue shape and tension in the Drosophilaembryo to show that geometric and mechanical constraints act as cues to orient the cytoskeleton and tension.
- Soline Chanet
- , Callie J. Miller
- & Adam C. Martin
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| Open Access
Foxa2 identifies a cardiac progenitor population with ventricular differentiation potential
The progenitor populations that contribute to the key cardiac lineages in a chamber-specific manner are unknown. Here, the authors identifyFoxa2+ progenitor population, which is specified at gastrulation, as contributing primarily to cardiovascular cells of both ventricles and the epicardium in mice.
- Evan Bardot
- , Damelys Calderon
- & Nicole C. Dubois
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| Open Access
Mechanotransductive cascade of Myo-II-dependent mesoderm and endoderm invaginations in embryo gastrulation
Mechanical signals regulate tissue differentiation but how this triggers downstream biochemical signals is unclear. Here, the authors place micro-magnets in theDrosophilaembryonic epithelia and show this triggers apical pulsations, in turn stabilizing Myosin-II, resulting in mesoderm invagination.
- Démosthène Mitrossilis
- , Jens-Christian Röper
- & Emmanuel Farge
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| Open Access
Embryo-scale tissue mechanics during Drosophila gastrulation movements
It is unclear how cell movements coordinate ventral furrow formation at the start of gastrulation in flies. Here, using multiview light-sheet microscopy and cell immobilization, Rauzi et al.observe differential epithelial cell movements, which contribute to the dynamics and timing of mesoderm internalization.
- Matteo Rauzi
- , Uros Krzic
- & Maria Leptin
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| Open Access
Organizer-derived Bmp2 is required for the formation of a correct Bmp activity gradient during embryonic development
The morphogen, Bmp, regulates differentiation of cell fates along the ventral to dorsal axis during vertebrate embryonic development. Here, Xue et al. show that Bmp2b produced by the organizer during early gastrulation in zebrafish embryos has a role in the establishment of an appropriate Bmp morphogen activity gradient and the correct dorsoventral patterning of the embryos.
- Yu Xue
- , Xiudeng Zheng
- & Anming Meng
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Bcl-wav and the mitochondrial calcium uniporter drive gastrula morphogenesis in zebrafish
Ca2+ is an intracellular messenger that has a critical role in zebrafish development. Here Prudent et al. show that during gastrulation, the newly identified Bcl-2 homologue, Bcl-wav and the mitochondrial calcium uniporter regulate cell migration by controlling mitochondrial Ca2+storage.
- Julien Prudent
- , Nikolay Popgeorgiev
- & Germain Gillet
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Ets2-dependent trophoblast signalling is required for gastrulation progression after primitive streak initiation
The transcription factor Ets2 is expressed in the extraembryonic ectoderm tropoblast during gastrulation. Here, the authors use Ets2 knock-out mice to show that Ets2 signalling is required for gastrulation, primitive streak elongation and development and the mesoderm epithelial-to-mesenchymal transition.
- Christiana Polydorou
- & Pantelis Georgiades
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Delivery of endosomes to lysosomes via microautophagy in the visceral endoderm of mouse embryos
Nutrients and growth factors initiate endocytotic processes in the embryonic endoderm that control embryonic patterning. Here, Kawamuraet al.show that the small GTP-binding protein rab7 controls a unique microautophagy-like process that is involved in endocytosis in the endoderm of mouse embryos.
- Nobuyuki Kawamura
- , Ge-Hong Sun-Wada
- & Yoh Wada
Regulation of long-range BMP gradients and embryonic polarity by propagation of local calcium-firing activity