DOCSLIB.ORG

Temporal Dynamics of Pair-Rule Stripes in Living Drosophila Embryos

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Temporal Dynamics of Pair-Rule Stripes in Living Drosophila Embryos Temporal dynamics of pair-rule stripes in living Drosophila embryos Bomyi Lima,1, Takashi Fukayab,2, Tyler Heistb, and Michael Levineb,c,1 aDepartment of Chemical and Biomolecular Engineering, University of Pennsylvania, Philadelphia, PA 19104; bLewis–Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ 08544; and cDepartment of Molecular Biology, Princeton University, Princeton, NJ 08544 Contributed by Michael Levine, June 29, 2018 (sent for review June 21, 2018; reviewed by Christine Rushlow and Alexander Stark) Traditional studies of gene regulation in the Drosophila embryo that enhancer–enhancer interactions within the eve locus may be centered primarily on the analysis of fixed tissues. These methods important for the precision of expression. provided considerable insight into the spatial control of gene ac- tivity, such as the borders of eve stripe 2, but yielded only limited Results and Discussion information about temporal dynamics. The advent of quantitative ftz is regulated by four separate enhancers located upstream and live-imaging and genome-editing methods permits the detailed downstream of the transcription unit (15, 16). Three of the en- examination of the temporal control of endogenous gene activity. hancers initiate stripes 3+6, 2+7, and 1+5. There is no stripe 4 “ ” Here, we present evidence that the pair-rule genes fushi tarazu enhancer, and thus its expression depends on the classical Zebra (ftz) and even-skipped (eve) undergo dynamic shifts in gene ex- enhancer, which directs all seven expression stripes at later stages following initiation by the individual stripe enhancers (3, 17). We pression. We observe sequential anterior shifting of the stripes ftz along the anterior to posterior axis, with stripe 1 exhibiting move- created separate alleles containing 24 copies of either MS2 or PP7 RNA stem loops inserted into the 3′ UTR of the endogenous ment before stripe 2 and the more posterior stripes. Conversely, A ftz- posterior stripes shift over greater distances (two or three nuclei) locus (Fig. 1 ). Fluorescent in situ hybridization (FISH) of MS2 revealed expression patterns comparable to those seen in than anterior stripes (one or two nuclei). Shifting of the ftz and yw SI Appendix eve ftz eve wild-type embryos ( ,Fig.S1). Moreover, homozy- stripes are slightly offset, with moving faster than . This gotes of these alleles were fully viable, fertile, and phenotypically observation is consistent with previous genetic studies, suggesting indistinguishable from wild-type flies. This suggests that the stem BIOLOGY eve ftz DEVELOPMENTAL that is epistatic to . The precision of pair-rule temporal loops do not significantly affect either transcription or translation. – dynamics might depend on enhancer enhancer interactions within Twelve embryos expressing either ftz-MS2 or ftz-PP7 were eve eve the locus, since removal of the endogenous stripe 1 en- analyzed, and similar results were obtained for both alleles. hancer via CRISPR/Cas9 genome editing led to precocious and ex- Nuclei were visualized with His2AV-mRFP or His2AV-eBFP2, panded expression of eve stripe 2. These observations raise the allowing us to trace transcriptional activity from individual nuclei possibility of an added layer of complexity in the positional infor- during nuclear cycle (nc) 14. There was a clear anterior shift in mation encoded by the segmentation gene regulatory network. the ftz expression pattern for all stripes during a 15–30-min in- terval of nc 14 (Fig. 1 B and C, SI Appendix, Fig. S2, and Movie live imaging | Drosophila embryo | MS2-PP7 | even-skipped | fushi tarazu S1). Strikingly, while each ftz stripe was formed at different time points in nc 14, the initial ftz transcripts were always first de- Drosophila tected in the interstripe regions of the mature stripes (Fig. 1 B he segmentation of the embryo represents one of C ftz-MS2 the most extensively examined gene regulatory networks in and and Movie S1). Comparison of mRNA accumu- T lation along the anteroposterior (AP) axis between early and animal development. Maternal gradients of Bicoid, Hunchback, SI and Caudal establish sequential, overlapping patterns of gap late nc 14 revealed clear anterior shifts in stripe positions ( Appendix, Fig. S3). Moreover, there was an anterior-to-posterior gene expression, which, in turn, delineate pair-rule stripes that subdivide the embryo into a repeating series of body seg- ments (1–3). The classical view of this system invokes thresh- Significance old responses of pair-rule stripe enhancers to static gradients of maternal and gap gene regulatory factors (4–6). However, Classical studies of gene activity in development focused on quantitative imaging studies have revealed anterior shifts in gap spatial limits due to the use of fixed tissues for analysis. The gene expression, particularly in posterior regions of cellularizing advent of live-imaging methods provides an opportunity to embryos (7–9). These shifts are thought to enrich the positional examine the temporal control of gene expression. Here, we information encoded by this system through dynamic changes in used quantitative live-imaging methods to visualize dynamic the distribution of regulatory gradients over time. We sought to shifts in the endogenous expression of eve and ftz pair-rule explore how these dynamic changes in gap gene expression would stripes in the early Drosophila embryo. We suggest that be read out at the level of the pair-rule genes that they regulate. these temporal dynamics add to the complexity encoded by the We analyzed the temporal dynamics of the pair-rule genes segmentation gene network. fushi tarazu (ftz) and even-skipped (eve), which are responsible for specifying the even and odd parasegments, respectively (10). Author contributions: B.L., T.F., and M.L. designed research; B.L., T.F., and T.H. performed MS2 and PP7 RNA stem loops were inserted into the 3′ UTRs of research; B.L. analyzed data; and B.L., T.F., and M.L. wrote the paper. the endogenous loci using CRISPR/Cas9-mediated genome Reviewers: C.R., New York University; and A.S., Research Institute of Molecular Pathology. editing (11–14). Visualization of the expression patterns in living Conflict of interest statement: C.R. and B.L. are coauthors of a 2015 paper. They did not embryos reveals highly dynamic shifts in each of the stripes, in- collaborate directly on this work. cluding those located in anterior regions of the embryo. These Published under the PNAS license. shifts are particularly striking for ftz, in that the initial sites of ex- 1To whom correspondence may be addressed. Email: [email protected] or msl2@ pression correspond to the interstripe regions of the mature stripes. princeton.edu. Simultaneous visualization of ftz and eve expression suggests rapid 2Present address: Institute for Quantitative Biosciences, The University of Tokyo, Tokyo shifting of the ftz stripes, followed by a slight lag in refinement of the 113-0032, Japan. eve stripes. We propose that the differential rates of ftz and eve This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. temporal dynamics contribute to the positional information enco- 1073/pnas.1810430115/-/DCSupplemental. ded by the segmentation network. Moreover, we provide evidence www.pnas.org/cgi/doi/10.1073/pnas.1810430115 PNAS Latest Articles | 1of6 Downloaded by guest on September 30, 2021 A fushi tarazu 3+6 2+7 Zebra 1+5 MS2 or PP7 ftz BCMature stripes Instantaneously active nuclei ftz Active nuclei within mature ftz domain Mature stripe region 300 123 4 5 6 7 250 200 150 100 13.1 min 13.1 50 0 Fluorescent intensity (a.u.) intensity Fluorescent anterior posteriote r 300 250 200 150 100 25.3 min 25.3 50 0 Fluorescent intensity (a.u.) intensity Fluorescent anterior posteriote r 300 250 200 150 100 37.4 min 37.4 50 0 Fluorescent intensity (a.u.) anterior posteriote r 300 250 200 150 100 50.2 min 50.2 50 0 Fluorescent intensity (a.u.) anterior posterior Fig. 1. Dynamics of endogenous ftz expression pattern. (A) Schematic of endogenous ftz gene locus and ftz enhancers. Here, 24 repeats of MS2 or PP7 stem loops are inserted into the 3′ UTR. (B) Snapshots from an embryo expressing ftz-MS2. Nuclei that will form mature ftz stripes are false-colored in red. Mature ftz stripes are defined as the nuclei that exhibit active transcription after 40 min into nc 14. Nuclei that show active transcription in a given frame are false-colored in green. Yellow nuclei represent those that show active transcription within the mature ftz domain. Nuclei were visualized with His2Av-mRFP and are shown in blue. Note that stripes are initially formed at one to three cells posterior to their final position. Time represents minutes after the onset of nc 14. (C) Average spatial profile of ftz transcriptional activity along the AP axis during nc 14. Each plot corresponds to the snapshot shown in B. The AP axis was divided into 35 bins, and an average transcriptional activity from all the nuclei within each bin was plotted. The error bar represents ±SEM of all the nuclei within each bin. Blue columns represent the location of mature ftz stripes 1–7. wave in the temporal shifts whereby stripe 1 shifted earlier than the shifts, there was a refinement in each of the stripes during the stripe 2, followed by the more posterior stripes (Fig. 1C). These latter periods of nc 14, such that the anterior boundary of each sequential shifts are evocative of the wavefront of gene expres- stripe was fixed and the posterior nuclei gradually lost tran- sion seen during somitogenesis in vertebrates (18, 19). Following scriptional activity (Fig. 1B). 2of6 | www.pnas.org/cgi/doi/10.1073/pnas.1810430115 Lim et al. Downloaded by guest on September 30, 2021 eve is regulated by five separate enhancers located upstream with the posterior stripes displaying more significant movement and downstream of the transcription unit (20, 21).
Load more

Recommended publications
  • Interactions of the Drosophila Gap Gene Giant with Maternal and Zygotic Pattern-Forming Genes
    Development 111, 367-378 (1991) 367 Printed in Great Britain © The Company of Biologists Limited 1991 Interactions of the Drosophila gap gene giant with maternal and zygotic pattern-forming genes ELIZABETH D. ELDON* and VINCENZO PIRROTTA Department of Cell Biology, Baylor College of Medicine, Texas Medical Center, Houston, TX 77030, USA 'Present address: Howard Hughes Medical Institute and Institute of Molecular Genetics, Baylor College of Medicine, Texas Medical Center, Houston, TX 77030, USA Summary The Drosophila gene giant (gt) is a segmentation gene other gap genes. These interactions, typical of the cross- that affects anterior head structures and abdominal regulation previously observed among gap genes, segments A5-A7. Immunolocalization of the gt product confirm that gt is a member of the gap gene class whose shows that it is a nuclear protein whose expression is function is necessary to establish the overall pattern of initially activated in an anterior and a posterior domain. gap gene expression. After cellular blastoderm, gt Activation of the anterior domain is dependent on the protein continues to be expressed in the head region in maternal bicoid gradient while activation of the posterior parts of the maxillary and mandibular segments as well domain requires maternal nanos gene product. Initial as in the labrum. Expression is never detected in the expression is not abolished by mutations in any of the labial or thoracic segment primordia but persists in zygotic gap genes. By cellular blastoderm, the initial certain head structures, including the ring gland, until pattern of expression has evolved into one posterior and the end of embryonic development.
    [Show full text]
  • Drosophila: the Genetics of Segmentation (WR Lecture 2)
    Drosophila: the genetics of segmentation (WR lecture 2) In the previous lecture we covered the Drosophila life cycle from developing oocyte to the newly-cellularized blastoderm. At this stage (left), the embryo is shaped like a slightly bent rugby ball with about 6000 cells distributed around the surface. There are very few recognizable surface or internal features, but the future body plan is already mapped out through the expression of a set of genes known as the segmentation genes. This expression pattern - which defines a series of 15 stripes around the embryo - is a "molecular blueprint" that specifies the larval and adult segments. In this lecture we learn about the molecular events that subdivide the embryo into stripes (known as parasegments in the embryo). The key players in this process were identified during a genetic screen that was carried out by Christiane Nusslein-Volhart, Eric Wieschaus and their collaborators. Their groundbreaking effort was rewarded in 1995 by the award of the Nobel prize in Physiology and Medicine, which they shared with Ed Lewis for his work on homeotic mutants (next lecture). All animals, whether flies or humans, are constructed according to a fundamental repeated pattern so this work in Drosophila lays the foundation for understanding development of all animals. 1. Three sets of maternal effect genes define the anterior-posterior axis. These are the anterior group, the posterior group and the terminal group genes (the latter determine structures at the extreme front and back ends of the fly - the telson at the back and the acron at the front). The main player in the anterior group is bicoid, mRNA for which is localized at the anterior end of the oocyte and is translated into protein (a homeodomain transcription factor) that diffuses posteriorly to set up an anterior-posterior (high-low) concentration gradient.
    [Show full text]
  • Annotated Classic Protein Control of Pattern Formation
    Annotated Classic Protein Control of Pattern Formation James Briscoe1,* 1Developmental Biology, National Institute for Medical Research, Mill Hill, London NW7 1AA, UK *Correspondence: [email protected] We are pleased to present a series of Annotated Classics celebrating 40 years of exciting biology in the pages of Cell. This installment revisits “The bicoid Protein Determines Position in the Drosophila Embryo in a Concentration-Dependent Manner” by Wolfgang Driever and Christiane Nüsslein-Volhard. Here, James Briscoe comments on one of a pair of papers from Driever and Nüsslein-Volhard, published back-to-back in Cell, that established bicoid as the first definitive example of a protein morphogen, that is, a protein which shapes a developmental pathway by virtue of its concentration gradient across a region of an embryo. Nüsslein-Volhard shared the Nobel Prize in Physiology or Medicine in 1995 with Edward B. Lewis and Eric F. Wieschaus for their discoveries related to control of early embryogenesis. Each Annotated Classic offers a personal perspective on a groundbreaking Cell paper from a leader in the field with notes on what stood out at the time of first reading and retrospective comments regarding the longer term influence of the work. To see James Briscoe’s thoughts on different parts of the manuscript, just download the PDF and then hover over or double- click the highlighted text and comment boxes. You can also view Briscoe’s annotation by opening the Comments navigation panel in Acrobat. Cell 157, April 24, 2014, 2014 ©2014 Elsevier Inc. Cell, Vol. 54, 95-104, July 1, 1988, Copyright © 1988 by Cell Press The bicoid Protein Determines Position in the Drosophila Embryo in a Concentration-Dependent Manner Wolfgang Driever and Christiane N0sslein-Volhard is established in early embryogenesis.
    [Show full text]
  • Embryonic Geometry Underlies Phenotypic Variation in Decanalized Conditions Anqi Huang1, Jean-Franc¸Ois Rupprecht1,2, Timothy E Saunders1,3,4*
    RESEARCH ARTICLE Embryonic geometry underlies phenotypic variation in decanalized conditions Anqi Huang1, Jean-Franc¸ois Rupprecht1,2, Timothy E Saunders1,3,4* 1Mechanobiology Institute, National University of Singapore, Singapore, Singapore; 2CNRS and Turing Center for Living Systems, Centre de Physique The´orique, Aix- Marseille Universite´, Marseille, France; 3Department of Biological Sciences, National University of Singapore, Singapore, Singapore; 4Institute of Molecular and Cell Biology, Proteos, A*Star, Singapore, Singapore Abstract During development, many mutations cause increased variation in phenotypic outcomes, a phenomenon termed decanalization. Phenotypic discordance is often observed in the absence of genetic and environmental variations, but the mechanisms underlying such inter- individual phenotypic discordance remain elusive. Here, using the anterior-posterior (AP) patterning of the Drosophila embryo, we identified embryonic geometry as a key factor predetermining patterning outcomes under decanalizing mutations. With the wild-type AP patterning network, we found that AP patterning is robust to variations in embryonic geometry; segmentation gene expression remains reproducible even when the embryo aspect ratio is artificially reduced by more than twofold. In contrast, embryonic geometry is highly predictive of individual patterning defects under decanalized conditions of either increased bicoid (bcd) dosage or bcd knockout. We showed that the phenotypic discordance can be traced back to variations in the gap gene expression, which is rendered sensitive to the geometry of the embryo under mutations. *For correspondence: [email protected] Introduction Competing interests: The The phenomenon of canalization describes the constancy in developmental outcomes between dif- authors declare that no ferent individuals within a wild-type species growing in their native environments (Flatt, 2005; competing interests exist.
    [Show full text]
  • Trading Bits in the Readout from a Genetic Network Marianne Bauer, Mariela Petkova, Thomas Gregor, Eric Wieschaus, William Bialek
    Trading bits in the readout from a genetic network Marianne Bauer, Mariela Petkova, Thomas Gregor, Eric Wieschaus, William Bialek To cite this version: Marianne Bauer, Mariela Petkova, Thomas Gregor, Eric Wieschaus, William Bialek. Trading bits in the readout from a genetic network. 2020. pasteur-03216308 HAL Id: pasteur-03216308 https://hal-pasteur.archives-ouvertes.fr/pasteur-03216308 Preprint submitted on 3 May 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Trading bits in the readout from a genetic network Marianne Bauer,1−4 Mariela D. Petkova,5 Thomas Gregor,1;2;6 Eric F. Wieschaus,2−4 and William Bialek1;2;7 1Joseph Henry Laboratories of Physics, 2Lewis{Sigler Institute for Integrative Genomics, 3Department of Molecular Biology, and 4Howard Hughes Medical Institute, Princeton University, Princeton, NJ 08544 USA 5Program in Biophysics, Harvard University, Cambridge, MA 02138, USA 6Department of Developmental and Stem Cell Biology, UMR3738, Institut Pasteur, 75015 Paris, France 7Initiative for the Theoretical Sciences, The Graduate Center, City University of New York, 365 Fifth Ave, New York, NY 10016 In genetic networks, information of relevance to the organism is represented by the concentrations of transcription factor molecules.
    [Show full text]
  • A Multiscale Agent-Based Model of Morphogenesis in Biological Systems
    A Multiscale Agent-based Model of Morphogenesis in Biological Systems Sara Montagna Andrea Omicini Alessandro Ricci DEIS–Universita` di Bologna DEIS–Universita` di Bologna DEIS–Universita` di Bologna via Venezia 52, 47023 Cesena, Italy via Venezia 52, 47023 Cesena, Italy via Venezia 52, 47023 Cesena, Italy Email: [email protected] Email: [email protected] Email: [email protected] Abstract—Studying the complex phenomenon of pattern for- simulate dynamics at different hierarchical levels and spatial mation created by the gene expression is a big challenge in and temporal scales. the field of developmental biology. This spatial self-organisation A central challenge in the field of developmental biology autonomously emerges from the morphogenetic processes and the hierarchical organisation of biological systems seems to play is to understand how mechanisms at intracellular and cellular a crucial role. Being able to reproduce the systems dynamics level of the biological hierarchy interact to produce higher at different levels of such a hierarchy might be very useful. In level phenomena, such as precise and robust patterns of this paper we propose the adoption of the agent-based model as gene expressions which clearly appear in the first stages of an approach capable of capture multi-level dynamics. Each cell morphogenesis and develop later into different organs. How is modelled as an agent that absorbs and releases substances, divides, moves and autonomously regulates its gene expression. does local interaction among cells and inside cells give rise to As a case study we present an agent-based model of Drosophila the emergent self-organised patterns that are observable at the melanogaster morphogenesis.
    [Show full text]
  • Krüppel Acts As a Gap Gene Regulating Expression of Hunchback and Even-Skipped in the Intermediate Germ Cricket Gryllus Bimaculatus
    Developmental Biology 294 (2006) 471–481 www.elsevier.com/locate/ydbio Krüppel acts as a gap gene regulating expression of hunchback and even-skipped in the intermediate germ cricket Gryllus bimaculatus Taro Mito, Haruko Okamoto, Wakako Shinahara, Yohei Shinmyo, Katsuyuki Miyawaki, ⁎ Hideyo Ohuchi, Sumihare Noji Department of Biological Science and Technology, Faculty of Engineering, The University of Tokushima, 2-1 Minami-Jyosanjima-cho, Tokushima City 770-8506, Japan Received in publication 25 August 2005, revised 22 December 2005, accepted 27 December 2005 Available online 17 April 2006 Abstract In Drosophila, a long germ insect, segmentation occurs simultaneously across the entire body. In contrast, in short and intermediate germ insects, the anterior segments are specified during the blastoderm stage, while the remaining posterior segments are specified during later stages.In Drosophila embryos, the transcriptional factors coded by gap genes, such as Krüppel, diffuse in the syncytial environment and regulate the expression of other gap, pair-rule, and Hox genes. To understand the segmentation mechanisms in short and intermediate germ insects, we investigated the role of Kr ortholog (Gb'Kr) in the development of the intermediate germ insect Gryllus bimaculatus. We found that Gb'Kr is expressed in a gap pattern in the prospective thoracic region after cellularization of the embryo. To determine the function of Gb'Kr in segmentation, we analyzed knockdown phenotypes using RNA interference (RNAi). Gb'Kr RNAi depletion resulted in a gap phenotype in which the posterior of the first thoracic through seventh abdominal segments were deleted. Analysis of the expression patterns of Hox genes in Gb'Kr RNAi embryos indicated that regulatory relationships between Hox genes and Kr in Gryllus differ from those in Oncopeltus, another intermediate germ insect.
    [Show full text]
  • Modeling of Gap Gene Expression in Drosophila Kruppel Mutants
    Modeling of Gap Gene Expression in Drosophila Kruppel Mutants Konstantin Kozlov1, Svetlana Surkova1, Ekaterina Myasnikova1, John Reinitz2, Maria Samsonova1* 1 Department of Computational Biology/Center for Advanced Studies, St.Petersburg State Polytechnical University, St.Petersburg, Russia, 2 Chicago Center for Systems Biology, Department of Ecology and Evolution, Department of Statistics, and Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago, Illinois, United States of America Abstract The segmentation gene network in Drosophila embryo solves the fundamental problem of embryonic patterning: how to establish a periodic pattern of gene expression, which determines both the positions and the identities of body segments. The gap gene network constitutes the first zygotic regulatory tier in this process. Here we have applied the systems-level approach to investigate the regulatory effect of gap gene Kruppel (Kr) on segmentation gene expression. We acquired a large dataset on the expression of gap genes in Kr null mutants and demonstrated that the expression levels of these genes are significantly reduced in the second half of cycle 14A. To explain this novel biological result we applied the gene circuit method which extracts regulatory information from spatial gene expression data. Previous attempts to use this formalism to correctly and quantitatively reproduce gap gene expression in mutants for a trunk gap gene failed, therefore here we constructed a revised model and showed that it correctly reproduces the expression patterns of gap genes in Kr null mutants. We found that the remarkable alteration of gap gene expression patterns in Kr mutants can be explained by the dynamic decrease of activating effect of Cad on a target gene and exclusion of Kr gene from the complex network of gap gene interactions, that makes it possible for other interactions, in particular, between hb and gt, to come into effect.
    [Show full text]
  • Embryology, Differentiation, Morphogenesis and Growth - Han Wang
    REPRODUCTION AND DEVELOPMENT BIOLOGY - Embryology, Differentiation, Morphogenesis and Growth - Han Wang EMBRYOLOGY, DIFFERENTIATION, MORPHOGENESIS AND GROWTH Han Wang Department of Zoology and Stephenson Research & Technology Center, University of Oklahoma, Norman, Oklahoma, USA Keywords: Zygote, cleavage, gastrulation, ectoderm, mesoderm, endoderm, commitment, specification, determination, differential gene expression, induction, competence, morphogens, signal transduction pathways, cell adhesion, cadherins, extracellular matrix (ECM), organogenesis and apoptosis Contents 1. Introduction – Life is a cycle 2. Cleavage 2.1. Biphasic Cell Divisions during Cleavage 2.2. Cleavage Patterns 2.3. Midblastula Transition (MBT) 3. Gastrulation, cell movements and the three germ layers 3.1. Modes of Cell Movements 3.2. Ectoderm and its Derivatives 3.3. Mesoderm and its Derivatives 3.4. Endoderm and its Derivatives 3.5. Cell Migration 4. Axis formation 4.1. Anterior-posterior Axis (AP axis) 4.2. Dorsal-ventral Axis (DV axis) 4.3. Left-right Axis (LR axis) 5. Differential gene expression and cellular differentiation 5.1. Genomic Equivalence and Somatic Nuclear Transfer – Cloning 5.2. Cell Fate Commitment 5.2.1. Autonomous Specification 5.2.2. Conditional Specification 5.2.3. Syncytial Specification 5.3. DifferentialUNESCO Gene Expression – EOLSS 6. Induction and morphogenesis 6.1. Induction, Competence, and Cell-cell Communications 6.2. Signal TransductionSAMPLE Pathways CHAPTERS 6.2.1. General Features of Signal Transduction Pathways 6.2.2. Wnt Signaling 6.2.3. Hedgehog Signaling 6.2.3. Notch Signaling 6.2.4. Other Signaling Pathways 6.3. Morphogenesis 7. Growth 7.1. Cellular Growth 7.2. Isometric Growth and Allometric Growth ©Encyclopedia of Life Support Systems(EOLSS) REPRODUCTION AND DEVELOPMENT BIOLOGY - Embryology, Differentiation, Morphogenesis and Growth - Han Wang 7.3.
    [Show full text]
  • PNR Lecture 24
    Lecture 24 Gene Regulation during Drosophila Development An organism arises from a fertilized egg as a result of three key processes: Cell division, Cell differentiation and Morphogenesis Following fertilization, as the egg starts dividing and development proceeds, cells which are initially undifferentiated (Embryonic stem cells) ultimately differentiate into specific cell types. Differential expression of genes in the embryonal cells plays a key role in their differentiation into diverse cell types, tissues and organs during development. Regulation of gene expression during development is directed by: Maternal molecules in the fertilized egg’s cytoplasm Extracellular signals and cell-cell interactions In animals, development & differentiation begin in early embryo: First, the basic body plan is established Next, Major axes are established (Dorsal, ventral, anterior, posterior) Gene regulation during embryonic development is studied in a number of model organisms such as Drosophila melanogaster, Cenorhabditis elegans, zebra fish, mouse etc. Drosophila melanogaster Bilateral symmetry Segmented body that is divided into Head, Thorax and Abdomen Drosophila melaogaster Early embryonic development After fertilization, the diploid, zygotic nucleus undergoes 10 rapid cleavages. At this stage, the embryo is called a syncitium because it is a single cell with multiple nuclei. After 8 cleavages, the resulting 256 nuclei begin to migrate to the outer edge of the cell. About 90 minutes after fertilization, most nuclei have reached the periphery. These nuclei undergo 3 more cleavages. Plasma membranes finally partition ~6,000 nuclei into separate cells at the thirteenth division. By this time the basic body plan (Body axes, segments, boundaries) is already determined. When the nuclei reach the periphery, they are totipotent.
    [Show full text]
  • Mutually Repressive Interactions Between the Gap Genes Giant and Kruppel Define Middle Body Regions of the Drosophila Embryo
    Development 111, 611-621 (1991) 611 Printed in Great Britain © The Company of Biologists Limited 1991 Mutually repressive interactions between the gap genes giant and Kruppel define middle body regions of the Drosophila embryo RACHEL KRAUT and MICHAEL LEVINE* Department of Biological Sciences, Fairchild Center, Columbia University, New York, NY 10027, USA * Present address: Department of Biology, Bonner Hall, University of California at San Diego, La Jolla, CA 92093-0346 Summary The gap genes play a key role in establishing pair-rule repression of Kruppel, and advanced-stage embryos and homeotic stripes of gene expression in the Dros- show cuticular defects similar to those observed in ophila embryo. There is mounting evidence that Kriippel" mutants. This result and others suggest that overlapping gradients of gap gene expression are crucial the strongest regulatory interactions occur among those for this process. Here we present evidence that the gap genes expressed in nonadjacent domains. We segmentation gene giant is a bona fide gap gene that is propose that the precisely balanced overlapping gradi- likely to act in concert with hunchback, Kruppel and ents of gap gene expression depend on these strong knirps to initiate stripes of gene expression. We show regulatory interactions, coupled with weak interactions that Kruppel and giant are expressed in complementary, between neighboring genes. non-overlapping sets of cells in the early embryo. These complementary patterns depend on mutually repressive interactions between the two genes. Ectopic expression Key words: gap genes, cross-regulation, gradients, giant, of giant in early embryos results in the selective segmentation, Drosophila. Introduction have been shown to bind specific sequences within the eve promoter (StanojeviC et al.
    [Show full text]
  • The Zygotic Control of Drosophila Pair-Rule Gene Expression II
    Development 107, 673-683 (1989) 673 Printed in Great Britain © The Company of Biologists Limited 1989 The zygotic control of Drosophila pair-rule gene expression II. Spatial repression by gap and pair-rule gene products SEAN B. CARROLL and STEPHANIE H. VAVRA Laboratory of Molecular Biology and Department of Genetics, University of Wisconsin-Madison, 1525 Linden Drive, Madison, WI 53706, USA Summary We examined gene expression patterns in certain single (hb), Krtippel (Kr), and knirps (Icnf) have been removed, and double pair-rule mutant embryos to determine indicating that these gap genes are not essential to which of the largely repressive pair-rule gene interac- activate the pair-rule genes. In fact, we show that in the tions are most likely to be direct and which interactions absence of either hb+ or kni+, or both gap genes, the Kr+ are probably indirect. From these studies we conclude product represses hairy expression. These results suggest that: (i) hairy+ and even-skipped (eve+) regulate the fushi that gap genes repress hairy expression in the interstripe tarazu (ftz) gene; (ii) eve+ and runt+ regulate the hairy regions, rather than activate hairy expression in the gene; (iii) runt+ regulates the eve gene; but, (iv) runt does stripes. The molecular basis of pair-rule gene regulation not regulate the ftz gene pattern, and hairy does not by gap genes must involve some dual control mechan- regulate the eve gene pattern. These pair-rule interac- isms such that combinations of gap genes affect pair-rule tions are not sufficient, however, to explain the period- transcription in a different manner than a single gap icity of the hairy and eve patterns, so we examined gene.
    [Show full text]