The insulin and ecdysone pathways as regulators of diapause termination: transcriptional and protein insights from Pieris napi

胰岛素和蜕皮激素通路作为滞育终止的调节因子:来自菜粉蝶的转录和蛋白质研究

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Abstract

Insect diapause is a pre-programmed alternative developmental pathway induced to survive adverse environmental conditions and is characterized by an absence of development, metabolic suppression and increased stress resistance. While the hormonal regulation of diapause induction has been studied extensively, clear molecular hypotheses on how low-temperature driven diapause termination is controlled are lacking. Here we propose a hypothesis for this low-temperature driven diapause termination, which was synthesized from literature research and an experimental study where we correlate gene expression levels and protein abundance of key regulators to transitions across diapause stages. This hypothesis states that the forkhead transcription factor FoxO silences the reception of ecdysone by binding to the ecdysone receptor. This binding is gradually degraded by the accumulation of insulin signalling, in response to low temperatures, which causes the phosphorylation of FoxO. The continuous increase of sensitivity to ecdysone leads to the termination of diapause. We find that, across diapause, components of the PTTH–ecdysone axis, including PTTH signalling and downstream ecdysone-responsive genes, are present in low transcript and protein abundance, suggesting that developmental hormone signalling remains downregulated throughout diapause maintenance. Second, multiple elements of the insulin signalling pathway, including insulin-like peptides and core downstream kinases, are found in higher transcript abundance under prolonged low-temperature conditions, consistent with a role for insulin signalling in environmental sensing during diapause. Finally, FoxO shows high transcript and protein abundance at diapause initiation, followed by a gradual decline toward diapause termination, and FoxO protein abundance is negatively associated with insulin pathway activity. The main connection between the insulin pathway and FoxO, the protein kinase B (AKT) does not display the expected mRNA and protein levels. However, there are multiple factors contributing to the connection between insulin and FoxO and there might be another one involved in diapause. Simultaneously, ecdysone receptor components display stage-specific transcript–protein mismatches, indicating post-transcriptional regulation of hormonal sensitivity. Even though these results are correlational and need to be further investigated by experimental work in future studies, they support the proposed hypothesis. Summarizing, we propose a model in which cold-induced insulin signalling promotes FoxO degradation, progressively releasing inhibition of the ecdysone receptor and restoring ecdysone sensitivity, thereby timing diapause termination. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-026-12747-2.

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