Abstract
BackgroundDiapause 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.ResultsShort 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-015-1907-4) contains supplementary material, which is available to authorized users.
Highlights
Diapause is a developmental alternative to direct ontogeny in many invertebrates
In this paper, we first report on profound and characteristic differences in gene expression levels associated with photoperiodic conditions (SD vs. Long Day (LD)), which trigger different developmental destinies in photoperiod-sensitive early 3rd instar wild-type larvae of C. costata; secondly, we report on fast, massive and directed change in the gene expression pattern after the transfer of wild-type larvae from LD to Short Day (SD) conditions
Our data suggest that the diapause phenotype in C. costata larvae might be importantly regulated by epigenetic processes such as alternative histone marking by methylation, alternative splicing and small RNA-mediated regulation of gene expression, and by factors which influence gene transcription (e2f2, vrille) and protein translation
Summary
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. Diapause is an environmentally programmed and hormonally regulated period of dormancy in invertebrates [1, 2]. First and foremost, diapause represents a central part of the life-cycle in many species and secures their survival over unfavourable seasons [3, 4]. Environmental seasonal cues, most often photoperiod, are perceived during a species-specific sensitive stage and transduced into one of two ontogenetic alternatives: direct development versus diapause development [5]. The active lifestyle and the ontogenetic processes are transiently (for the harsh season) but dramatically turned off. The period of developmental arrest during diapause is not static but rather represents a dynamic succession of more or less clearly expressed ecophysiological phases of induction, preparation, initiation, maintenance and termination [6]
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