{"title":"A conserved sequence that sparked the field of evo-devo","authors":"Leslie Pick, Kristen Au","doi":"10.1016/j.ydbio.2024.11.005","DOIUrl":"10.1016/j.ydbio.2024.11.005","url":null,"abstract":"<div><div>The discovery that homeotic genes in <em>Drosophila</em> are conserved and utilized for embryonic development throughout the animal kingdom, including humans, revolutionized the fields of developmental biology and evolutionary developmental biology (evo-devo). In a pair of back-to-back papers published in <em>Cell</em> in 1984, researchers at the Biozentrum in Basel, Switzerland, showed that the homeobox – previously identified as a sequence shared by homeotic genes in <em>Drosophila</em> – was also present in the genome of diverse animals. The first paper (McGinnis et al., 1984a) showed that genomes of both invertebrates and vertebrates contain sequences that cross-hybridized with <em>Drosophila</em> homeobox probes. The second paper (Carrasco et al., 1984) identified a cross-hybridizing sequence in the model system <em>Xenopus laevis</em>. They then isolated the first vertebrate homeobox-containing gene by cloning and sequencing of the corresponding genomic region. Finally, they showed that this gene (<em>AC1</em>, later renamed <em>HoxC6</em>) was expressed during embryonic development, the first evidence that developmentally expressed <em>Drosophila</em> genes could be used to isolate regulators of vertebrate embryonic development. These findings led to a flurry of activity in the evo-devo field, initially focused on isolating <em>Hox</em> genes across diverse species, and then expanding to isolation of other gene families based on <em>Drosophila</em> orthologs, an approach that continues today. This led to the notion of a conserved genetic toolkit for embryonic development, currently accepted, but unexpected at the time of its discovery. We attempt to provide some context for the sea-change in thinking that these discoveries brought about by referring to Jean Piaget's theories about the sequential acquisition of scientific knowledge.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"518 ","pages":"Pages 1-7"},"PeriodicalIF":2.5,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142643757","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Maternal and zygotic contributions to H3K4me1 chromatin marking during germ layer formation","authors":"Kitt D. Paraiso , Ira L. Blitz , Ken W.Y. Cho","doi":"10.1016/j.ydbio.2024.11.006","DOIUrl":"10.1016/j.ydbio.2024.11.006","url":null,"abstract":"<div><div>An early step in triploblastic embryo differentiation is the formation of the three germ layers. Maternal pioneer transcription factors (TFs) bind to embryonic enhancers before zygotic genome activation, initiating germ layer specification. While maternal TFs' role in establishing epigenetic marks is known, how early pluripotent cells gain spatially restricted epigenetic identities remains unclear. We show that by the early gastrula stage, H3K4me1-marked regions become distinct in each germ layer, with certain chromatin regions forming high density H3K4me1 marked regions (HDRs). Genes associated with these HDRs are more robustly expressed compared to those associated with low density H3K4me1 marked regions (LDRs) in the genome. This process is driven by the sequential actions of maternal and zygotic factors. Knockdown of key maternal endodermal TFs (Otx1, Vegt and Foxh1) leads to a loss of endodermal H3K4me1 marks in endoderm, with a concurrent emergence of ectodermal and mesodermal marks, indicating a shift in chromatin state. This work highlights the importance of coordinated activities of maternal and zygotic TFs in defining the regionally-resolved and dynamic process of chromatin modification conferred by H3K4me1 in the early <em>Xenopus</em> embryo.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"518 ","pages":"Pages 8-19"},"PeriodicalIF":2.5,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142643762","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The establishment of the anther somatic niche with single-cell sequencing","authors":"D. Blaine Marchant , Virginia Walbot","doi":"10.1016/j.ydbio.2024.11.004","DOIUrl":"10.1016/j.ydbio.2024.11.004","url":null,"abstract":"<div><div>The anther is the developmental housing of pollen and therefore the male gametes of flowering plants. The meiotic cells from which pollen are derived must differentiate <em>de novo</em> from somatic anther cells and synchronously develop with the rest of the anther. Anthropogenic control over another development has become crucial for global agriculture so as to maintain inbred lines and generate hybrid seeds of many crops. Understanding the genes that underlie the proper differentiation, developmental landmarks, and functions of each anther cell type is thus fundamental to both basic and applied plant sciences. We investigated the development of the somatic niche of the maize (<em>Zea mays</em>) anther using single-cell RNA-seq (scRNA-seq). Extensive background knowledge on the birth then pace and pattern of cell division of the maize anther cell types and published examples of cell-type gene expression from <em>in situ</em> hybridization allowed us to identify the primary cell types within the anther lobe, as well as the connective cells between the four lobes. We established the developmental trajectories of somatic cell types from pre-meiosis to post-meiosis, identified putative marker genes for the somatic cell types that previously lacked any known specific functions, and addressed the possibility that tapetal cells sequentially differentiate. This comprehensive scRNA-seq dataset of the somatic niche of the maize anther will serve as a baseline for future analyses investigating male-sterile genotypes and the impact of environmental conditions on male fertility in flowering plants.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"518 ","pages":"Pages 37-47"},"PeriodicalIF":2.5,"publicationDate":"2024-11-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142638665","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Graham J. Burton , Eric Jauniaux , Tereza Cindrova-Davies , Margherita Y. Turco
{"title":"The human gestational sac as a choriovitelline placenta during early pregnancy; the secondary yolk sac and organoid models","authors":"Graham J. Burton , Eric Jauniaux , Tereza Cindrova-Davies , Margherita Y. Turco","doi":"10.1016/j.ydbio.2024.11.007","DOIUrl":"10.1016/j.ydbio.2024.11.007","url":null,"abstract":"<div><div>The yolk sac is phylogenetically the oldest of the extra-embryonic membranes and plays important roles in nutrient transfer during early pregnancy in many species. In the human this function is considered largely vestigial, in part because the secondary yolk sac never makes contact with the inner surface of the chorionic sac. Instead, it is separated from the chorion by the fluid-filled extra-embryonic coelom and attached to the developing embryo by a relatively long vitelline duct. The coelomic fluid is, however, rich in nutrients and key co-factors, including folic acid and anti-oxidants, derived from maternal plasma and the endometrial glands. Bulk sequencing has recently revealed the presence of transcripts encoding numerous transporter proteins for these ligands. Mounting evidence suggests the human secondary yolk sac plays a pivotal role in the transfer of histotrophic nutrition during the critical phase of organogenesis but also of chemicals such as medical drugs and cotinine. We therefore propose that the early placental villi, coelomic cavity and yolk sac combine to function physiologically as a choriovitelline placenta during the first weeks of pregnancy. We have derived organoids from the mouse yolk sac as proof-of-principle of a model system that could be used to answer many questions concerning the functional capacity of the human yolk sac as a maternal-fetal exchange interface during the first trimester of pregnancy.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"518 ","pages":"Pages 28-36"},"PeriodicalIF":2.5,"publicationDate":"2024-11-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142643808","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Kevin Y.L. Ho , Annie Y.J. Ou , Nicholas Samuelson , Guy Tanentzapf
{"title":"Novel features of Drosophila hematopoiesis uncovered by long-term live imaging","authors":"Kevin Y.L. Ho , Annie Y.J. Ou , Nicholas Samuelson , Guy Tanentzapf","doi":"10.1016/j.ydbio.2024.10.004","DOIUrl":"10.1016/j.ydbio.2024.10.004","url":null,"abstract":"<div><div>Stem cells are subject to continuous regulation to ensure that the correct balance between stem cell differentiation and self-renewal is maintained. The dynamic and ongoing nature of stem cell regulation, as well as the complex signaling microenvironment in which stem cells are typically found, means that studying them in their endogenous environment in real time has multiple advantages over static fixed-sample approaches. We recently described a method for long-term, <em>ex-vivo</em>, live imaging of the blood progenitors in the <em>Drosophila</em> larval hematopoietic organ, the Lymph Gland (LG). This methodology has allowed us to analyze multiple aspects of fly hematopoiesis, in real time, in a manner that could not be carried out previously. Here, we describe novel insights derived from our quantitative live imaging approach. These insights include: the identification of extensive filopodia in the progenitors and description of their morphology and dynamics; visualization and quantitative analysis of JAK/STAT signaling in progenitors by the simultaneous tracking of thousands of vesicles containing internalized Domeless receptors; quantitative analysis of the location, morphology, and dynamics of mitochondria in blood progenitors; long-term tracking of patterns of cell division and migration of mature blood cell in the LG; long-term tracking of multiple cell behaviors in the distal committed progenitors; analysis of Ca<sup>2+</sup> signaling of blood progenitors in the secondary lobes of the LG. Together, these observations illustrate the power of imaging fly hematopoiesis in real time and identify many previously undescribed processes and behaviors in the LG that are likely to play important roles in the regulation of progenitor differentiation and self-renewal.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"517 ","pages":"Pages 286-300"},"PeriodicalIF":2.5,"publicationDate":"2024-11-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142615146","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Manohara Mahadeva, Sebastian Niestępski, Magdalena Kowacz
{"title":"Modifying membrane potential synchronously controls the somite's formation periodicity and growth","authors":"Manohara Mahadeva, Sebastian Niestępski, Magdalena Kowacz","doi":"10.1016/j.ydbio.2024.11.002","DOIUrl":"10.1016/j.ydbio.2024.11.002","url":null,"abstract":"<div><div>Coordination between periodicity of somite formation and somite growth is crucial for regular body pattern formation during somitogenesis. Yet, the specific mechanism that links the two processes remains unclear. Using chick embryos, we demonstrate that both temporal and spatial features can be simultaneously controlled by membrane potential (V<sub>m</sub>) of somite-forming cells. Our findings show that somites hyperpolarize as they mature, displaying step-like changes in V<sub>m</sub> observed between specific groups of somites, reflecting the reported onset of biochemical and structural changes within them. We modify V<sub>m</sub> by changing chemical compositions of the microenvironment of the embryo. Alteration of V<sub>m</sub> sets a new pace of somite formation (cell migration and self-assembly) and its concurrent growth (cell proliferation) without disturbing the somite's regular aspect ratio. Our results therefore suggest that V<sub>m</sub> has the ability to orchestrate cell proliferation, migration and self-assembly - processes that are hallmarks of embryogenesis, tumorigenesis and tissue regeneration.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"517 ","pages":"Pages 317-326"},"PeriodicalIF":2.5,"publicationDate":"2024-11-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142615215","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"R391 human dominant mutation does not affect TubB4b localization and sensory hair cells structure in zebrafish inner ear and lateral line","authors":"Wiam Smaili , Camille Pezet , Sandrine Marlin , Sylvain Ernest","doi":"10.1016/j.ydbio.2024.11.001","DOIUrl":"10.1016/j.ydbio.2024.11.001","url":null,"abstract":"<div><div>Heterozygous R391 <em>TUBB4B</em> pathogenic variations are responsible for an association of hearing loss and retinal dystrophy in human. With the goal of understanding the functions of TuBB4b and the pathogenic role of R391 variations, we characterized <em>tubB4B</em> in zebrafish and identified the gene regulatory elements necessary and sufficient for expression of TubB4b as in endogenous tissues. Using knock-out and transgenic approaches, we determined that R391 mutations impair neither localization of TubB4B within sensory hair cells (SHC) nor their structure, but induced to a small decrease in SHC number from anterior crista. Expression of R391 mutations in sensory hair cells has no effect on zebrafish audition, suggesting a different equilibrium between various tubulin isotypes in zebrafish possibly due to compensatory mechanisms. The careful expression analysis and transgenic tools generated in this study could help understand how recently described pathogenic variants lead to more severe clinical forms of TUBB4B-related diseases.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"517 ","pages":"Pages 301-316"},"PeriodicalIF":2.5,"publicationDate":"2024-11-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142602701","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Off to a good start: The importance of the placental exchange surface – Lessons from the mouse","authors":"Noura Ballasy , Ifeoluwa Apantaku , Wendy Dean , Myriam Hemberger","doi":"10.1016/j.ydbio.2024.10.009","DOIUrl":"10.1016/j.ydbio.2024.10.009","url":null,"abstract":"<div><div>The role of the chorio-allantoic placenta as the critical nutrient- and oxygen-supplying organ to nourish the demands of the fetus has been well recognized. This function relies on the successful establishment of the placental feto-maternal exchange unit, or interhaemal barrier, across which all nutrients as well as waste products must pass to cross from the maternal to the fetal blood circulation, or vice versa, respectively. As a consequence, defects in the establishment of this elaborate interface lead to fetal growth retardation or even embryonic lethality, depending on the severity of the defect. Beyond this essential role, however, it has also emerged that the functionality of the feto-maternal interface dictates the proper development of specific embryonic organs, with tightest links observed to the formation of the heart. In this article, we build on the foundational strength of the mouse as experimental model in which the placental causality of embryonic defects can be genetically proven. We discuss in detail the formation of the interhaemal barrier that makes up the labyrinth layer of the murine placenta, including insights into drivers of its formation and the interdependence of the cell types that make up this essential interface, from <em>in vivo</em> and <em>in vitro</em> data using mouse trophoblast stem cells. We highlight mouse genetic tools that enable the elucidation of cause-effect relationships between defects driven by either the trophoblast cells of the placenta or by embryonic cell types. We specifically emphasize gene knockouts for which a placental causality of embryonic heart defects has been demonstrated. This in-depth perspective provides much-needed insights while highlighting remaining gaps in knowledge that are essential for gaining a better understanding of the multi-facetted roles of the placenta in setting us up for a healthy start in life well beyond nutritional support alone.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"517 ","pages":"Pages 248-264"},"PeriodicalIF":2.5,"publicationDate":"2024-11-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142567747","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Helen F. Schmidt, Chelsea B. Darwin, Meera V. Sundaram
{"title":"The Pax transcription factor EGL-38 links EGFR signaling to assembly of a cell type-specific apical extracellular matrix in the Caenorhabditis elegans vulva","authors":"Helen F. Schmidt, Chelsea B. Darwin, Meera V. Sundaram","doi":"10.1016/j.ydbio.2024.10.008","DOIUrl":"10.1016/j.ydbio.2024.10.008","url":null,"abstract":"<div><div>The surface of epithelial tissues is covered by an apical extracellular matrix (aECM). The aECMs of different tissues have distinct compositions to serve distinct functions, yet how a particular cell type assembles the proper aECM is not well understood. We used the cell type-specific matrix of the <em>C. elegans</em> vulva to investigate the connection between cell identity and matrix assembly. The vulva is an epithelial tube composed of seven cell types descending from EGFR/Ras-dependent (1°) and Notch-dependent (2°) lineages. Vulva aECM contains multiple Zona Pellucida domain (ZP) proteins, which are a common component of aECMs across life. ZP proteins LET-653 and CUTL-18 assemble on 1° cell surfaces, while NOAH-1 assembles on a subset of 2° surfaces. All three ZP genes are broadly transcribed, indicating that cell type-specific ZP assembly must be determined by features of the destination cell surface. The paired box (Pax) transcription factor EGL-38 promotes assembly of 1° matrix and prevents inappropriate assembly of 2° matrix, suggesting that EGL-38 promotes expression of one or more ZP matrix organizers. Our results connect the known signaling pathways and various downstream effectors to EGL-38/Pax expression and the ZP matrix component of vulva cell fate execution. We propose that dedicated transcriptional networks may contribute to cell-appropriate assembly of aECM in many epithelial organs.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"517 ","pages":"Pages 265-277"},"PeriodicalIF":2.5,"publicationDate":"2024-11-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142567751","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Blastocoel expansion and AMOT degradation cooperatively promote YAP nuclear localization during epiblast formation","authors":"Hinako Maeda (前田日向子), Hiroshi Sasaki (佐々木洋)","doi":"10.1016/j.ydbio.2024.10.007","DOIUrl":"10.1016/j.ydbio.2024.10.007","url":null,"abstract":"<div><div>The epiblast is a pluripotent cell population formed in the late blastocyst stage of preimplantation embryos. During the process of epiblast formation from the inner cell mass (ICM) of the early blastocyst, activation of the Hippo pathway transcription factor TEAD by the nuclear translocation of the coactivator protein YAP is required for the robust expression of pluripotency factors. However, the mechanisms that alter YAP localization during epiblast formation remain unknown. Here, we reveal two such mechanisms. Expansion of the blastocoel promotes nuclear YAP localization by increasing cytoplasmic F-actin and reducing YAP phosphorylation. Additionally, cell differentiation regulates YAP. Expression of the junctional Hippo component, AMOT, gradually decreases during epiblast formation through a tankyrase-mediated degradation. SOX2 expression in the ICM is necessary for the reduction of AMOT and YAP phosphorylation. These two mechanisms function in parallel. Thus, the blastocoel–F-actin and SOX2–AMOT axes cooperatively suppress YAP phosphorylation and promote YAP nuclear localization during epiblast formation. The cooperation of these two distinct mechanisms likely contributes to the robustness of epiblast cell differentiation.</div></div>","PeriodicalId":11070,"journal":{"name":"Developmental biology","volume":"517 ","pages":"Pages 234-247"},"PeriodicalIF":2.5,"publicationDate":"2024-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142564164","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}