Development and ultrastructure of the rigid dorsal and flexible ventral cuticles of the elytron of the red flour beetle, Tribolium castaneum
Insect exoskeletons are composed of the cuticle, a biomaterial primarily formed from the linear and relatively rigid polysaccharide, chitin, and structural proteins. This extracellular material serves both as a skin and skeleton, protecting insects from environmental stresses and mechanical damage....
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description | Insect exoskeletons are composed of the cuticle, a biomaterial primarily formed from the linear and relatively rigid polysaccharide, chitin, and structural proteins. This extracellular material serves both as a skin and skeleton, protecting insects from environmental stresses and mechanical damage. Despite its rather limited compositional palette, cuticles in different anatomical regions or developmental stages exhibit remarkably diverse physicochemical and mechanical properties because of differences in chemical composition, molecular interactions and morphological architecture of the various layers and sublayers throughout the cuticle including the envelope, epicuticle and procuticle (exocuticle and endocuticle). Even though the ultrastructure of the arthropod cuticle has been studied rather extensively, its temporal developmental pattern, in particular, the synchronous development of the functional layers in different cuticles during a molt, is not well understood. The beetle elytron, which is a highly modified and sclerotized forewing, offers excellent advantages for such a study because it can be easily isolated at precise time points during development. In this study, we describe the morphogenesis of the dorsal and ventral cuticles of the elytron of the red flour beetle, Tribolium castaneum, during the period from the 0 d-old pupa to the 9 d-old adult. The deposition of exocuticle and mesocuticle is substantially different in the two cuticles. The dorsal cuticle is four-fold thicker than the ventral. Unlike the ventral cuticle, the dorsal contains a thicker exocuticle consisting of a large number of horizontal laminae and vertical pore canals with pore canal fibers and rib-like veins and bristles as well as a mesocuticle, lying right above the enodcuticle. The degree of sclerotization appears to be much greater in the dorsal cuticle. All of these differences result in a relatively thick and tanned rigid dorsal cuticle and a much thinner and less pigmented membrane-like ventral cuticle.
[Display omitted]
•Development of Tribolium elytral dorsal and ventral cuticles is asynchronous except at certain phases of deposition.•Exocuticle of the dorsal cuticle contains numerous horizontal laminae and vertical pore canals with chitin fibers.•Mesocuticle is present between the exocuticle and the endocuticle in the dorsal cuticle but not in the ventral cuticle.•Both dorsal and ventral cuticles contain an endocuticle consisting of a thick brick (macrofiber/Balken |
doi_str_mv | 10.1016/j.ibmb.2017.11.003 |
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[Display omitted]
•Development of Tribolium elytral dorsal and ventral cuticles is asynchronous except at certain phases of deposition.•Exocuticle of the dorsal cuticle contains numerous horizontal laminae and vertical pore canals with chitin fibers.•Mesocuticle is present between the exocuticle and the endocuticle in the dorsal cuticle but not in the ventral cuticle.•Both dorsal and ventral cuticles contain an endocuticle consisting of a thick brick (macrofiber/Balken)-type of laminae.•The dorsal cuticle is four-fold thicker and more sclerotized than the ventral.</description><identifier>ISSN: 0965-1748</identifier><identifier>EISSN: 1879-0240</identifier><identifier>DOI: 10.1016/j.ibmb.2017.11.003</identifier><identifier>PMID: 29117500</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Animal Shells - growth & development ; Animal Shells - ultrastructure ; Animals ; Chitin ; Cuticle/exoskeleton ; Elytron ; Pore canal ; Pupa - ultrastructure ; Transmission electron microscopy (TEM) ; Tribolium - growth & development ; Tribolium - ultrastructure ; Tribolium castaneum</subject><ispartof>Insect biochemistry and molecular biology, 2017-12, Vol.91, p.21-33</ispartof><rights>2017 Elsevier Ltd</rights><rights>Copyright © 2017 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c422t-b7652eed844b627ae6c41c0e437b208ba4407b1a086a2aeeada245cee782996e3</citedby><cites>FETCH-LOGICAL-c422t-b7652eed844b627ae6c41c0e437b208ba4407b1a086a2aeeada245cee782996e3</cites><orcidid>0000-0002-9538-1349</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.ibmb.2017.11.003$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29117500$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Noh, Mi Young</creatorcontrib><creatorcontrib>Muthukrishnan, Subbaratnam</creatorcontrib><creatorcontrib>Kramer, Karl J.</creatorcontrib><creatorcontrib>Arakane, Yasuyuki</creatorcontrib><title>Development and ultrastructure of the rigid dorsal and flexible ventral cuticles of the elytron of the red flour beetle, Tribolium castaneum</title><title>Insect biochemistry and molecular biology</title><addtitle>Insect Biochem Mol Biol</addtitle><description>Insect exoskeletons are composed of the cuticle, a biomaterial primarily formed from the linear and relatively rigid polysaccharide, chitin, and structural proteins. This extracellular material serves both as a skin and skeleton, protecting insects from environmental stresses and mechanical damage. Despite its rather limited compositional palette, cuticles in different anatomical regions or developmental stages exhibit remarkably diverse physicochemical and mechanical properties because of differences in chemical composition, molecular interactions and morphological architecture of the various layers and sublayers throughout the cuticle including the envelope, epicuticle and procuticle (exocuticle and endocuticle). Even though the ultrastructure of the arthropod cuticle has been studied rather extensively, its temporal developmental pattern, in particular, the synchronous development of the functional layers in different cuticles during a molt, is not well understood. The beetle elytron, which is a highly modified and sclerotized forewing, offers excellent advantages for such a study because it can be easily isolated at precise time points during development. In this study, we describe the morphogenesis of the dorsal and ventral cuticles of the elytron of the red flour beetle, Tribolium castaneum, during the period from the 0 d-old pupa to the 9 d-old adult. The deposition of exocuticle and mesocuticle is substantially different in the two cuticles. The dorsal cuticle is four-fold thicker than the ventral. Unlike the ventral cuticle, the dorsal contains a thicker exocuticle consisting of a large number of horizontal laminae and vertical pore canals with pore canal fibers and rib-like veins and bristles as well as a mesocuticle, lying right above the enodcuticle. The degree of sclerotization appears to be much greater in the dorsal cuticle. All of these differences result in a relatively thick and tanned rigid dorsal cuticle and a much thinner and less pigmented membrane-like ventral cuticle.
[Display omitted]
•Development of Tribolium elytral dorsal and ventral cuticles is asynchronous except at certain phases of deposition.•Exocuticle of the dorsal cuticle contains numerous horizontal laminae and vertical pore canals with chitin fibers.•Mesocuticle is present between the exocuticle and the endocuticle in the dorsal cuticle but not in the ventral cuticle.•Both dorsal and ventral cuticles contain an endocuticle consisting of a thick brick (macrofiber/Balken)-type of laminae.•The dorsal cuticle is four-fold thicker and more sclerotized than the ventral.</description><subject>Animal Shells - growth & development</subject><subject>Animal Shells - ultrastructure</subject><subject>Animals</subject><subject>Chitin</subject><subject>Cuticle/exoskeleton</subject><subject>Elytron</subject><subject>Pore canal</subject><subject>Pupa - ultrastructure</subject><subject>Transmission electron microscopy (TEM)</subject><subject>Tribolium - growth & development</subject><subject>Tribolium - ultrastructure</subject><subject>Tribolium castaneum</subject><issn>0965-1748</issn><issn>1879-0240</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kctu1DAUhi0EokPhBbqovGRBwrHHiROpm6pcpUpsytqynTPUIyee-jJi3oGHxsO0XbKydPR9_7H9E3LBoGXA-o_b1pnZtByYbBlrAdYvyIoNcmyAC3hJVjD2XcOkGM7Im5S2ACBEJ1-TMz4yJjuAFfnzCffow27GJVO9TLT4HHXKsdhcItKwofkeaXS_3ESnEJP2_7CNx9_OeKT7KsY6tCU76zE9GegPOYblOQCPTiiRGsTs8QO9i84E78pMbd2nFyzzW_Jqo33Cd4_nOfn55fPdzbfm9sfX7zfXt40VnOfGyL7jiNMghOm51NhbwSygWEvDYTBaCJCGaRh6zTWinjQXnUWUAx_HHtfn5P0pdxfDQ8GU1eySRe_rLUJJio09F2vWjWNF-Qm1MaQUcaN20c06HhQDdWxBbdWxBXVsQTGmagtVunzML2bG6Vl5-vYKXJ0ArK_cO4wqWYeLxclFtFlNwf0v_y9Ml5uA</recordid><startdate>201712</startdate><enddate>201712</enddate><creator>Noh, Mi Young</creator><creator>Muthukrishnan, Subbaratnam</creator><creator>Kramer, Karl J.</creator><creator>Arakane, Yasuyuki</creator><general>Elsevier Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-9538-1349</orcidid></search><sort><creationdate>201712</creationdate><title>Development and ultrastructure of the rigid dorsal and flexible ventral cuticles of the elytron of the red flour beetle, Tribolium castaneum</title><author>Noh, Mi Young ; Muthukrishnan, Subbaratnam ; Kramer, Karl J. ; Arakane, Yasuyuki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c422t-b7652eed844b627ae6c41c0e437b208ba4407b1a086a2aeeada245cee782996e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Animal Shells - growth & development</topic><topic>Animal Shells - ultrastructure</topic><topic>Animals</topic><topic>Chitin</topic><topic>Cuticle/exoskeleton</topic><topic>Elytron</topic><topic>Pore canal</topic><topic>Pupa - ultrastructure</topic><topic>Transmission electron microscopy (TEM)</topic><topic>Tribolium - growth & development</topic><topic>Tribolium - ultrastructure</topic><topic>Tribolium castaneum</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Noh, Mi Young</creatorcontrib><creatorcontrib>Muthukrishnan, Subbaratnam</creatorcontrib><creatorcontrib>Kramer, Karl J.</creatorcontrib><creatorcontrib>Arakane, Yasuyuki</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Insect biochemistry and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Noh, Mi Young</au><au>Muthukrishnan, Subbaratnam</au><au>Kramer, Karl J.</au><au>Arakane, Yasuyuki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Development and ultrastructure of the rigid dorsal and flexible ventral cuticles of the elytron of the red flour beetle, Tribolium castaneum</atitle><jtitle>Insect biochemistry and molecular biology</jtitle><addtitle>Insect Biochem Mol Biol</addtitle><date>2017-12</date><risdate>2017</risdate><volume>91</volume><spage>21</spage><epage>33</epage><pages>21-33</pages><issn>0965-1748</issn><eissn>1879-0240</eissn><abstract>Insect exoskeletons are composed of the cuticle, a biomaterial primarily formed from the linear and relatively rigid polysaccharide, chitin, and structural proteins. This extracellular material serves both as a skin and skeleton, protecting insects from environmental stresses and mechanical damage. Despite its rather limited compositional palette, cuticles in different anatomical regions or developmental stages exhibit remarkably diverse physicochemical and mechanical properties because of differences in chemical composition, molecular interactions and morphological architecture of the various layers and sublayers throughout the cuticle including the envelope, epicuticle and procuticle (exocuticle and endocuticle). Even though the ultrastructure of the arthropod cuticle has been studied rather extensively, its temporal developmental pattern, in particular, the synchronous development of the functional layers in different cuticles during a molt, is not well understood. The beetle elytron, which is a highly modified and sclerotized forewing, offers excellent advantages for such a study because it can be easily isolated at precise time points during development. In this study, we describe the morphogenesis of the dorsal and ventral cuticles of the elytron of the red flour beetle, Tribolium castaneum, during the period from the 0 d-old pupa to the 9 d-old adult. The deposition of exocuticle and mesocuticle is substantially different in the two cuticles. The dorsal cuticle is four-fold thicker than the ventral. Unlike the ventral cuticle, the dorsal contains a thicker exocuticle consisting of a large number of horizontal laminae and vertical pore canals with pore canal fibers and rib-like veins and bristles as well as a mesocuticle, lying right above the enodcuticle. The degree of sclerotization appears to be much greater in the dorsal cuticle. All of these differences result in a relatively thick and tanned rigid dorsal cuticle and a much thinner and less pigmented membrane-like ventral cuticle.
[Display omitted]
•Development of Tribolium elytral dorsal and ventral cuticles is asynchronous except at certain phases of deposition.•Exocuticle of the dorsal cuticle contains numerous horizontal laminae and vertical pore canals with chitin fibers.•Mesocuticle is present between the exocuticle and the endocuticle in the dorsal cuticle but not in the ventral cuticle.•Both dorsal and ventral cuticles contain an endocuticle consisting of a thick brick (macrofiber/Balken)-type of laminae.•The dorsal cuticle is four-fold thicker and more sclerotized than the ventral.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>29117500</pmid><doi>10.1016/j.ibmb.2017.11.003</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-9538-1349</orcidid></addata></record> |
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subjects | Animal Shells - growth & development Animal Shells - ultrastructure Animals Chitin Cuticle/exoskeleton Elytron Pore canal Pupa - ultrastructure Transmission electron microscopy (TEM) Tribolium - growth & development Tribolium - ultrastructure Tribolium castaneum |
title | Development and ultrastructure of the rigid dorsal and flexible ventral cuticles of the elytron of the red flour beetle, Tribolium castaneum |
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