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      Mechanical Control of Whole Body Shape by a Single Cuticular Protein Obstructor-E in Drosophila melanogaster

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          Abstract

          Body shapes are much more variable than body plans. One way to alter body shapes independently of body plans would be to mechanically deform bodies. To what extent body shapes are regulated physically, or molecules involved in physical control of morphogenesis, remain elusive. During fly metamorphosis, the cuticle (exoskeleton) covering the larval body contracts longitudinally and expands laterally to become the ellipsoidal pupal case (puparium). Here we show that Drosophila melanogaster Obstructor-E (Obst-E) is a protein constituent of the larval cuticle that confers the oriented contractility/expandability. In the absence of obst-E function, the larval cuticle fails to undergo metamorphic shape change and finally becomes a twiggy puparium. We present results indicating that Obst-E regulates the arrangement of chitin, a long-chain polysaccharide and a central component of the insect cuticle, and directs the formation of supracellular ridges on the larval cuticle. We further show that Obst-E is locally required for the oriented shape change of the cuticle during metamorphosis, which is associated with changes in the morphology of those ridges. Thus, Obst-E dramatically affects the body shape in a direct, physical manner by controlling the mechanical property of the exoskeleton.

          Author Summary

          Shapes of objects, living or not, should depend on their material properties and forces acting on them. Mechanical processes that create whole body shapes of multicellular organisms, or genes that regulate such processes, are largely unknown. Insect bodies are coated by cuticle, a matrix composed of proteins and the polysaccharide chitin. We show that, during metamorphosis of the fruit fly Drosophila melanogaster, the cuticle covering the long and thin larva (maggot) undergoes longitudinal contraction and lateral expansion to become the short and stout puparium covering the pupa. Furthermore, we identify a single protein component of the larval cuticle that confers the oriented contractility/expandability, thereby determining the pupal body shape in a mechanical manner.

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          Most cited references 27

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          Design and mechanical properties of insect cuticle.

          Since nearly all adult insects fly, the cuticle has to provide a very efficient and lightweight skeleton. Information is available about the mechanical properties of cuticle-Young's modulus of resilin is about 1 MPa, of soft cuticles about 1 kPa to 50 MPa, of sclerotised cuticles 1-20 GPa; Vicker's Hardness of sclerotised cuticle ranges between 25 and 80 kgf mm(-2); density is 1-1.3 kg m(-3)-and one of its components, chitin nanofibres, the Young's modulus of which is more than 150 GPa. Experiments based on fracture mechanics have not been performed although the layered structure probably provides some toughening. The structural performance of wings and legs has been measured, but our understanding of the importance of buckling is lacking: it can stiffen the structure (by elastic postbuckling in wings, for example) or be a failure mode. We know nothing of fatigue properties (yet, for instance, the insect wing must undergo millions of cycles, flexing or buckling on each cycle). The remarkable mechanical performance and efficiency of cuticle can be analysed and compared with those of other materials using material property charts and material indices. Presented in this paper are four: Young's modulus-density (stiffness per unit weight), specific Young's modulus-specific strength (elastic hinges, elastic energy storage per unit weight), toughness-Young's modulus (fracture resistance under various loading conditions), and hardness (wear resistance). In conjunction with a structural analysis of cuticle these charts help to understand the relevance of microstructure (fibre orientation effects in tendons, joints and sense organs, for example) and shape (including surface structure) of this fibrous composite for a given function. With modern techniques for analysis of structure and material, and emphasis on nanocomposites and self-assembly, insect cuticle should be the archetype for composites at all levels of scale.
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            On the growth and form of the gut.

            The developing vertebrate gut tube forms a reproducible looped pattern as it grows into the body cavity. Here we use developmental experiments to eliminate alternative models and show that gut looping morphogenesis is driven by the homogeneous and isotropic forces that arise from the relative growth between the gut tube and the anchoring dorsal mesenteric sheet, tissues that grow at different rates. A simple physical mimic, using a differentially strained composite of a pliable rubber tube and a soft latex sheet is consistent with this mechanism and produces similar patterns. We devise a mathematical theory and a computational model for the number, size and shape of intestinal loops based solely on the measurable geometry, elasticity and relative growth of the tissues. The predictions of our theory are quantitatively consistent with observations of intestinal loops at different stages of development in the chick embryo. Our model also accounts for the qualitative and quantitative variation in the distinct gut looping patterns seen in a variety of species including quail, finch and mouse, illuminating how the simple macroscopic mechanics of differential growth drives the morphology of the developing gut.
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              Interplay of cell dynamics and epithelial tension during morphogenesis of the Drosophila pupal wing

              How tissue shape emerges from the collective mechanical properties and behavior of individual cells is not understood. We combine experiment and theory to study this problem in the developing wing epithelium of Drosophila. At pupal stages, the wing-hinge contraction contributes to anisotropic tissue flows that reshape the wing blade. Here, we quantitatively account for this wing-blade shape change on the basis of cell divisions, cell rearrangements and cell shape changes. We show that cells both generate and respond to epithelial stresses during this process, and that the nature of this interplay specifies the pattern of junctional network remodeling that changes wing shape. We show that patterned constraints exerted on the tissue by the extracellular matrix are key to force the tissue into the right shape. We present a continuum mechanical model that quantitatively describes the relationship between epithelial stresses and cell dynamics, and how their interplay reshapes the wing. DOI: http://dx.doi.org/10.7554/eLife.07090.001
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Genet
                PLoS Genet
                plos
                plosgen
                PLoS Genetics
                Public Library of Science (San Francisco, CA USA )
                1553-7390
                1553-7404
                11 January 2017
                January 2017
                : 13
                : 1
                Affiliations
                [1 ]Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa-shi, Chiba, Japan
                [2 ]Laboratory Research Support Section, Center for Cooperative Research Promotion, Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa-shi, Chiba, Japan
                New York University, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                • Conceptualization: RT TK.

                • Formal analysis: RT TK.

                • Funding acquisition: RT TK HF.

                • Investigation: RT NO.

                • Methodology: RT TK NO.

                • Project administration: RT TK.

                • Validation: RT TK HF.

                • Visualization: RT TK.

                • Writing – original draft: RT TK.

                • Writing – review & editing: RT TK HF NO.

                Article
                PGENETICS-D-16-01339
                10.1371/journal.pgen.1006548
                5226733
                28076349
                © 2017 Tajiri et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 11, Tables: 0, Pages: 26
                Product
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: JP15J40022
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100007428, Naito Foundation;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001700, Ministry of Education, Culture, Sports, Science, and Technology;
                Award ID: JP22128005
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001700, Ministry of Education, Culture, Sports, Science, and Technology;
                Award ID: JP20017007
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: JP24570230
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: JP11J06260
                Award Recipient :
                This work was supported by the Japan Society for the Promotion of Science Research Fellowship [15J40022] and grant from the Naito Foundation to RT, and Grants-in-Aid for Scientific Research (KAKENHI) to TK [24570230] and to HF [22128005, 20017007]. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Larvae
                Research and Analysis Methods
                Experimental Organism Systems
                Model Organisms
                Drosophila Melanogaster
                Research and Analysis Methods
                Model Organisms
                Drosophila Melanogaster
                Research and Analysis Methods
                Experimental Organism Systems
                Animal Models
                Drosophila Melanogaster
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Drosophila
                Drosophila Melanogaster
                Biology and Life Sciences
                Developmental Biology
                Metamorphosis
                Physical Sciences
                Chemistry
                Polymer Chemistry
                Macromolecules
                Polymers
                Chitin
                Physical Sciences
                Materials Science
                Materials by Structure
                Polymers
                Chitin
                Biology and Life Sciences
                Anatomy
                Integumentary System
                Skin
                Epidermis
                Medicine and Health Sciences
                Anatomy
                Integumentary System
                Skin
                Epidermis
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Pupae
                Medicine and Health Sciences
                Diagnostic Medicine
                Signs and Symptoms
                Dehydration (Medicine)
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Signs and Symptoms
                Dehydration (Medicine)
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Genetics

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