Accessory gland as a site for prothoracicotropic hormone controlled ecdysone synthesis in adult male insects

Julie Lilith Hentze, Meghan S Bengtsson, James Warren, Lawrence Gilbert, Ole Andersen, Kim Furbo Rewitz, Morten Erik Møller, Anne Færch Jørgensen, Anna Maria Borðoy

    Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

    Resumé

    Insect steroid hormones (ecdysteroids) are important for female reproduction in many insect species and are required for the initiation and coordination of vital developmental processes. Ecdysteroids are also important for adult male physiology and behavior, but their exact function and site of synthesis remains unclear, although previous studies suggest that the reproductive system may be their source. We have examined expression profiles of the ecdysteroidogenic Halloween genes, during development and in adults of the flour beetle Tribolium castaneum. Genes required for the biosynthesis of ecdysone (E), the precursor of the molting hormone 20-hydroxyecdysone (20E), are expressed in the tubular accessory glands (TAGs) of adult males. In contrast, expression of the gene encoding the enzyme mediating 20E synthesis was detected in the ovaries of females. Further, Spookiest (Spot), an enzyme presumably required for endowing tissues with competence to produce ecdysteroids, is male specific and predominantly expressed in the TAGs. We also show that prothoracicotropic hormone (PTTH), a regulator of E synthesis during larval development, regulates ecdysteroid levels in the adult stage in Drosophila melanogaster and the gene for its receptor Torso seems to be expressed specifically in the accessory glands of males. The composite results suggest strongly that the accessory glands of adult male insects are the main source of E, but not 20E. The finding of a possible male-specific source of E raises the possibility that E and 20E have sex-specific roles analogous to the vertebrate sex steroids, where males produce primarily testosterone, the precursor of estradiol. Furthermore this study provides the first evidence that PTTH regulates ecdysteroid synthesis in the adult stage and could explain the original finding that some adult insects are a rich source of PTTH.
    OriginalsprogEngelsk
    TidsskriftP L o S One
    Vol/bind8/2
    Udgave nummere55131
    ISSN1932-6203
    DOI
    StatusUdgivet - 1 feb. 2013

    Citer dette

    Hentze, J. L., Bengtsson, M. S., Warren, J., Gilbert, L., Andersen, O., Rewitz, K. F., ... Borðoy, A. M. (2013). Accessory gland as a site for prothoracicotropic hormone controlled ecdysone synthesis in adult male insects. P L o S One, 8/2(e55131). https://doi.org/10.1371/journal.pone.0055131
    Hentze, Julie Lilith ; Bengtsson, Meghan S ; Warren, James ; Gilbert, Lawrence ; Andersen, Ole ; Rewitz, Kim Furbo ; Møller, Morten Erik ; Færch Jørgensen, Anne ; Borðoy, Anna Maria. / Accessory gland as a site for prothoracicotropic hormone controlled ecdysone synthesis in adult male insects. I: P L o S One. 2013 ; Bind 8/2, Nr. e55131.
    @article{975effaaac944a2f9013b777f50fdb89,
    title = "Accessory gland as a site for prothoracicotropic hormone controlled ecdysone synthesis in adult male insects",
    abstract = "Insect steroid hormones (ecdysteroids) are important for female reproduction in many insect species and are required for the initiation and coordination of vital developmental processes. Ecdysteroids are also important for adult male physiology and behavior, but their exact function and site of synthesis remains unclear, although previous studies suggest that the reproductive system may be their source. We have examined expression profiles of the ecdysteroidogenic Halloween genes, during development and in adults of the flour beetle Tribolium castaneum. Genes required for the biosynthesis of ecdysone (E), the precursor of the molting hormone 20-hydroxyecdysone (20E), are expressed in the tubular accessory glands (TAGs) of adult males. In contrast, expression of the gene encoding the enzyme mediating 20E synthesis was detected in the ovaries of females. Further, Spookiest (Spot), an enzyme presumably required for endowing tissues with competence to produce ecdysteroids, is male specific and predominantly expressed in the TAGs. We also show that prothoracicotropic hormone (PTTH), a regulator of E synthesis during larval development, regulates ecdysteroid levels in the adult stage in Drosophila melanogaster and the gene for its receptor Torso seems to be expressed specifically in the accessory glands of males. The composite results suggest strongly that the accessory glands of adult male insects are the main source of E, but not 20E. The finding of a possible male-specific source of E raises the possibility that E and 20E have sex-specific roles analogous to the vertebrate sex steroids, where males produce primarily testosterone, the precursor of estradiol. Furthermore this study provides the first evidence that PTTH regulates ecdysteroid synthesis in the adult stage and could explain the original finding that some adult insects are a rich source of PTTH.",
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    Hentze, JL, Bengtsson, MS, Warren, J, Gilbert, L, Andersen, O, Rewitz, KF, Møller, ME, Færch Jørgensen, A & Borðoy, AM 2013, 'Accessory gland as a site for prothoracicotropic hormone controlled ecdysone synthesis in adult male insects', P L o S One, bind 8/2, nr. e55131. https://doi.org/10.1371/journal.pone.0055131

    Accessory gland as a site for prothoracicotropic hormone controlled ecdysone synthesis in adult male insects. / Hentze, Julie Lilith; Bengtsson, Meghan S; Warren, James ; Gilbert, Lawrence ; Andersen, Ole; Rewitz, Kim Furbo; Møller, Morten Erik; Færch Jørgensen, Anne; Borðoy, Anna Maria.

    I: P L o S One, Bind 8/2, Nr. e55131, 01.02.2013.

    Publikation: Bidrag til tidsskriftTidsskriftartikelForskningpeer review

    TY - JOUR

    T1 - Accessory gland as a site for prothoracicotropic hormone controlled ecdysone synthesis in adult male insects

    AU - Hentze, Julie Lilith

    AU - Bengtsson, Meghan S

    AU - Warren, James

    AU - Gilbert, Lawrence

    AU - Andersen, Ole

    AU - Rewitz, Kim Furbo

    AU - Møller, Morten Erik

    AU - Færch Jørgensen, Anne

    AU - Borðoy, Anna Maria

    PY - 2013/2/1

    Y1 - 2013/2/1

    N2 - Insect steroid hormones (ecdysteroids) are important for female reproduction in many insect species and are required for the initiation and coordination of vital developmental processes. Ecdysteroids are also important for adult male physiology and behavior, but their exact function and site of synthesis remains unclear, although previous studies suggest that the reproductive system may be their source. We have examined expression profiles of the ecdysteroidogenic Halloween genes, during development and in adults of the flour beetle Tribolium castaneum. Genes required for the biosynthesis of ecdysone (E), the precursor of the molting hormone 20-hydroxyecdysone (20E), are expressed in the tubular accessory glands (TAGs) of adult males. In contrast, expression of the gene encoding the enzyme mediating 20E synthesis was detected in the ovaries of females. Further, Spookiest (Spot), an enzyme presumably required for endowing tissues with competence to produce ecdysteroids, is male specific and predominantly expressed in the TAGs. We also show that prothoracicotropic hormone (PTTH), a regulator of E synthesis during larval development, regulates ecdysteroid levels in the adult stage in Drosophila melanogaster and the gene for its receptor Torso seems to be expressed specifically in the accessory glands of males. The composite results suggest strongly that the accessory glands of adult male insects are the main source of E, but not 20E. The finding of a possible male-specific source of E raises the possibility that E and 20E have sex-specific roles analogous to the vertebrate sex steroids, where males produce primarily testosterone, the precursor of estradiol. Furthermore this study provides the first evidence that PTTH regulates ecdysteroid synthesis in the adult stage and could explain the original finding that some adult insects are a rich source of PTTH.

    AB - Insect steroid hormones (ecdysteroids) are important for female reproduction in many insect species and are required for the initiation and coordination of vital developmental processes. Ecdysteroids are also important for adult male physiology and behavior, but their exact function and site of synthesis remains unclear, although previous studies suggest that the reproductive system may be their source. We have examined expression profiles of the ecdysteroidogenic Halloween genes, during development and in adults of the flour beetle Tribolium castaneum. Genes required for the biosynthesis of ecdysone (E), the precursor of the molting hormone 20-hydroxyecdysone (20E), are expressed in the tubular accessory glands (TAGs) of adult males. In contrast, expression of the gene encoding the enzyme mediating 20E synthesis was detected in the ovaries of females. Further, Spookiest (Spot), an enzyme presumably required for endowing tissues with competence to produce ecdysteroids, is male specific and predominantly expressed in the TAGs. We also show that prothoracicotropic hormone (PTTH), a regulator of E synthesis during larval development, regulates ecdysteroid levels in the adult stage in Drosophila melanogaster and the gene for its receptor Torso seems to be expressed specifically in the accessory glands of males. The composite results suggest strongly that the accessory glands of adult male insects are the main source of E, but not 20E. The finding of a possible male-specific source of E raises the possibility that E and 20E have sex-specific roles analogous to the vertebrate sex steroids, where males produce primarily testosterone, the precursor of estradiol. Furthermore this study provides the first evidence that PTTH regulates ecdysteroid synthesis in the adult stage and could explain the original finding that some adult insects are a rich source of PTTH.

    U2 - 10.1371/journal.pone.0055131

    DO - 10.1371/journal.pone.0055131

    M3 - Journal article

    VL - 8/2

    JO - P L o S One

    JF - P L o S One

    SN - 1932-6203

    IS - e55131

    ER -