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Balancing competing effects of tissue growth and cytoskeletal regulation during Drosophila wing disc development
The authors integrate computational and quantitative approaches to elucidate how organ shape arises through the interplay between multiple growth pathways through regulation of both proliferation and the cytoskeleton.
- Nilay Kumar
- , Jennifer Rangel Ambriz
- & Mark Alber
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| Open Access
Temporospatial hierarchy and allele-specific expression of zygotic genome activation revealed by distant interspecific urochordate hybrids
Wei et al. report a unique interspecific ascidian hybrid system and single-cell RNA sequencing to reveal the temporal hierarchy, spatial heterogeneity, and allele-specific expression of zygotic genome activation in urochordates.
- Jiankai Wei
- , Wei Zhang
- & Bo Dong
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| Open Access
Dynamic enhancer landscapes in human craniofacial development
Rajderkar et al. provide a genome-wide compendium of transcriptional enhancers active in human craniofacial development, along with single-cell resources for studies of mammalian craniofacial morphogenesis.
- Sudha Sunil Rajderkar
- , Kitt Paraiso
- & Axel Visel
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A GREB1-steroid receptor feedforward mechanism governs differential GREB1 action in endometrial function and endometriosis
The endometrium is activated by the pregnancy hormones estrogen and progesterone to facilitate embryo implantation, and errors in endometrial responsiveness can lead to reduced fertility or endometriosis. Here they show that GREB1 interacts with hormone receptors in the endometrium, leading to normal or pathological consequences depending on the hormones involved.
- Sangappa B. Chadchan
- , Pooja Popli
- & Ramakrishna Kommagani
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Regulation of long-range BMP gradients and embryonic polarity by propagation of local calcium-firing activity
Identical twins from a single embryo are formed in multiple species, albeit rarely. It is not clear how such twinning is suppressed during early development. Here they show that calcium signalling activity is propagated through the extraembryonic tissue to prevent ectopic primitive streak formation during gastrulation.
- Hyung Chul Lee
- , Nidia M. M. Oliveira
- & Claudio D. Stern
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R-Spondin 2 governs Xenopus left-right body axis formation by establishing an FGF signaling gradient
Left-right (LR) body asymmetry is established by leftward flow in the LR organizer. Here, the authors show in Xenopus that R-Spondin 2 acts as an FGF receptor antagonist that produces a right-to-left FGF signaling gradient in response to flow to break LR symmetry.
- Hyeyoon Lee
- , Celine Marie Camuto
- & Christof Niehrs
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Ran-GTP assembles a specialized spindle structure for accurate chromosome segregation in medaka early embryos
Mitotic spindle assembles in each blastomere to segregate duplicated chromosomes during cleavage of the fertilized egg. Here, the authors establish functional assays in fish embryos and find that Ran-GTP assembles a microtubule network at the metaphase spindle center that is essential for chromosome segregation.
- Ai Kiyomitsu
- , Toshiya Nishimura
- & Tomomi Kiyomitsu
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| Open Access
Single-cell multiomics decodes regulatory programs for mouse secondary palate development
Development of the secondary palate is a complex process. Here, the authors profile mouse palatogenesis through single-cell multiome sequencing, revealing dynamic gene regulation across embryonic days (E) 12.5, E13.5, E14.0, and E14.5.
- Fangfang Yan
- , Akiko Suzuki
- & Zhongming Zhao
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| Open Access
LinRace: cell division history reconstruction of single cells using paired lineage barcode and gene expression data
Inferring lineage trees while incorporating gene expressions and lineage barcodes is a challenging task. Here, authors present LinRace, which infers improved cell lineage trees and ancestral cell states using the proposed asymmetric division model.
- Xinhai Pan
- , Hechen Li
- & Xiuwei Zhang
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| Open Access
Puckered and JNK signaling in pioneer neurons coordinates the motor activity of the Drosophila embryo
How the stereotypical architecture of the nervous system is generated, and how this underlies function, is not well understood. Here, the authors show that JNK signaling in Drosophila pioneer neurons directs its structural organization, required for motor coordination.
- Katerina Karkali
- , Samuel W. Vernon
- & Enrique Martín-Blanco
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| Open Access
An oocyte meiotic midbody cap is required for developmental competence in mice
Midbodies form during cell division and play roles in cell function and fate. Here, the authors show that the meiotic midbody in mouse oocytes has a specialized cap structure required to retain nascent proteins in eggs and for full developmental competence.
- Gyu Ik Jung
- , Daniela Londoño-Vásquez
- & Karen Schindler
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| Open Access
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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| 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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Cell diversity and plasticity during atrioventricular heart valve EMTs
Lotto et al. delineate cell diversity and mechanisms during heart valve development using scRNA-seq. They identify distinct cell types and states, the emergence of epithelial-mesenchymal plasticity, and cell interactions that may govern this process.
- Jeremy Lotto
- , Rebecca Cullum
- & Pamela A. Hoodless
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| Open Access
Coordination of alternative splicing and alternative polyadenylation revealed by targeted long read sequencing
In this study using a targeted long read RNA sequencing approach called PL-Seq, the authors uncover coordination of alternative splicing and alternative polyadenylation within individual genes in Drosophila melanogaster.
- Zhiping Zhang
- , Bongmin Bae
- & Pedro Miura
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| Open Access
Placental growth factor exerts a dual function for cardiomyogenesis and vasculogenesis during heart development
Growth factors play key roles during heart development. Here they show that PLGF has both autocrine and paracrine roles during cardiomyogenesis and vasculogenesis, suggesting it may have therapeutic potential for heart disease.
- Nevin Witman
- , Chikai Zhou
- & Makoto Sahara
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| Open Access
Deciphering early human pancreas development at the single-cell level
Here, the authors revealed molecular heterogeneity, developmental trajectory and regulatory network of early human pancreas development, and depict the whole progression of pancreatic organogenesis during the first trimester at the single-cell level.
- Zhuo Ma
- , Xiaofei Zhang
- & Tao Xu
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| Open Access
Stepwise modifications of transcriptional hubs link pioneer factor activity to a burst of transcription
Eukaryotic transcription involves the formation of subnuclear hubs that enrich transcriptional machinery. Here the authors show that the hubs undergo stepwise modifications to fuel a burst of transcription rather than having a stable composition.
- Chun-Yi Cho
- & Patrick H. O’Farrell
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| Open Access
A ubiquitin-based effector-to-inhibitor switch coordinates early brain, craniofacial, and skin development
The molecular mechanisms ensuring early face, brain, and skin formation are unclear. Here, the authors uncover a posttranslational pathway that controls cytoskeletal signaling circuits to coordinate ectodermal patterning and neurulation.
- Anthony J. Asmar
- , Shaun R. Abrams
- & Achim Werner
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| Open Access
Plakoglobin is a mechanoresponsive regulator of naive pluripotency
The mechanical microenvironment influences stem cell pluripotency. Here, the authors culture stem cells in microgels with controlled volumetric confinement and identify Plakoglobin as a mechanoresponsive regulator of pluripotency in mouse and human.
- Timo N. Kohler
- , Joachim De Jonghe
- & Florian Hollfelder
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Selective binding of retrotransposons by ZFP352 facilitates the timely dissolution of totipotency network
During zygotic genome activation the embryo must re-wire the regulatory network that sustains totipotency earlier during development. Here they identify ZFP352 as an essential factor that targets retrotransposon families to facilitate dissolution of the totipotency network and enable ZGA.
- Zhengyi Li
- , Haiyan Xu
- & Hongqing Liang
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| Open Access
Apicobasal RNA asymmetries regulate cell fate in the early mouse embryo
How do cells of the preimplantation mouse embryo make decisions? Here the authors discovered that the spatial sorting of mRNAs, tRNA, rRNAs and organelles lead to localized translation, conducive for cell fate allocation and embryonic development.
- Azelle Hawdon
- , Niall D. Geoghegan
- & Jennifer Zenker
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| Open Access
The nuclear lamina couples mechanical forces to cell fate in the preimplantation embryo via actin organization
Contractile forces are key to sorting the embryonic inner cell mass from the extraembryonic trophectoderm. Here they show that Lamin-A links changes in mechanical forces to cell fate specification, enabling Yap-Cdx2 signaling in outer, but not inner cells.
- Robin M. Skory
- , Adam A. Moverley
- & Nicolas Plachta
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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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| Open Access
Molecular mechanisms of tubulogenesis revealed in the sea star hydro-vascular organ
Understanding how cells organize into organs is a key effort in developmental biology. Here the authors introduce the sea star hydrovascular organ as a genetically tractable system to understand the contribution of cell migration and signaling pathways in tubulogenesis.
- Margherita Perillo
- , S. Zachary Swartz
- & Gary M. Wessel
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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
Defects in placental syncytiotrophoblast cells are a common cause of developmental heart disease
Placental dysfunction can affect heart development, but the prevalence of this causality has not been well established. Here, the authors use mouse genetic tools to show that the placenta may constitute a significant source of congenital heart defects.
- Bethany N. Radford
- , Xiang Zhao
- & Myriam Hemberger
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| Open Access
Mechanisms and function of de novo DNA methylation in placental development reveals an essential role for DNMT3B
DNA methylation is a repressive modification that is essential for development. Here the authors reveal a critical role for DNA methylation in placental development during pregnancy. Failure to properly establish placental DNA methylation patterns compromises not only placental function, but embryo survival.
- Simon Andrews
- , Christel Krueger
- & Courtney W. Hanna
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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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Wnt4 and ephrinB2 instruct apical constriction via Dishevelled and non-canonical signaling
Apical constriction is known to be critical for neural tube closure, but the signals that induce this process have not been fully characterized. Here Yoon et al. identify a signaling complex that instructs actomyosin contractions during apical constriction and show that it is required for neural tube closure.
- Jaeho Yoon
- , Jian Sun
- & Ira O. Daar
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| Open Access
scm6A-seq reveals single-cell landscapes of the dynamic m6A during oocyte maturation and early embryonic development
Modification of RNA with N6-methyladenosine can regulate RNA metabolism. Here they developed scm6A-seq to profile the methylome and transcriptome in single cells, and reveal the functions of m6A modification during oocyte maturation and early embryo development.
- Huan Yao
- , Chun-Chun Gao
- & Yun-Gui Yang
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| Open Access
In vivo clonal tracking reveals evidence of haemangioblast and haematomesoblast contribution to yolk sac haematopoiesis
The lineage relationship between blood and endothelial cells has been difficult to examine due to the multiphasic timing of hematopoiesis in the embryo. Here the authors use using in vivo barcoding technology to assess cell ancestry and show that blood and endothelial cells emerge through common (haemangioblast) or separate (mesenchymoangioblasts and haematomesoblasts) progenitors in the yolk sac.
- C. Biben
- , T. S. Weber
- & S. Taoudi
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| 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
Human multilineage pro-epicardium/foregut organoids support the development of an epicardium/myocardium organoid
Stem cell models of organogenesis are a valuable tool for the study of human development, but often lack the context of tissue-tissue interaction. Here they generate human multi-lineage organoids comprising pro-epicardium, septum transversum, and liver bud, which they co-culture with heart organoids to generate a physiologically relevant model of organogenesis.
- Mariana A. Branco
- , Tiago P. Dias
- & Maria Margarida Diogo
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| Open Access
A Wolbachia factor for male killing in lepidopteran insects
Bacterial symbionts, such as Wolbachia species, can manipulate the sexual development and reproduction of their insect hosts. Here, the authors identify a Wolbachia protein that interacts with a host masculinization factor and leads to male killing in lepidopteran insects.
- Susumu Katsuma
- , Kanako Hirota
- & Takashi Kiuchi
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| Open Access
Translation regulatory factor BZW1 regulates preimplantation embryo development and compaction by restricting global non-AUG Initiation
It is unclear how translational efficiency and codon stringency affect zygotic genome activation and early embryonic development. Here they show that the zygotic gene BZW1 increases start codon stringency, which is important for preimplantation development.
- Jue Zhang
- , Shuai-Bo Pi
- & Heng-Yu Fan
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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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| 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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| Open Access
The TFEB-TGIF1 axis regulates EMT in mouse epicardial cells
Epithelial-mesenchymal transition (EMT) is a complex process involved in organogenesis. Here, the authors show that the transcription factor EB (TFEB) regulates EMT in epicardium during heart development by tuning sensitivity to TGFβ signaling.
- Elena Astanina
- , Gabriella Doronzo
- & Federico Bussolino
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| Open Access
Histone H3K36me2 and H3K36me3 form a chromatin platform essential for DNMT3A-dependent DNA methylation in mouse oocytes
DNMT3A is known to methylate DNA at histone H3 lysine 36 (H3K36me3)-marked transcriptionally active regions in mouse oocytes. Here the authors show that DNMT3A is also guided by H3K36me2 to methylate broad domains in genic and intergenic loci, as well as on the X chromosome. These two histone marks together comprise the minimal chromatin signature for global DNA methylation in mouse oocytes.
- Seiichi Yano
- , Takashi Ishiuchi
- & Hiroyuki Sasaki
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| 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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| Open Access
A hexa-species transcriptome atlas of mammalian embryogenesis delineates metabolic regulation across three different implantation modes
Mammalian embryogenesis relies on glycolysis and oxidative phosphorylation, but understanding of the dynamics of metabolic regulation in the postimplantation embryo in vivo remains elusive. Here the authors compile single-cell embryo profiling data in six mammalian species and reveal a conserved metabolic programme despite different implantation modes.
- Anna Malkowska
- , Christopher Penfold
- & Thorsten E. Boroviak
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| Open Access
Serotonin limits generation of chromaffin cells during adrenal organ development
Adrenal glands are major organs regulating stress response., Melnikova et al., show that local release of serotonin limits adrenalin-producing cell number during rodent development, a mechanism which has implications for neuroblastoma development and stress-related maternal effects transmitted to progeny.
- Polina Kameneva
- , Victoria I. Melnikova
- & Igor Adameyko
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| Open Access
CNPY4 inhibits the Hedgehog pathway by modulating membrane sterol lipids
Although lipids are known to affect Hedgehog (Hh) signalling, the underlying mechanisms remain unclear. Here, the authors show that Canopy4 regulates membrane sterol lipid levels, with knockout mouse embryos exhibiting digit number changes and other Hh signalling-related developmental defects.
- Megan Lo
- , Amnon Sharir
- & Ophir D. Klein
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| Open Access
ERK1/2 is an ancestral organising signal in spiral cleavage
How invertebrates with spiral cleavage establish their body plans is unclear. Here the authors show that, like molluscs, a basal annelid uses ERK1/2 to instruct body patterning, suggesting that this is a deep ancestral trait in animal embryogenesis.
- Océane Seudre
- , Allan M. Carrillo-Baltodano
- & José M. Martín-Durán
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| Open Access
Vasa nucleates asymmetric translation along the mitotic spindle during unequal cell divisions
Association of mRNA translation with the mitotic spindle is thought to be involved in localized production of cell fate determinants. Here, the authors show Vasa facilitates asymmetric translation, which contributes to differential regulation during sea urchin embryogenesis.
- Ana Fernandez-Nicolas
- , Alicia Uchida
- & Mamiko Yajima
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| Open Access
Dynamic FMR1 granule phase switch instructed by m6A modification contributes to maternal RNA decay
Maternal RNA degradation is critical for embryogenesis and is tightly controlled by maternal RNA-binding proteins. Here the authors show that a subset of m6A-modified mRNAs regulates the dynamics of RNA-granules, thus contributes to maternal mRNA decay.
- Guoqiang Zhang
- , Yongru Xu
- & Dahua Chen
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Article
| 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
Cell-type-specific mRNA transcription and degradation kinetics in zebrafish embryogenesis from metabolically labeled single-cell RNA-seq