TGF-β signaling in insects regulates metamorphosis via juvenile hormone biosynthesis

Yoshiyasu Ishimaru, Sayuri Tomonari, Yuji Matsuoka, Takahito Watanabe, Katsuyuki Miyawaki, Tetsuya Bando, Kenji Tomioka, Hideyo Ohuchi, Sumihare Noji, Taro Mito

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

Although butterflies undergo a dramatic morphological transformation from larva to adult via a pupal stage (holometamorphosis), crickets undergo a metamorphosis from nymph to adult without formation of a pupa (hemimetamorphosis). Despite these differences, both processes are regulated by common mechanisms that involve 20-hydroxyecdysone (20E) and juvenile hormone (JH). JH regulates many aspects of insect physiology, such as development, reproduction, diapause, and metamorphosis. Consequently, strict regulation of JH levels is crucial throughout an insect's life cycle. However, it remains unclear how JH synthesis is regulated. Here, we report that in the corpora allata of the cricket, Gryllus bimaculatus, Myoglianin (Gb'Myo), a homolog of Drosophila Myoglianin/vertebrate GDF8/11, is involved in the down-regulation of JH production by suppressing the expression of a gene encoding JH acid O-methyltransferase, Gb'jhamt. In contrast, JH production is up-regulated by Decapentaplegic (Gb'Dpp) and Glass-bottom boat/60A (Gb'Gbb) signaling that occurs as part of the transcriptional activation of Gb'jhamt. Gb'Myo defines the nature of each developmental transition by regulating JH titer and the interactions between JH and 20E. When Gb'myo expression is suppressed, the activation of Gb'jhamt expression and secretion of 20E induce molting, thereby leading to the next instar before the last nymphal instar. Conversely, high Gb'myo expression induces metamorphosis during the last nymphal instar through the cessation of JH synthesis. Gb'myo also regulates final insect size. Because Myo/GDF8/11 and Dpp/bone morphogenetic protein (BMP)2/4-Gbb/BMP5-8 are conserved in both invertebrates and vertebrates, the present findings provide common regulatory mechanisms for endocrine control of animal development.

Original languageEnglish
Pages (from-to)5634-5639
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number20
DOIs
Publication statusPublished - May 17 2016

Fingerprint

Juvenile Hormones
Insects
Gryllidae
Vertebrates
Corpora Allata
Bone Morphogenetic Protein 4
Ecdysterone
Molting
Nymph
Bone Morphogenetic Protein 2
Butterflies
Pupa
Ships
Methyltransferases
Invertebrates
Life Cycle Stages
Transcriptional Activation
Drosophila
Glass
Reproduction

Keywords

  • GDF8/11
  • Gryllus bimaculatus
  • Juvenile hormone
  • Metamorphosis
  • RNA interference

ASJC Scopus subject areas

  • General

Cite this

TGF-β signaling in insects regulates metamorphosis via juvenile hormone biosynthesis. / Ishimaru, Yoshiyasu; Tomonari, Sayuri; Matsuoka, Yuji; Watanabe, Takahito; Miyawaki, Katsuyuki; Bando, Tetsuya; Tomioka, Kenji; Ohuchi, Hideyo; Noji, Sumihare; Mito, Taro.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 113, No. 20, 17.05.2016, p. 5634-5639.

Research output: Contribution to journalArticle

Ishimaru, Yoshiyasu ; Tomonari, Sayuri ; Matsuoka, Yuji ; Watanabe, Takahito ; Miyawaki, Katsuyuki ; Bando, Tetsuya ; Tomioka, Kenji ; Ohuchi, Hideyo ; Noji, Sumihare ; Mito, Taro. / TGF-β signaling in insects regulates metamorphosis via juvenile hormone biosynthesis. In: Proceedings of the National Academy of Sciences of the United States of America. 2016 ; Vol. 113, No. 20. pp. 5634-5639.
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