Juvenile Hormone and Insulin Regulate Trehalose Homeostasis in the Red Flour Beetle, Tribolium castaneum

Jingjing Xu,Subba Reddy Palli,Zhentao Sheng,Eric Rulifson

doi:10.1371/journal.pgen.1003535

Abstract

Insulin/IGF-1 signaling (IIS) has been well studied for its role in the control of life span extension and resistance to a variety of stresses. The Drosophila melanogaster insulin-like receptor (InR) mutant showed extended life span due to reduced juvenile hormone (JH) levels. However, little is known about the mechanism of cross talk between IIS and JH in regulation of life span extension and resistance to starvation. In the current study, we investigated the role of IIS and JH signaling in regulation of resistance to starvation. Reduction in JH biosynthesis, JH action, or insulin-like peptide 2 (ILP2) syntheses by RNA interference (RNAi)-aided knockdown in the expression of genes coding for juvenile hormone acid methyltransferase (JHAMT), methoprene-tolerant (Met), or ILP2 respectively decreased lipid and carbohydrate metabolism and extended the survival of starved beetles. Interestingly, the extension of life span could be restored by injection of bovine insulin into JHAMT RNAi beetles but not by application of JH III to ILP2 RNAi beetles. These data suggest that JH controls starvation resistance by regulating synthesis of ILP2. More importantly, JH regulates trehalose homeostasis, including trehalose transport and metabolism, and controls utilization of stored nutrients in starved adults.

Highlights

Many biological functions of juvenile hormone (JH) in regulation of almost every aspect of an insect’s life have been reported since its discovery in 1965 [1,2]
To maintain the larval state, JH induces the expression of the genes coding for transcription factors such as Kr-h1 to prevent metamorphosis; knockdown in the expression of the gene coding for Kr-h1 by RNA interference (RNAi) in larvae leads to precocious metamorphosis that cannot be rescued by exogenous JH application [3]
JH suppresses imaginal disc growth promoted by nutrition [4], and the nutritional signals mediated by insulin/IGF signaling (IIS) can override JH suppression [5]; but, in the absence of JH, the wing disc grows despite severe starvation

Summary

Introduction

Many biological functions of juvenile hormone (JH) in regulation of almost every aspect of an insect’s life have been reported since its discovery in 1965 [1,2]. JH suppresses imaginal disc growth promoted by nutrition [4], and the nutritional signals mediated by insulin/IGF signaling (IIS) can override JH suppression [5]; but, in the absence of JH, the wing disc grows despite severe starvation. The wing disc growth is well correlated with trehalose levels during the larval stage until the critical weight is reached; starvation causes a decline in hemolymph glucose and trehalose and cessation of wing imaginal disk growth, which can be rescued by injection of trehalose. After reaching the critical weight, the trehalose response to starvation disappears and the action of insulin becomes decoupled from nutrition. The wing disks lose their sensitivity to repression by JH [6]

Methods

Results

Discussion

Conclusion