The FOXO transcription factor controls insect growth and development by regulating juvenile hormone degradation in the silkworm, Bombyx mori

May 12, 2017The Journal of biological chemistry

The FOXO protein controls silkworm growth by managing juvenile hormone breakdown

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Abstract

Mutants of silkworm FOXO exhibited growth delays and precocious metamorphosis, pupating earlier than wild-type animals.

The FOXO mutant (FOXO-M) pupated after the fourth instar instead of the fifth, indicating altered developmental timing.
Total larval developmental time in FOXO-M was similar to that of wild-type animals despite the early pupation.
Application of 20-hydroxyecdysone or a juvenile hormone analog reversed the trimolter phenotype in FOXO-M.
Gene expression analysis revealed up-regulation of genes involved in juvenile hormone degradation in FOXO-M.
FOXO was found to bind to the promoters of genes coding for enzymes that degrade juvenile hormone.

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Forkhead box O (FOXO) functions as the terminal transcription factor of the insulin signaling pathway and regulates multiple physiological processes in many organisms, including lifespan in insects. However, how FOXO interacts with hormone signaling to modulate insect growth and development is largely unknown. Here, using the transgene-based CRISPR/Cas9 system, we generated and characterized mutants of the silkwormFOXO () to elucidate its physiological functions during development of this lepidopteran insect. Themutant (FOXO-M) exhibited growth delays from the first larval stage and showed precocious metamorphosis, pupating at the end of the fourth instar (trimolter) rather than at the end of the fifth instar as in the wild-type (WT) animals. However, different from previous reports on precocious metamorphosis caused by juvenile hormone (JH) deficiency in silkworm mutants, the total developmental time of the larval period in the FOXO-M was comparable with that of the WT. Exogenous application of 20-hydroxyecdysone (20E) or of the JH analog rescued the trimolter phenotype. RNA-seq and gene expression analyses indicated that genes involved in JH degradation but not in JH biosynthesis were up-regulated in the FOXO-M compared with the WT animals. Moreover, we identified several FOXO-binding sites in the promoter of genes coding for JH-degradation enzymes. These results suggest that FOXO regulates JH degradation rather than its biosynthesis, which further modulates hormone homeostasis to control growth and development inIn conclusion, we have uncovered a pivotal role for FOXO in regulating JH signaling to control insect development. Bombyx mori BmFOXO BmFOXO B. mori

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The FOXO transcription factor controls insect growth and development by regulating juvenile hormone degradation in the silkworm, Bombyx mori

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