Abstract
BackgroundDiapause is a seasonal dormancy that allows organisms to survive unfavorable conditions and optimizes the timing of reproduction and growth. Emergence from diapause reverses the state of arrested development and metabolic suppression returning the organism to an active state. The physiological mechanisms that regulate the transition from diapause to post-diapause are still unknown. In this study, this transition has been characterized for the sub-arctic calanoid copepod Neocalanus flemingeri, a key crustacean zooplankter that supports the highly productive North Pacific fisheries. Transcriptional profiling of females, determined over a two-week time series starting with diapausing females collected from > 400 m depth, characterized the molecular mechanisms that regulate the post-diapause trajectory.ResultsA complex set of transitions in relative gene expression defined the transcriptomic changes from diapause to post-diapause. Despite low temperatures (5–6 °C), the switch from a “diapause” to a “post-diapause” transcriptional profile occurred within 12 h of the termination stimulus. Transcriptional changes signaling the end of diapause were activated within one-hour post collection and included the up-regulation of genes involved in the 20E cascade pathway, the TCA cycle and RNA metabolism in combination with the down-regulation of genes associated with chromatin silencing. By 12 h, females exhibited a post-diapause phenotype characterized by the up-regulation of genes involved in cell division, cell differentiation and multiple developmental processes. By seven days post collection, the reproductive program was fully activated as indicated by up-regulation of genes involved in oogenesis and energy metabolism, processes that were enriched among the differentially expressed genes.ConclusionsThe analysis revealed a finely structured, precisely orchestrated sequence of transcriptional changes that led to rapid changes in the activation of biological processes paving the way to the successful completion of the reproductive program. Our findings lead to new hypotheses related to potentially universal mechanisms that terminate diapause before an organism can resume its developmental program.
Highlights
Diapause is a seasonal dormancy that allows organisms to survive unfavorable conditions and optimizes the timing of reproduction and growth
Diapause and post-diapause states have distinct transcriptional phenotypes The existence of distinct transcriptional phenotypes within a set of samples can be inferred by the approaches described in methods and in particular by the occurrence of clusters in a t-distributed Stochastic Neighbor Embedding (t-SNE) dimensionality-reduction plot
Gene expression analysis confirmed the presence of large differences in transcriptional profiles from T0 to T14d as indicated by more than 14,000 differentially expressed genes (DEGs) identified across all samples (p ≤ 0.05 after followed by likelihood ratio tests (FDR) correction)
Summary
Diapause is a seasonal dormancy that allows organisms to survive unfavorable conditions and optimizes the timing of reproduction and growth. The molecular basis of such major physiological transitions is fundamentally interesting, in particular the transition from diapause to post-diapause, which requires the restart of a diverse set of biological processes such as development, metabolic activation, muscle function, cell division and digestion [5, 6]. We investigated this transition in an organism with adult-female diapause, where the primary biological process during post-diapause is the completion of the reproductive program [7, 8]
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