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Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly.

ABSTRACT: Diapause is a widespread adaptation to seasonality across invertebrate taxa. It is critical for persistence in seasonal environments, synchronizing life histories with favorable, resource-rich conditions and mitigating exposure to harsh environments. Despite some promising recent progress, however, we still know very little about the molecular modifications underlying diapause. We used transcriptional profiling to identify key groups of genes and pathways differentially regulated during pupal diapause, dynamically regulated across diapause development, and differentially regulated after diapause was pharmacologically terminated in the flesh fly Sarcophaga crassipalpis. We describe major shifts in stress axes, endocrine signaling, and metabolism that accompany diapause, several of which appear to be common features of dormancy in other taxa. To assess whether invertebrates with different diapause strategies have converged toward similar transcriptional profiles, we use archived expression data to compare the pupal diapause of S. crassipalpis with the adult reproductive diapause of Drosophila melanogaster and the larval dauer of Caenorhabditis elegans. Although dormant invertebrates converge on a few similar physiological phenotypes including metabolic depression and stress resistance, we find little transcriptional similarity among dormancies across species, suggesting that there may be many transcriptional strategies for producing physiologically similar dormancy responses.

SUBMITTER: Ragland GJ

PROVIDER: S-EPMC2930464 | biostudies-literature | 2010 Aug

REPOSITORIES: biostudies-literature

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Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly.

Ragland Gregory J GJ Denlinger David L DL Hahn Daniel A DA

Proceedings of the National Academy of Sciences of the United States of America 20100728 33

Diapause is a widespread adaptation to seasonality across invertebrate taxa. It is critical for persistence in seasonal environments, synchronizing life histories with favorable, resource-rich conditions and mitigating exposure to harsh environments. Despite some promising recent progress, however, we still know very little about the molecular modifications underlying diapause. We used transcriptional profiling to identify key groups of genes and pathways differentially regulated during pupal di ...[more]

PMID: 20668242

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Project description:BACKGROUND:Diapause is a developmental alternative to direct ontogeny in many invertebrates. Its primary adaptive meaning is to secure survival over unfavourable seasons in a state of developmental arrest usually accompanied by metabolic suppression and enhanced tolerance to environmental stressors. During photoperiodically triggered diapause of insects, the ontogeny is centrally turned off under hormonal control, the molecular details of this transition being poorly understood. Using RNAseq technology, we characterized transcription profiles associated with photoperiodic diapause induction in the larvae of the drosophilid fly Chymomyza costata with the goal of identifying candidate genes and processes linked to upstream regulatory events that eventually lead to a complex phenotypic change. RESULTS:Short day photoperiod triggering diapause was associated to inhibition of 20-hydroxy ecdysone (20-HE) signalling during the photoperiod-sensitive stage of C. costata larval development. The mRNA levels of several key genes involved in 20-HE biosynthesis, perception, and signalling were significantly downregulated under short days. Hormonal change was translated into downregulation of a series of other transcripts with broad influence on gene expression, protein translation, alternative histone marking by methylation and alternative splicing. These changes probably resulted in blockade of direct development and deep restructuring of metabolic pathways indicated by differential expression of genes involved in cell cycle regulation, metabolism, detoxification, redox balance, protection against oxidative stress, cuticle formation and synthesis of larval storage proteins. This highly complex alteration of gene transcription was expressed already during first extended night, within the first four hours after the change of the photoperiodic signal from long days to short days. We validated our RNAseq differential gene expression results in an independent qRT-PCR experiment involving wild-type (photoperiodic) and NPD-mutant (non-photoperiodic) strains of C. costata. CONCLUSIONS:Our study revealed several strong candidate genes for follow-up functional studies. Candidate genes code for upstream regulators of a complex change of gene expression, which leads to phenotypic switch from direct ontogeny to larval diapause.

Project description:Insects use diapause, a programmed period of dormancy, to avoid stressful times of the year and to exploit seasonal times of resource availability. Because most diapausing insects do not feed, they must live off their body reserves for several months and the proper use of metabolic reserves is critical for surviving diapause and performing after diapause termination. Across multiple insects, metabolic depression during diapause has been associated with a switch from aerobic metabolism to facultative anaerobic metabolism, despite insects not suffering environmental oxygen limitation. While metabolic rates are depressed during diapause overall to save energy, some insects show regular cyclical bouts of higher metabolic activity during diapause. The functional importance of these metabolic cycles and the mechanisms underlying these cycles are still unknown, but they may be critical for properly maintaining the balance between energy states and purge the accumulation of anaerobic metabolic byproducts. In the present study, we will test the hypothesis that periodic cycles of increased metabolism during insect diapause are associated with both regenerating organismal energetic states, particularly ATP that may decline during metabolic depression, and for purging metabolites associated with anaerobic metabolism. We will use a combination of non-targeted uHPLC-MS/MS metabolomics and targeted NMR-spectroscopy to identify and quantify metabolites that are altered during the cycles in diapausing pupae of the flesh fly, Sarcophaga crassipalpis. This work will allow us to propose specific biochemical and cellular hypotheses for the regulation of cyclic releases from metabolic depression in diapausing insects. Our work may not only reveal the physiological mechanisms regulating metabolic cycles during diapause in flesh fly, but also provide insight to understand the regulation of similar metabolic cycles in mammalian hibernators (i.e., periodic arousal), and also provide insights into how these cycles could be exploited to disrupt the diapause of insect pests.

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Dataset Information

Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly.

Publications

Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly.

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