Precocious metamorphosis in the juvenile hormone-deficient mutant of the silkworm, Bombyx mori

Takaaki Daimon, Toshinori Kozaki, Ryusuke Niwa, Isao Kobayashi, Kenjiro Furuta, Toshiki Namiki, Keiro Uchino, Yutaka Banno, Susumu Katsuma, Toshiki Tamura, Kazuei Mita, Hideki Sezutsu, Masayoshi Nakayama, Kyo Itoyama, Toru Shimada, Tetsuro Shinoda

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87 Citations (Scopus)

Abstract

Insect molting and metamorphosis are intricately governed by two hormones, ecdysteroids and juvenile hormones (JHs). JHs prevent precocious metamorphosis and allow the larva to undergo multiple rounds of molting until it attains the proper size for metamorphosis. In the silkworm, Bombyx mori, several "moltinism" mutations have been identified that exhibit variations in the number of larval molts; however, none of them have been characterized molecularly. Here we report the identification and characterization of the gene responsible for the dimolting (mod) mutant that undergoes precocious metamorphosis with fewer larval-larval molts. We show that the mod mutation results in complete loss of JHs in the larval hemolymph and that the mutant phenotype can be rescued by topical application of a JH analog. We performed positional cloning of mod and found a null mutation in the cytochrome P450 gene CYP15C1 in the mod allele. We also demonstrated that CYP15C1 is specifically expressed in the corpus allatum, an endocrine organ that synthesizes and secretes JHs. Furthermore, a biochemical experiment showed that CYP15C1 epoxidizes farnesoic acid to JH acid in a highly stereospecific manner. Precocious metamorphosis of mod larvae was rescued when the wild-type allele of CYP15C1 was expressed in transgenic mod larvae using the GAL4/UAS system. Our data therefore reveal that CYP15C1 is the gene responsible for the mod mutation and is essential for JH biosynthesis. Remarkably, precocious larval-pupal transition in mod larvae does not occur in the first or second instar, suggesting that authentic epoxidized JHs are not essential in very young larvae of B. mori. Our identification of a JH-deficient mutant in this model insect will lead to a greater understanding of the molecular basis of the hormonal control of development and metamorphosis.

Original languageEnglish
Article numbere1002486
JournalPLoS genetics
Volume8
Issue number3
DOIs
Publication statusPublished - Mar 1 2012

All Science Journal Classification (ASJC) codes

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

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    Daimon, T., Kozaki, T., Niwa, R., Kobayashi, I., Furuta, K., Namiki, T., Uchino, K., Banno, Y., Katsuma, S., Tamura, T., Mita, K., Sezutsu, H., Nakayama, M., Itoyama, K., Shimada, T., & Shinoda, T. (2012). Precocious metamorphosis in the juvenile hormone-deficient mutant of the silkworm, Bombyx mori. PLoS genetics, 8(3), [e1002486]. https://doi.org/10.1371/journal.pgen.1002486