Juvenile Hormone Is Required to Couple Imaginal Disc Formation with Nutrition in Insects

Faculty of Agriculture and Life Sciences, Hirosaki University, Khirosaki, Aomori, Japan
Science (Impact Factor: 33.61). 07/2006; 312(5778):1385-8. DOI: 10.1126/science.1123652
Source: PubMed


In starved larvae of the tobacco hornworm moth Manduca sexta, larval and imaginal tissues stop growing, the former because they lack nutrient-dependent signals but the latter because
of suppression by juvenile hormone. Without juvenile hormone, imaginal discs form and grow despite severe starvation. This
hormone inhibits the intrinsic signaling needed for disc morphogenesis and does so independently of ecdysteroid action. Starvation
and juvenile hormone treatments allowed the separation of intrinsic and nutrient-dependent aspects of disc growth and showed
that both aspects must occur during the early phases of disc morphogenesis to ensure normal growth leading to typical-sized

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    • "Its classic roles are to ensure a stationary molt when titers are high (Mutti et al., 2011; Jindra et al., 2013; Restrepo et al., 2014) and to regulate developmental switches between alternative phenotypes (Nijhout, 1994). But JH can also stimulate cell proliferation (Truman et al., 2006; Mutti et al., 2011; Jindra et al., 2013; Restrepo et al., 2014) and link trait growth with nutrition (Emlen et al., 2005; Truman et al., 2006; Tang et al., 2011; Mirth and Shingleton 2012). Perturbations to JH affect the size of a number of condition-dependent insect traits including eyestalks of stalk-eyed flies (Cotton et al., 2004; Fry, 2006), mandibles of stag beetles (Gotoh et al., 2011) and broadhorned flour beetles (Okada et al., 2006), and horns of dung beetles (Emlen and Nijhout, 1999; Shelby et al., 2007). "
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    ABSTRACT: Insects exhibit a diversity of environmentally sensitive phenotypes that allow them to be an extraordinarily successful group. For example, mandible size in male stag beetles is exquisitely sensitive to the larval nutritional environment and is a reliable signal of male condition. To date, studies of how such phenotypically plastic traits develop have focused on two types of mechanistic processes. Local, tissue-specific genetic mechanisms specify the shape and approximate final size of structures, whereas whole-animal hormonal signaling mechanisms modulate trait growth in response to environmental circumstance, including the body size and nutritional state of each individual. Hormones such as juvenile hormone, ecdysteroids, and/or ligands of the insulin-signaling pathway specify whether traits grow and regulate how much growth occurs across a diversity of insect groups. What remains to be shown is how the local, tissue-specific developmental genetic pathways interact with these whole animal hormonal signaling pathways during development to yield phenotypically plastic patterns of trait growth. Because the Fat/Hippo signaling pathway coordinates trait growth and development through its interactions with morphogens and hormonal pathways, we propose that Fat/Hippo signaling is a missing mechanistic link coordinating environmentally sensitive trait development in insects. This article is protected by copyright. All rights reserved. © 2015 Wiley Periodicals, Inc.
    Developmental Dynamics 05/2015; 244(9). DOI:10.1002/dvdy.24296 · 2.38 Impact Factor
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    • "Starvation represses the growth of the wing discs, and eye and leg primordia (Macwhinnie et al., 2005; Truman et al., 2006). Eliminating JH by removing the CA partially restores disc growth even in starved larvae (Truman et al., 2006). The effects of JH on tissue growth are overridden by insulin; wing discs cultured in the presence of JH alone show reduced growth whereas when they are cultured with JH and insulin, growth rates are restored (Koyama et al., 2008). "
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    ABSTRACT: Nutrition, via the insulin/insulin-like growth factor (IIS)/Target of Rapamycin (TOR) signaling pathway, can provide a strong molding force for determining animal size and shape. For instance, nutrition induces a disproportionate increase in the size of male horns in dung and rhinoceros beetles, or mandibles in staghorn or horned flour beetles, relative to body size. In these species, well-fed male larvae produce adults with greatly enlarged horns or mandibles, whereas males that are starved or poorly fed as larvae bear much more modest appendages. Changes in IIS/TOR signaling plays a key role in appendage development by regulating growth in the horn and mandible primordia. In contrast, changes in the IIS/TOR pathway produce minimal effects on the size of other adult structures, such as the male genitalia in fruit flies and dung beetles. The horn, mandible and genitalia illustrate that although all tissues are exposed to the same hormonal environment within the larval body, the extent to which insulin can induce growth is organ specific. In addition, the IIS/TOR pathway affects body size and shape by controlling production of metamorphic hormones important for regulating developmental timing, like the steroid molting hormone ecdysone and sesquiterpenoid hormone juvenile hormone. In this review, we discuss recent results from Drosophila and other insects that highlight mechanisms allowing tissues to differ in their sensitivity to IIS/TOR and the potential consequences of these differences on body size and shape.
    Frontiers in Physiology 09/2013; 4:263. DOI:10.3389/fphys.2013.00263 · 3.53 Impact Factor
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    • "At the beginning of the final larval instar, wing discs are committed to initiate larval-pupal development. Juvenile hormone (JH) prevents this commitment in earlier instars and in starved final instar larvae, but nutrient intake overcomes this effect of JH in the latter (Truman et al., 2006). "
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    ABSTRACT: A quarter of a century has passed since bombyxin, the first insulin-like peptide identified in insects, was discovered in the silkmoth Bombyx mori. During these years, bombyxin has been studied for its structure, genes, distribution, hemolymph titers, secretion control, as well as physiological functions, thereby stimulating a wide range of studies on insulin-like peptides in other insects. Moreover, recent studies have identified a new class of insulin family peptides, IGF-like peptides, in B. mori and Drosophila melanogaster, broadening the base of the research area of the insulin-related peptides in insects. In this review, we describe the achievements of the studies on insulin-like and IGF-like peptides mainly in B. mori with short histories of their discovery. Our emphasis is that bombyxins, secreted by the brain neurosecretory cells, regulate nutrient-dependent growth and metabolism, whereas the IGF-like peptides, secreted by the fat body and other peripheral tissues, regulate stage-dependent growth of tissues.
    Frontiers in Physiology 08/2013; 4:217. DOI:10.3389/fphys.2013.00217 · 3.53 Impact Factor
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