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| Open AccessAlveolar cell fate selection and lifelong maintenance of AT2 cells by FGF signaling
Here the authors show that FGF signaling initiates alveolus development in mouse lung by inducing AT2 fate and a secondary signal for AT1 fate, and continuously maintains AT2 cells throughout life. FGF inhibition triggers immediate AT2 apoptosis and compensatory regeneration.
- Douglas G. Brownfield
- , Alex Diaz de Arce
- & Mark A. Krasnow
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Article
| Open AccessBiological effects of the loss of homochirality in a multicellular organism
Active regulation of chirality, or handedness, is crucial for life. Here, the authors describe assays to characterise proteome chirality in vivo and show that errors degrade enzyme activity triggering tumour formation and reduced lifespan.
- Agnes Banreti
- , Shayon Bhattacharya
- & Stéphane Noselli
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| Open AccessPatterned mechanical feedback establishes a global myosin gradient
How does DNA encode shape? Here, via in toto light sheet microscopy and optogenetic control of cellular forces, the authors show that spatially patterned mechanical feedback loops establish the cytoskeletal patterns driving axis elongation tissue flow in Drosophila.
- Hannah J. Gustafson
- , Nikolas Claussen
- & Sebastian J. Streichan
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| Open AccessMulticiliated cells use filopodia to probe tissue mechanics during epithelial integration in vivo
Cell integration is a critical process in shaping complex tissues. Ventura and Amiri et al. reveal how multiciliated cells exert forces using filopodia to probe and remodel the neighboring cells, facilitating the formation of a susceptible environment for their integration in vivo.
- Guilherme Ventura
- , Aboutaleb Amiri
- & Jakub Sedzinski
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| Open AccessEya-controlled affinity between cell lineages drives tissue self-organization during Drosophila oogenesis
Oogenesis depends on close interaction between germ cells and the surrounding somatic niche. Here the authors demonstrate that Eya controls bilateral affinity at the germline-soma interface to generate self-organizing inter-lineage units that ensure oocyte maturation.
- Vanessa Weichselberger
- , Patrick Dondl
- & Anne-Kathrin Classen
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| Open AccessEndothelial cell cycle state determines propensity for arterial-venous fate
During blood vessel development, endothelial cells become specified toward arterial or venous fates. Chavkin et al find that distinct endothelial cell cycle states provide windows of opportunity for the molecular induction of arterial or venous fate.
- Nicholas W. Chavkin
- , Gael Genet
- & Karen K. Hirschi
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Article
| Open AccessThe transcription factor Zfh1 acts as a wing-morph switch in planthoppers
The molecular mechanisms underlying wing polyphenism remain poorly understood. Here the authors use plant hoppers to show that the development of long and short wing morphs is balanced by the relative activities of the Zfh1-FoxO and insulin signaling cascades.
- Jin-Li Zhang
- , Sun-Jie Chen
- & Hai-Jun Xu
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Article
| Open AccessPredictive model for cytoneme guidance in Hedgehog signaling based on Ihog- Glypicans interaction
Cytonemes are specialized filopodia-like structures known to be involved in signal transduction. Here they propose a new predictive model for cytoneme guidance in Hedgehog signaling, which is based on Ihog, Dally, and Dlp protein levels.
- Adrián Aguirre-Tamaral
- , Manuel Cambón
- & Isabel Guerrero
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| Open AccessLive 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 AccessOptogenetic control of apical constriction induces synthetic morphogenesis in mammalian tissues
Apical constriction is a force-generating process required during embryonic development; there is a lack of tools to manipulate 3D shapes of mammalian tissues. Here the authors report the optogenetic method, OptoShroom3, to achieve fast spatiotemporal control of apical constriction in mammalian epithelia.
- Guillermo Martínez-Ara
- , Núria Taberner
- & Miki Ebisuya
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| Open AccessSpatiotemporal dynamics of self-organized branching in pancreas-derived organoids
Pancreatic ductal adenocarcinomas (PDAC) exhibit complex morphologies challenging to capture in organoid models. Here, the authors develop PDAC organoids that can recreate branched structures and, with the use of a minimal mathematical model, shed light to pathways and processes directing the dynamics of self-organization and branching morphogenesis.
- S. Randriamanantsoa
- , A. Papargyriou
- & A. R. Bausch
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Article
| Open AccessSpecificity of the Hox member Deformed is determined by transcription factor levels and binding site affinities
Despite the central role of Hox genes in controlling morphogenesis, the DNA binding of different Hox members is relatively similar. Here they show that specificity of Hox member Dfd relies on a precise balance of transcription factors and binding site affinities.
- Pedro B. Pinto
- , Katrin Domsch
- & Ingrid Lohmann
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| Open AccessAn interplay between cellular growth and atypical fusion defines morphogenesis of a modular glial niche in Drosophila
Little is known of how the architectural complexity of the neural stem cell niche is achieved. Rujano et al. show that the morphogenesis of a glial niche in Drosophila involves complex proliferative strategies and atypical cell–cell fusion.
- Maria Alexandra Rujano
- , David Briand
- & Pauline Spéder
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| Open AccessSpatiotemporal single-cell regulatory atlas reveals neural crest lineage diversification and cellular function during tooth morphogenesis
The mechanisms that govern cell fate decisions of postmigratory cranial neural crest cells remain largely unknown. Here the authors present a spatiotemporal single-cell regulatory atlas tracking these cells’ dental lineage diversification.
- Junjun Jing
- , Jifan Feng
- & Yang Chai
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| Open AccessSynaptotagmin-13 orchestrates pancreatic endocrine cell egression and islet morphogenesis
How pancreatic islets of Langerhans are built during development is incompletely understood. Here the authors find that Synaptotagmin-13 mediates remodeling of cell-matrix adhesion to regulate endocrine cell egression and islet morphogenesis.
- Mostafa Bakhti
- , Aimée Bastidas-Ponce
- & Heiko Lickert
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| Open AccessDynamic enlargement and mobilization of lipid droplets in pluripotent cells coordinate morphogenesis during mouse peri-implantation development
Prior to its implantation into the uterus, the mammalian embryo stores substantial lipids. Here the authors unveil how lipid storage and morphogenesis of pluripotent stem cells are fundamentally connected during peri-implantation development.
- King Hang Tommy Mau
- , Donja Karimlou
- & Véronique Azuara
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Article
| Open AccessMicrotubule disassembly by caspases is an important rate-limiting step of cell extrusion
Using the Drosophila pupal notum, the authors demonstrate that the disassembly of microtubules by effector caspases initiate cell extrusion independently of actomyosin regulation, thus providing insights into how caspases orchestrate dying epithelial cell expulsion.
- Alexis Villars
- , Alexis Matamoro-Vidal
- & Romain Levayer
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| Open AccessInhibition of negative feedback for persistent epithelial cell–cell junction contraction by p21-activated kinase 3
Actin and myosin operate at cell–cell junctions during junctional shortening. Here the authors show that prolonged actomyosin contractility can compromise junctional shortening, and that Pak3 is required for attenuation of abnormal active protrusive structure and thus keeps junction contraction, appropriate E-cadherin distribution, and junction shortening in Drosophila.
- Hiroyuki Uechi
- , Kazuki Fukushima
- & Erina Kuranaga
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| Open AccessGPI-anchored FGF directs cytoneme-mediated bidirectional contacts to regulate its tissue-specific dispersion
Cytonemes are signaling filopodia that mediate target-specific long-distance communications of signals like FGFs. Du et al. show that a Drosophila FGF is anchored to the FGF-producing cell surface, inhibiting free FGF secretion and activating contact-dependent bidirectional FGF-FGFR interactions, controlling target-specific cytoneme contacts and contact-dependent FGF release.
- Lijuan Du
- , Alex Sohr
- & Sougata Roy
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| Open AccessEmbryo-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 AccessKidney epithelial cells are active mechano-biological fluid pumps
How mechanical forces drive fluid transport in the kidney remains unclear. Here, the authors use a microfluidic platform to show that kidney epithelial cells generate hydraulic pressure gradients across the epithelium, and that the fluid flux is from apical to basal for normal cells, and inverted in autosomal dominant polycystic kidney disease cells.
- Mohammad Ikbal Choudhury
- , Yizeng Li
- & Sean X. Sun
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| Open AccessPeriodic formation of epithelial somites from human pluripotent stem cells
Somitogenesis has been well characterized in model organisms, resulting in detailed description of the somite segmentation clock. Here they generate somitogenic organoids from human pluripotent stem cells that recapitulate somitogenesis, periodic segmentation, and proper polarity.
- Marina Sanaki-Matsumiya
- , Mitsuhiro Matsuda
- & Miki Ebisuya
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| Open AccessTig1 regulates proximo-distal identity during salamander limb regeneration
The mechanisms by which cells determine their position within the 3D space are poorly understood. Research in salamanders offers fresh insights into this question, uncovering Tig1 as a central determinant of proximo-distal identity in regeneration.
- Catarina R. Oliveira
- , Dunja Knapp
- & Maximina H. Yun
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| Open AccessA hemimetabolous wing development suggests the wing origin from lateral tergum of a wingless ancestor
Here, the authors investigate wing development in cricket and find support for evolution of the novel insect wing from the pre-existing dorsal body wall of a wingless ancestor by activation of an evolutionarily conserved growth mechanism.
- Takahiro Ohde
- , Taro Mito
- & Teruyuki Niimi
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| Open AccessASPP2 maintains the integrity of mechanically stressed pseudostratified epithelia during morphogenesis
The early embryo maintains its structure in the face of large mechanical stresses during morphogenesis. Here they show that ASPP2 acts to preserve epithelial integrity in regions of high apical tension during early development.
- Christophe Royer
- , Elizabeth Sandham
- & Shankar Srinivas
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| Open AccessMesenchymal-epithelial crosstalk shapes intestinal regionalisation via Wnt and Shh signalling
The small intestine forms via crosstalk between epithelial and mesenchymal cell compartments. Here, the authors show that a gradient of Wnt signalling along the anterior-posterior axis regulates Sonic Hedgehog which is required for correct formation and regionalization of the small intestine.
- Martti Maimets
- , Marianne Terndrup Pedersen
- & Kim B. Jensen
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| Open AccessTissue fluidity mediated by adherens junction dynamics promotes planar cell polarity-driven ommatidial rotation
Ommatidial rotation in the Drosophila eye is a regulated process and a Planar Cell Polarity (PCP) cell motility model. Here, the authors show that tissue fluidity via junctional remodeling, as regulated by the PCP effector kinase Nemo, is critical for this cell motility process.
- Nabila Founounou
- , Reza Farhadifar
- & Marek Mlodzik
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| Open AccessTheory of branching morphogenesis by local interactions and global guidance
Many organs and cells have complex tree-like morphologies, but how these patterns emerge during development from global guidance cues and local self-organization remains unclear. Here, the authors develop a theory for the influence of both factors and test it on neuronal branching data.
- Mehmet Can Uçar
- , Dmitrii Kamenev
- & Edouard Hannezo
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Article
| Open AccessHox genes regulate asexual reproductive behavior and tissue segmentation in adult animals
Hox genes are highly conserved and well-known for their role in segmental patterning during early development. Here, the authors identify an unreported role for Hox genes in the adult tissue patterning and fission behavior required for asexual reproduction in planarian flatworms.
- Christopher P. Arnold
- , Analí Migueles Lozano
- & Alejandro Sánchez Alvarado
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| Open AccessSmad4 controls signaling robustness and morphogenesis by differentially contributing to the Nodal and BMP pathways
The role of the transcriptional effector SMAD4 in vertebrate embryo development remains unresolved. Here the authors show that in the absence of Smad4, dorsal/ventral embryo patterning is disrupted due to the loss of BMP signaling, while Nodal signaling is maintained, but insufficient for optimal endoderm specification.
- Luca Guglielmi
- , Claire Heliot
- & Caroline S. Hill
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| Open AccessIntroducing dorsoventral patterning in adult regenerating lizard tails with gene-edited embryonic neural stem cells
Organisms with regenerative capacity typically regrow organs with correct axial patterning, however, regrown lizard tails lack this feature. Here the authors used neural stem cells to induce patterning in regenerating lizard tails and rescued normal skeletal morphology.
- Thomas P. Lozito
- , Ricardo Londono
- & Megan L. Hudnall
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Article
| Open AccessCHARGE syndrome protein CHD7 regulates epigenomic activation of enhancers in granule cell precursors and gyrification of the cerebellum
CHARGE syndrome that affects cerebellar development can be caused by haploinsufficiency of the chromatin remodeling enzyme CHD7; however the precise role of CHD7 remains unknown. Here the authors show CHD7 promotes chromatin accessibility and enhancer activity in granule cell precursors and regulates morphogenesis of the cerebellar cortex, where loss of CHD7 triggers cerebellar polymicrogyria.
- Naveen C. Reddy
- , Shahriyar P. Majidi
- & Harrison W. Gabel
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| Open AccessReconstructing aspects of human embryogenesis with pluripotent stem cells
Human early development remains largely inaccessible, owing to technical and ethical limitations of working with natural embryos. Here the authors assess the extent to which human expanded pluripotent stem cells can specify distinct cell lineages and capture aspects of early human embryogenesis.
- Berna Sozen
- , Victoria Jorgensen
- & Magdalena Zernicka-Goetz
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| Open AccessApplication of 3D MAPs pipeline identifies the morphological sequence chondrocytes undergo and the regulatory role of GDF5 in this process
Inability to image large numbers of growth plate chondrocytes while retaining their spatial context during analysis has hindered the study of bone development. Here, the authors present a pipeline called 3D MAPs and use it to uncover morphogenic behaviors and growth strategies in normal bones as well as aberrations in Gdf5 KO bones.
- Sarah Rubin
- , Ankit Agrawal
- & Elazar Zelzer
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| Open AccessFluid flow-induced left-right asymmetric decay of Dand5 mRNA in the mouse embryo requires a Bicc1-Ccr4 RNA degradation complex
Questioning what regulates left-right asymmetry breaking in the mouse node: the authors identify a 200 bp stretch of the Dand5 3’UTR where Bicc1 binds, and Cnot proteins downstream of calcium flow regulate the post-transcriptional regulation of Dand5 by Bicc1.
- Katsura Minegishi
- , Benjamin Rothé
- & Hiroshi Hamada
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| Open AccessThe steroid-hormone ecdysone coordinates parallel pupariation neuromotor and morphogenetic subprograms via epidermis-to-neuron Dilp8-Lgr3 signal induction
Pupariation in Drosophila is triggered by the steroid-hormone ecdysone and requires coordination between associated behavioral and body-reshaping motor subprograms. The authors show that coordination requires ecdysone-dependent Dilp8-Lgr3 signaling between the cuticle epidermis and interneurons.
- Fabiana Heredia
- , Yanel Volonté
- & Alisson M. Gontijo
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| Open AccessBAD regulates mammary gland morphogenesis by 4E-BP1-mediated control of localized translation in mouse and human models
Preventing phosphorylation of BAD (3SA) in mouse models and human cells inhibits mammary gland development, acting by disrupting 4E-BP1- mediated translation and affecting focal adhesion/protrusion stability, cell migration and ductal tubulogenesis.
- John Maringa Githaka
- , Namita Tripathi
- & Ing Swie Goping
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Article
| Open AccessEMX2-GPR156-Gαi reverses hair cell orientation in mechanosensory epithelia
Sensory hair cells develop an asymmetric architecture to restrict stimulus detection to a single axis. Here the authors identify GPR156 as directing a 180-degree reversal in hair cell orientation through Gαi, downstream of EMX2 in the mouse inner ear and zebrafish lateral line.
- Katie S. Kindt
- , Anil Akturk
- & Basile Tarchini
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Article
| Open AccessCell non-autonomy amplifies disruption of neurulation by mosaic Vangl2 deletion in mice
Mutations that cause tissue mosaicism have been identified in individuals with severe congenital defects. Here, the authors show that mosaic deletion of Vangl2 in the murine neuroepithlium causes spina bifida by preventing apical constriction via reduced myosin II and tubulin organisation.
- Gabriel L. Galea
- , Eirini Maniou
- & Andrew J. Copp
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| Open AccessA network-based framework for shape analysis enables accurate characterization of leaf epidermal cells
While cell shape is crucial for function and development of organisms, versatile frameworks for cell shape quantification, comparison, and classification remain underdeveloped. Here, the authors use a network-based framework for Arabidopsis leaf epidermal cell shape characterization and classification.
- Jacqueline Nowak
- , Ryan Christopher Eng
- & Zoran Nikoloski
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Article
| Open AccessDifferential cell adhesion implemented by Drosophila Toll corrects local distortions of the anterior-posterior compartment boundary
The differential adhesion hypothesis is proposed to play a role during epithelial tissue morphogenesis but it has remained unclear. Here, the authors identify the Toll-1 receptor as a differentially expressed adhesion molecule that maintains lineage restriction boundaries in the Drosophila epidermal epithelium.
- Norihiro Iijima
- , Katsuhiko Sato
- & Daiki Umetsu
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Article
| Open AccessEstablishment of a morphological atlas of the Caenorhabditis elegans embryo using deep-learning-based 4D segmentation
The systematic characterization of C. elegans morphology during development has yet to be performed. Here, the authors produce a 3D atlas of C. elegans morphology from 17 embryos and 54 developmental stages, using an automated pipeline, CShaper (combining segmentation of fluorescently labeled membranes with automated cell lineage tracing).
- Jianfeng Cao
- , Guoye Guan
- & Hong Yan
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| Open Accessβ-Pix-dependent cellular protrusions propel collective mesoderm migration in the mouse embryo
Mesodermal directional cell migration is needed to establish body plan but how this is regulated is unclear. Here, the authors show that loss of the guanine nucleotide exchange factor for Rac1 and Cdc42, β-Pix, at mouse gastrulation disrupts the orderly, collective anterior migration of mesoderm cells due to defective cell protrusions.
- Tatiana Omelchenko
- , Alan Hall
- & Kathryn V. Anderson
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Article
| Open AccessRegionalized 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 AccessFeeding-dependent tentacle development in the sea anemone Nematostella vectensis
How the developmental capacity of long-lived animals copes with fluctuations in the food supply is unclear. Here, the authors show using the sea anemone Nematostella vectensis that the crosstalk between Target of Rapamycin and fibroblast growth factor signalling in ring muscles links postembryonic tentacle patterning with food availability.
- Aissam Ikmi
- , Petrus J. Steenbergen
- & Matthew C. Gibson
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Article
| Open AccessIRSp53 controls plasma membrane shape and polarized transport at the nascent lumen in epithelial tubules
The I-BAR protein IRSp53 senses membrane curvature but its physiological role is unclear. Here, the authors show that during early lumen morphogenesis, IRSp53 controls the shape of the apical plasma membrane and polarized trafficking and ensures the correct epithelial tubular architecture and if deleted, affects renal tubules morphogenesis in various organisms.
- Sara Bisi
- , Stefano Marchesi
- & Andrea Disanza
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Article
| Open AccessUncovering mutation-specific morphogenic phenotypes and paracrine-mediated vessel dysfunction in a biomimetic vascularized mammary duct platform
In vitro models of the human mammary gland have struggled to mimic the 3D morphogenic processes that occur in vivo. Here the authors develop a 3D microfluidic platform of a vascularized human mammary duct that simulates diverse morphogenic transitions and paracrine crosstalk.
- Matthew L. Kutys
- , William J. Polacheck
- & Christopher S. Chen
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Article
| Open AccessTurning induced plasticity into refined adaptations during range expansion
Phenotypic robustness to environmental variation is seemingly at odds with evolvability. Here, the authors analyze carotenoid use and accommodation in feather development across a recent avian range expansion and show that cooption of a stress-buffering mechanism can reconcile robustness and evolvability.
- Ahva L. Potticary
- , Erin S. Morrison
- & Alexander V. Badyaev
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Article
| Open AccessEpithelial invagination by a vertical telescoping cell movement in mammalian salivary glands and teeth
Mechanisms that regulate epithelial bending mainly link to cell shape changes, for example, the formation of wedge shaped cells. Here, the authors identify a different cell behaviour in the salivary glands and teeth where initial invagination arises by a coordinated vertical cell movement.
- Jingjing Li
- , Andrew D. Economou
- & Jeremy B. A. Green