Abstract

A strategy known as diapause (developmental arrest) has evolved in insects to increase their survival rate under harsh environmental conditions. Diapause causes a dramatic reduction in the metabolic rate and drastically extends lifespan. However, little is known about the mechanisms underlying the metabolic changes involved. Using gas chromatography-mass spectrometry, we compared the changes in the metabolite levels in the brain and hemolymph of nondiapause- and diapause-destined cotton bollworm, Helicoverpa armigera, during the initiation, maintenance, and termination of pupal diapause. A total of 55 metabolites in the hemolymph and 52 metabolites in the brain were detected. Of these metabolites, 21 and 12 metabolite levels were altered in the diapause pupal hemolymph and brain, respectively. During diapause initiation and maintenance, the number of metabolites with increased levels in the hemolymph of the diapausing pupae is far greater than the number in the nondiapause pupae. These increased metabolites function as an energy source, metabolic intermediates, and cryoprotectants. The number of metabolites with decreased levels in the brain of diapausing pupae is far greater than the number in the nondiapause pupae. Low metabolite levels are likely to directly or indirectly repress the brain metabolic activity. During diapause termination, most of the metabolite levels in the hemolymph of the diapausing pupae rapidly decrease because they function as energy and metabolic sources that promote pupa-adult development. In conclusion, the metabolites with altered levels in the hemolymph and brain serve as energy and metabolic resources and help to maintain a low brain metabolic activity during diapause.

Highlights

  • Most insect species have evolved an adaptive strategy known as diapause to survive an unfavorable season [1,2]

  • H. armigera pupal diapause is initiated by exposing 5th–6th instar larvae under short day (10 h light: 14 h dark) and 20 uC conditions, and the lifespan is over three times than in their nondiapause counterparts reared under long day (14 h light: 10 h dark) and 25 uC without diapause

  • The gas chromatography-mass spectrometry (GC-MS) analyses of diapause H. armigera pupal hemolymph and brain successfully identified a cluster of metabolites that are involved in carbohydrate metabolism, amino acid metabolism, as well as polyol and fatty acid metabolism during the initiation, maintenance, and termination of pupal diapause

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Summary

Introduction

Most insect species have evolved an adaptive strategy known as diapause (developmental arrest) to survive an unfavorable season [1,2]. Diapause is typically characterized by reduced metabolic activity and enhanced stress tolerance and is induced by environmental signals (day length, temperature, etc.). The neuroendocrine system translates the physical signals into hormonal factors that induce the individual to enter diapause. In the cotton bollworm, Helicoverpa armigera that is an important agricultural noctuid moth in the world, its pupal diapause is induced by incubating larvae under short day-light and low-temperature conditions that down-regulate the expression of neuropeptide prothoracicotropic hormone (PTTH) in the pupal brain. The low PTTH expression level inhibits the prothoracic glands from synthesizing steroid hormone ecdysteroids (or ecdysone), which are needed to promote continuous development [3]. H. armigera pupal diapause is initiated by exposing 5th–6th instar larvae under short day (10 h light: 14 h dark) and 20 uC conditions, and the lifespan is over three times than in their nondiapause counterparts reared under long day (14 h light: 10 h dark) and 25 uC without diapause

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