Involvement of Taiman in juvenile hormone signaling controlling sexual maturation in a male moth

TL;DR

This study shows that the Taiman protein helps juvenile hormone regulate sexual maturation in male moths by influencing behavior and gland development.

Contribution

The study identifies Taiman as a mediator of juvenile hormone signaling in the regulation of sexual maturation in male moths.

Findings

Taiman expression in ALs and ASGs increases with sexual maturity in male moths.

Taiman silencing reduces sexual behavior and delays ASG development in older males.

Taiman positively regulates Kr-h1, linking juvenile hormone signaling to sexual maturation.

Abstract

•Tai mRNAs in ALs and ASGs are at higher levels in sexually mature old males than in sexually immature young males.•Tai silencing in old males causes a decrease in sexual behavior.•Tai-deficient older males exhibit delayed ASG development.•JH deprivation by allatectomy results in a reduction of Tai expression in ALs and ASGs.•Tai is a mediator of JH actions through a positive regulation of Kr-h1.

Tai mRNAs in ALs and ASGs are at higher levels in sexually mature old males than in sexually immature young males.

Tai silencing in old males causes a decrease in sexual behavior.

Tai-deficient older males exhibit delayed ASG development.

JH deprivation by allatectomy results in a reduction of Tai expression in ALs and ASGs.

Tai is a mediator of JH actions through a positive regulation of Kr-h1.

In insects, juvenile hormone (JH) is essential for orchestrating reproductive events. For example, in the male moth Agrotis ipsilon, the behavioral response to female sex pheromone is linked to neuronal sensitivity in the primary olfactory centers (antennal lobes, ALs), and the maturation of accessory sex glands (ASGs) are known to be age- and JH-dependent. The molecular basis of this regulatory action of JH is not fully deciphered, and we show here that the heterodimerizing partner of Methoprene-tolerant called Taiman (Tai) is essential for the sexual maturation of male A. ipsilon. Tai expression in ALs and ASGs is elevated from the third day of adult life and is responsible for the acquisition of behavioral responsiveness to the sex pheromone and ASG maturation. Tai-deficient old males exhibited altered sexual behavior and delayed ASG maturation. Moreover, the expression levels of Tai and Krüppel homolog 1 (Kr-h1), an early JH-induced transcription factor, were reduced in ALs and ASGs of JH-deprived and Tai-deficient old males, respectively. Exogenous JH injection into young males resulted in precocious sexual maturation and this JH induction was suppressed by Tai silencing. Our results demonstrate that Tai is an actor of the JH signaling pathway that operates in ALs and ASGs to promote pheromone information processing and consequently the display of sexual behavior in synchrony with ASG maturation, ultimately optimizing male reproductive success. Thus, this study provides additional insights into the molecular mechanisms underlying hormonal regulation of sexual maturation in insects.

Image, graphical abstract

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