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Egg envelopes and cuticle renewal in Porcellio embryos and marsupial mancas

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      Abstract

      AbstractAn important adaptation to land habitats in terrestrial isopod crustaceans is development of embryos in a fluid-filled female brood pouch, marsupium. The study brings insight into the structure and protective role of egg envelopes and cuticle renewal during ontogenetic development of Porcellio embryos and marsupial mancas. Egg envelopes cover embryos, the outer chorion until late-stage embryo and the inner vitelline membrane throughout the whole embryonic development. Egg envelopes of Porcellio have relatively simple ultrastuctural architecture compared to Drosophila egg envelopes. Exoskeletal cuticle is produced in late embryonic development by hypodermal cells of the embryo and is renewed in further development in relation to growth of developing embryos and mancas. Cuticle structure and renewal in prehatching late-stage embryos and marsupial mancas exhibit main features of cuticle in adults. Epicuticle is thin and homogenous. The characteristic arrangement of chitin-protein fibers and the dense distal layer in exocuticle are hardly discernible in prehatching embryo and distinct in marsupial mancas. Endocuticle consists of alternating electron dense and electron lucent sublayers and is perforated by pore canals in both stages. Differences from adult cuticle are evident in cuticle thickness, ultrastructure and mineralization. Signs of cuticle renewal in prehatching embryo and marsupial mancas such as detachment of cuticle from hypodermis, partial disintegration of endocuticle and assembly of new cuticle are described.

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      Recent advances in understanding mechanisms of insect cuticle differentiation.

      Insects possess a cuticle that covers all tissues exposed to the outside world including the body, the fore- and hindgut and the luminal side of the tracheae. The cuticle is a multifunctional device that protects its carriers against dehydration, arms them against predators, constitutes a physical barrier to prevent pathogen entry and serves as an exoskeleton allowing locomotion. Depending the developmental stage and the body part, the composition and function of the cuticle changes. The body cuticle of larvae of holometabolous insects for example is soft while their cuticular head skeletons used to chew food is hard. In spite of these differences, the basic architecture of the insect cuticle is evolutionarily well conserved between developmental stages and between species. The insect larval cuticle is formed at the apical site of a monolayer of polarised epithelial cells that differentiate concomitantly during embryogenesis. The stratified structure of the cuticle results from the concerted unfolding of basic cellular functions including timed transcription, biosynthetic enzymatic cascades, secretion and membrane trafficking as well as elaborate extracellular self-organization of the components. The aim of this review is to summarize recent advances in understanding these processes. Copyright 2010 Elsevier Ltd. All rights reserved.
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        Cuticle differentiation during Drosophila embryogenesis.

        The constitutive criterion for the evolutionary successful clade of ecdysozoans is a protective exoskeleton. In insects the exoskeleton, the so-called cuticle consists of three functional layers, the waterproof envelope, the proteinaceous epicuticle and the chitinous procuticle that are produced as an extracellular matrix by the underlying epidermal cells. Here, we present our electron-microscopic study of cuticle differentiation during embryogenesis in the fruit fly Drosophila melanogaster. We conclude that cuticle differentiation in the Drosophila embryo occurs in three phases. In the first phase, the layers are established. Interestingly, we find that establishment of the layers occurs partially simultaneously rather than in a strict sequential manner as previously proposed. In the second phase the cuticle thickens. Finally, in the third phase, when secretion of cuticle material has ceased, the chitin laminae acquire their typical orientation, and the epicuticle of the denticles and the head skeleton darken. Our work will help to understand the phenotypes of embryos mutant for genes encoding essential cuticle factors, in turn revealing mechanisms of cuticle differentiation.
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          Spatial distribution of calcite and amorphous calcium carbonate in the cuticle of the terrestrial crustaceans Porcellio scaber and Armadillidium vulgare.

          The crustacean cuticle is an interesting model to study the properties of mineralized bio-composites. The cuticle consists of an organic matrix composed of chitin-protein fibres associated with various amounts of crystalline and amorphous calcium carbonate. It is thought that in isopods the relative amounts of these mineral polymorphs depend on its function and the habitat of the animal. In addition to the composition, the distribution of the various components should affect the properties of the cuticle. However, the spatial distribution of calcium carbonate polymorphs within the crustacean cuticle is unknown. Therefore, we analyzed the mineralized cuticles of the terrestrial isopods Armadillidium vulgare and Porcellio scaber using scanning electron-microscopy, electron probe microanalysis and confocal mu-Raman spectroscopic imaging. We show for the first time that the mineral phases are arranged in distinct layers. Calcite is restricted to the outer layer of the cuticle that corresponds to the exocuticle. Amorphous calcium carbonate is located within the endocuticle that lies below the exocuticle. Within both layers mineral is arranged in rows of granules with diameters of about 20 nm. The results suggest functional implications of mineral distribution that accord to the moulting and escape behaviour of the animals.
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            Author and article information

            Affiliations
            [1 ]Department of Biology, Biotehnical faculty, University of Ljubljana, Večna pot 111, SI-1000 Ljubljana, Slovenia
            [2 ]Department of Ultrastructural Research, University of Vienna, Althanstrasse 14,  A-1090 Vienna, Austria
            Author notes
            Corresponding author: Polona Mrak ( polona.mrak@ 123456bf.uni-lj.si )

            Academic editor: S. Sfenthouraki

            Journal
            Zookeys
            Zookeys
            ZooKeys
            ZooKeys
            Pensoft Publishers
            1313-2989
            1313-2970
            2012
            20 March 2012
            : 176
            : 55-72
            3335405
            22536099
            10.3897/zookeys.176.2418
            Polona Mrak, Nada Žnidaršič, Magda Tušek-Žnidarič, Waltraud Klepal, Daniela Gruber, Jasna Štrus

            This is an open access article distributed under the terms of the Creative Commons Attribution License 3.0 (CC-BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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